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Androgen control of vocal control region volumes in a wild migratory songbird (Junco hyemalis) is region and possibly age dependent
Abstract
Previous laboratory studies have shown that photoperiodic adult songbirds experience seasonal variations in singing frequency that correlate with plasma androgen levels, as well as changes in the brain regions that control singing (vocal control regions). The present study investigates naturally occurring seasonal changes in the sizes of these regions in a wild migratory species (dark-eyed junco, Junco hyemalis), with samples from adolescence to post-breeding fall migration. In adult males, the volumes of the vocal control regions area X and the higher vocal center (HVC) were large during the breeding season when birds were singing and androgen levels were high, and decreased in size after the breeding season when singing had stopped and androgen levels were low. HVC volume in adolescent males caught in the fall (no singing), when plasma androgen levels were low, was smaller than in breeding adults, thereby following the seasonal pattern of change in plasma androgen levels. In adolescent males, however, area X volume was the same as in breeding adults. Thus, area X size in adolescent male juncos may be testosterone independent. The seasonal pattern of robust nucleus of the archistriatum volume was similar to that of the HVC. The volumes of neither the magnocellular nucleus of the anterior neostriatum nor the nucleus rotundus, a control region, differed seasonally. Castration of breeding adult males caused both area X and HVC volumes to decrease compared to castrated controls with testosterone replacement, indicating that maintenance of these two region volumes is testosterone dependent in adults.
... We expected males to have high plasma T during the breeding season compared to other times of the year, as a result of the HPG axis (see review: Wingfield and Sapolsky, 2003). Plasma T has been shown to increase at the onset of breeding and aid in SCR neuroplasticity, testicular development, and breeding behavior, such as singing (Nottebohm, 1980;Brenowitz et al., 1991;Rasika et al., 1994;Gulledge and Deviche, 1997;Gulledge and Deviche, 1998;Smith et al., 1997a;Dloniak and Deviche, 2001;Strand and Deviche, 2007). In monogamous bird species, such as Dark-eyed Juncos and House Finches, T declines soon after pair formation, possibly because T is costly to make, decreases paternal behavior, increases aggression (and therefore exposure), and decreases immunity (Hegner and Wingfield, 1987;Wingfield et al., 1990;Ketterson et al., 1992;Casto et al., 2001). ...
... In songbirds, however, plasma T is the primary mechanism mediating seasonal neuroplasticity (Nottebohm et al., 1987;Smith et al., 1995;Gulledge and Deviche, 1997;Strand and Deviche, 2007), and high stress and CORT levels decrease plasma T concentrations (Dong et al., 2004;Hardy et al., 2005;Deviche et al., 2010; also see review: Wingfield and Sapolsky, 2003). Stress may affect T concentrations by decreasing LH secretion, decreasing the sensitivity of the gonads to LH, or directly inhibiting T production (Wingfield and Sapolsky, 2003;Deviche et al., 2010). ...
... We hypothesized that stress would reduce neurogenesis and neuroplasticity in the SCRs of House Finches. This is because previous studies found that 1) high T contributes to the growth of SCRs seen in spring (Nottebohm, 1980;Brenowitz et al., 1991;Rasika et al., 1994;Gulledge and Deviche, 1997;Smith et al., 1997a;Strand and Deviche, 2007), 2) CORT can decrease T (Dong et al., 2004;Deviche et al., 2010; also see review: Hardy et al., 2005), and 3) CORT is released during stress (Wingfield et al., 1982;1983;1995). Therefore, we predicted that stressed House Finches would have high CORT, low T, and smaller HVC volumes. ...
Song production in songbirds is controlled by parts of the brain known as the song control regions (SCRs). During spring, gonads increase in size, males sing to attract mates, and SCRs become larger. This neuroplasticity is controlled by the change in day length and increased plasma testosterone (T) levels. Plasma T can be reduced by stress through the production of corticosterone (CORT), through the production of beta-endorphin, or through direct effects on the testes via the nervous system. We determined the T, estradiol, and CORT hormonal profiles of wild House Finches by capturing and sampling blood from the finches every season for two years. To track SCR neuroplasticity in the wild, we also measured the volume of two specific SCRs, the HVC and RA, every season. We then examined the effects of stress on the finch endocrine system in the wild by performing a 30-minute restraint stress protocol once every season and took blood samples before and after the restraint. To determine whether stress and/or CORT affect neuroplasticity in SCRs, we captured male house finches during winter and brought them into captivity. They were allowed to acclimate to captivity for one month on short days (8L:16D) before we transferred them to long days (16L:8D) and restraint stressed half the birds. We measured their gonads, plasma T and CORT levels, volumes of the HVC and RA, and the number of new neurons in the HVC. HVC volumes were smaller in stressed than non-stressed birds, while RA volumes did not differ. There was no difference in number of new neurons or estimated total number of neurons in the HVC between control and restrained birds. Because the HVC is involved in song production, it is possible that stress negatively impacts singing behavior and reproductive success in House Finches. Future work should address how natural stressors may affect neuroplasticity in birds.
... In birds, the effects of chronic manipulations of sex steroids have been well described for the song system (Brenowitz, 2004). Following chronic testosterone treatment, males will sing more and adult gonadectomized female canaries under the influence of testosterone acquire male-like song Dloniak and Deviche, 2001;Gulledge and Deviche, 1997;Nottebohm, 1980;Smith et al., 1997b). ...
... Although in birds little is known about the effects of sex steroids on hippocampal morphology, seasonal structural changes in the song system in response to fluctuations in sex steroids illustrate the capacity for plasticity in the avian brain (De Groof et al., 2009;Tramontin and Brenowitz, 2000). Both testosterone and oestrogen contribute to seasonal growth of the song system in males, particularly the HVC, and this increase in volume is positively correlated with rates of singing (Ball et al., 2002;Brenowitz, 2004;Dloniak and Deviche, 2001;Gulledge and Deviche, 1997;Smith et al., 1997b). Testosterone treatment also increases the size of two vocal control nuclei (the HVC and RA) in adult gonadectomized female canaries (Nottebohm, 1980). ...
... In mammals, long-term elevation of plasma sex steroid levels through implants or repeated injections is associated with improved performance on spatial memory tasks including the t-maze, the water maze and the radial-arm maze in rodents and in computer-based assessments in humans (Cherrier et al., 2001;Daniel et al., 1997;Fader et al., 1998;Fader et al., 1999;Gibbs, 2000;Gray et al., 2005;Janowsky et al., 1994;Luine et al., 1998;Sandstrom et al., 2006;Sandstrom and Williams, 2004). Considering how much is known about the effects of chronic manipulations of sex steroids on the song system, it is perhaps surprising how little we know about sex steroid effects on spatial cognition in birds Brenowitz, 2004;Dloniak and Deviche, 2001;Gulledge and Deviche, 1997;Nottebohm, 1980;Smith et al., 1997b). One study found that castrated zebra finches with testosterone or oestrogen implants learnt a spatial task when tested over 20 days, but birds implanted with dihydrotestosterone did not (Oberlander et al., 2004). ...
It is well established in mammals that chronic, long-term elevations in sex steroids
are associated with improvements in spatial cognition. It is less clear the extent to
which short to medium term elevations in sex steroids improve spatial cognition and
change hippocampal morphology, particularly in birds. The avian hippocampus
expresses both androgen receptors (AR) and oestrogen receptor alpha (ERα) and
high levels of the enzyme aromatase that converts testosterone to oestrogen. I began
by comparing spatial cognition, hippocampal sex steroid receptor and aromatase
expression between males and females. There were no differences in spatial or
visual cognition or in hippocampal sex steroid receptor expression between the
sexes, although hippocampal aromatase mRNA expression was higher in males. I
then addressed the effects of acute and medium-term sex steroid treatment on spatial
cognition and hippocampal aromatase and sex steroid receptor expression. A single
treatment of testosterone 30 minutes or four hours prior to cognitive testing improved
spatial performance. Additionally, when testosterone and oestrogen were given daily
for five days spatial cognition in both sexes was improved. The testosterone-induced
improvement was blocked when testosterone was administered in conjunction with
the aromatase inhibitor fadrozole but not when administered with saline. These
findings suggest that spatial cognition is improved by an oestrogenic effect. Thirty
minutes following acute testosterone treatment, plasma testosterone levels,
hippocampal AR and ERα mRNA expression all increased. Five days of oestrogen
treatment increased plasma oestrogen levels, hippocampal ERα mRNA and Nmethyl-
D-aspartate (NMDA) receptor levels in males and females; all were
positively correlated with enhanced spatial cognition on day five of treatment.
Finally, I determined which genes were differentially expressed as a result of five
days of oestrogen treatment. Nineteen genes, identified as being involved in learning
and memory were differentially expressed in the hippocampus, eleven of which were
up-regulated and eight were down-regulated. Taken together these results
demonstrate that oestrogen can improve spatial cognition in birds. It is plausible that
oestrogen acts to improve spatial memory in the hippocampus through upregulation
of genes that control neurotransmitter release, reuptake and receptor levels.
... In contrast, gonadal steroids mediate seasonal VCR volume changes in intact adults. Indeed, these volumes in adult male juncos that were in breeding condition decreased following castration, an effect that was prevented by T treatment to castrates (Gulledge and Deviche, 1997). ...
... In the present work, Area X and MAN were large in both control and T-treated SD photosensitive castrated males. Area X in adolescent male juncos is the same size as in breeding adult males, even though plasma T levels are low in adolescence and high during the breeding season (Gulledge and Deviche, 1997). Taken together, these results suggest that Area X volume increases in a plasma androgen-independent fashion in adolescents in the fall and remains large until early spring, when birds are still exposed to SD and have presumably low T levels. ...
... Taken together, these results suggest that Area X volume increases in a plasma androgen-independent fashion in adolescents in the fall and remains large until early spring, when birds are still exposed to SD and have presumably low T levels. Gulledge and Deviche (1997) found that castrating adult male juncos during the breeding season caused Area X to shrink compared to that of T-treated castrated birds. This indicated that T is necessary to maintain large Area X volumes during the breeding season. ...
A male migratory songbird (dark-eyed junco, Junco hyemalis) was used as a model for studies on the influence of testosterone (T) on feeding, and on interactive effects on this behavior between T and the opioid antagonist naloxone hydrochloride (Nal). Administered chronically to birds exposed to nonstimulating photoperiods, T increased food intake by 30-58% without altering the body mass, the fat index, or the standard metabolic rate. An intramuscular injection of Nal decreased feeding temporarily in a dose-related manner. T-treated juncos exhibited a decreased sensitivity to the anorexic influence of Nal administration, demonstrating that T interacts with opioids to control food consumption. Neuroendocrine mechanisms that potentially account for this interaction are discussed.
... These volumes decrease between summer and fall in parallel with plasma T levels. Furthermore, castration of males in breeding condition caused a reduction in HVc and Area X volumes that was prevented by T replacement at physiological doses (Gulledge and Deviche, 1997). Other investigations likewise identified an important role for T in the control of adult male VCR sizes (Brown and Bottjer, 1993; Bernard and Ball, 1997; Smith et al., 1997a). ...
... The volume of MAN increased between summer and fall in males. The significance of this result is unclear because in a previous study, male junco MAN volumes did not change seasonally and did not differ between castrated birds that did or did not receive exogenous T (Gulledge and Deviche, 1997). Seasonal changes in HVc, Area X, and probably RA volumes in male juncos are partly regulated by circulating T concentrations. ...
... These volumes decrease between summer and fall in parallel with plasma T levels. Furthermore, castration of males in breeding condition caused a reduction in HVc and Area X volumes that was prevented by T replacement at physiological doses (Gulledge and Deviche, 1997). Other investigations likewise identified an important role for T in the control of adult male VCR sizes (Brown and Bottjer, 1993; Smith et al., 1997a). ...
Previous research established that in several species of seasonally breeding oscine birds, brain areas [vocal control regions (VCRs)] that control vocal behavior learning and expression exhibit seasonal plasticity, being larger during than outside the reproductive period. In adult males, this seasonal decrease correlates with circulating testosterone (T) concentrations. VCRs contain androgen receptors and T plays an important role in neural plasticity and in the control of singing behavior. In behaviorally dimorphic species, VCRs are larger in males than females and change seasonally also in females, but the dependency of these changes on circulating T levels in females has not been established. In free-living adult dark-eyed juncos (Junco hyemalis), a species in which females do not normally sing, the sizes of three VCRs (high vocal center, robust nucleus of the archistriatum, and Area X) were larger in males than females and decreased between summer and fall in both sexes. In males, this decrease was associated with changes in circulating T concentrations. Females, however, had on average undetectable T levels throughout the breeding season. Seasonal changes in VCR volumes in adult females may depend on very low (below detection limit) circulating T concentrations, on nonandrogenic plasma steroids, on androgen (or androgen metabolites) produced in brain tissues, and/or on nonsteroidal factors such as photoperiod or social interactions with conspecific birds.
... Area X and MAN are essential for song learning Bottjer, Meismer, and Arnold, 1984;Sohrabji, Nordeen, and Nordeen, 1990;Scharff and Nottebohm, 1991), whereas HVc and RA are necessary for song expression . The vocal control system exhibits neuronal plasticity throughout adulthood in many species (Nottebohm, Nottebohm, and Crane, 1986;Smith, 1996;Brenowitz, Nalls, Wingfield, and Kroodsma, 1991;Gulledge and Deviche, 1997). In seasonally breeding adult songbirds, VCR volumes are larger during than after the breeding season (Smith, 1996;Smith, Brenowitz, Beecher, and Wingfield, 1997a;Gulledge and Deviche, 1997;Deviche and Gulledge, 2000). ...
... The vocal control system exhibits neuronal plasticity throughout adulthood in many species (Nottebohm, Nottebohm, and Crane, 1986;Smith, 1996;Brenowitz, Nalls, Wingfield, and Kroodsma, 1991;Gulledge and Deviche, 1997). In seasonally breeding adult songbirds, VCR volumes are larger during than after the breeding season (Smith, 1996;Smith, Brenowitz, Beecher, and Wingfield, 1997a;Gulledge and Deviche, 1997;Deviche and Gulledge, 2000). Changes similar to those observed in free-living birds occur in captive birds exposed to breeding versus nonbreeding photoperiods or T concentrations (Nottebohm, 1981;Brenowitz et al., 1991;Smith, Brenowitz, Wingfield, and Baptista, 1995;Gulledge and Deviche, 1997). ...
... In seasonally breeding adult songbirds, VCR volumes are larger during than after the breeding season (Smith, 1996;Smith, Brenowitz, Beecher, and Wingfield, 1997a;Gulledge and Deviche, 1997;Deviche and Gulledge, 2000). Changes similar to those observed in free-living birds occur in captive birds exposed to breeding versus nonbreeding photoperiods or T concentrations (Nottebohm, 1981;Brenowitz et al., 1991;Smith, Brenowitz, Wingfield, and Baptista, 1995;Gulledge and Deviche, 1997). The effects of T on VCR volumes and singing are presumably mediated by androgen receptors located in HVc, RA, and MAN (Arnold, Nottebohm, and Pfaff, 1976;Smith, Brenowitz, and Prins, 1996). ...
In seasonally breeding male oscines, song learning and expression are controlled by brain regions (vocal control regions, VCRs) that exhibit seasonal neural plasticity in adulthood. Several VCRs contain androgen receptors, and gonadal androgens play important roles in the control of seasonal structural and functional changes of VCRs. Recent studies also found that adult VCRs are influenced by factors other than gonadal hormones, including photoperiod, but the relative importance of these factors and their mechanisms of action are poorly understood. To address this issue, we investigated the contributions of photoperiod and testicular androgens to the regulation of VCR volumes and to the control of song expression in adult dark-eyed juncos, Junco hyemalis. Exposing castrated (CX) photosensitive males to long days (LD) enhanced their high vocal center (HVc) volumes compared to those of males held on short days (SD). These volumes were not further increased by concurrent testosterone (T) treatment, revealing a marked and gonadal androgen-independent stimulatory influence of photoperiod on the size of this brain region. HVc sizes were smaller in LD-exposed photorefractory than photosensitive males irrespective of whether birds were intact or had been castrated before photoperiodic manipulations, but HVc sizes increased in response to T treatment in intact photorefractory males. Thus, LD exposure can increase HVc volumes in the absence of gonadal T, but large volume induction in photorefractory males requires elevated plasma T levels. Testosterone treatment of SD-exposed photosensitive males increased HVc, but not Area X, MAN, or RA volumes. Only T-treated males sang and this treatment given to castrates was equally effective behaviorally when administered to photosensitive, photostimulated, or photorefractory juncos. This result indicates that the stimulating influence of LD exposure on HVc volumes is insufficient to induce song in the absence of elevated plasma T levels.
... If this were the case, they would have been noticed long ago and performing a meta-analysis would have been a superfluous exercise. Nobody will deny that every study has its idiosyncrasies which are never the same from study to study, even when performed on the same species by the same investigators (see, for example , the dark-eyed junco telencephalon data from Deviche and Gulledge inTable 1; Deviche and Gulledge, 2000; Gulledge and Deviche, 1997). Nevertheless, across all this " noise, " some patterns do emerge. ...
... Huang et al. (1998) also found seasonal changes in neurogenesis in thalamic, hypothalamic, and brainstem nuclei in golden hamsters (Mesocricetus auratus). Because changes take place in several nontelencephalic areas as well, it is unlikely that the seasonal variation in Tel volume in birds is due solely to the changes in the song system, which is part of the Tel (Brenowitz et al., 1998; Gulledge and Deviche, 1997; Kirn et al., 1989; Li, Fu, and Zhang, 1996; Nottebohm, 1981; Smith, 1996; Smith et al., 1997a). In addition, the absolute changes in the song system are too small to cause the observed effects of an on average 1 2 SD increase in total Tel volume. ...
... Treatment of male birds (whether castrated or intact ) with testosterone mimics certain effects of a natural breeding season: males will sing more, perform other behaviors related to mating or mate attraction (e.g., De Ridder, Pinxten, and Eens, 2000; Ketterson, Nolan, Wolf, and Ziegenfus, 1992; Nowicki and Ball, 1989; Schoech, Ketterson, Nolan, Sharp, and Buntin, 1998; Wingfield, Jacobs, and Hillgarth, 1997), and their song system nuclei increase in size (e.g., Dloniak and Deviche, 2001; Gulledge and Deviche, 1997; Nottebohm, 1980; Smith et al., 1997b). It was therefore surprising to find that in those same T-treated birds, Tel, Rt, and Pt volumes decreased. ...
A meta-analysis of the literature shows that in adult male songbirds, brain mass, telencephalon volume and n. rotundus (a thalamic visual nucleus) volume increase from the nonbreeding season (low testosterone) to the breeding season (higher testosterone). These effects can at least partially be mimicked by photoperiod manipulations in captivity. In contrast, an artificial testosterone (T) titer increase by chronic implants yields the opposite results: telencephalon, n. rotundus, and n. pretectalis volumes are lower in T-treated animals than in controls. These results suggest that artificial testosterone manipulations do not necessarily mimic the effects of natural variations in hormone levels and that results from experiments using T implants to mimic natural hormonal effects should be interpreted with caution.
... Once SCRs attain maximal size, their volumes are maintained by extending cell survival and by neuronal replacement [Alvarez-Buylla et al., 1992]. In many seasonally breeding species, SCR volumes are larger during the breeding (singing) season when circulating concentrations of gonadal steroids are elevated than after this season when steroid concentrations have decreased [Nottebohm et al., 1986;Gulledge and Deviche, 1997;Smith et al., 1997]. Castration of males in breeding condition causes HVC and Area X to shrink to a similar degree as naturally occurs at the end of the breeding season [Gulledge and Deviche, 1997]. ...
... In many seasonally breeding species, SCR volumes are larger during the breeding (singing) season when circulating concentrations of gonadal steroids are elevated than after this season when steroid concentrations have decreased [Nottebohm et al., 1986;Gulledge and Deviche, 1997;Smith et al., 1997]. Castration of males in breeding condition causes HVC and Area X to shrink to a similar degree as naturally occurs at the end of the breeding season [Gulledge and Deviche, 1997]. Further, T treatment to newly castrated or intact photoregressed adult males maintains or increases, respectively, SCR volumes, confirming that sex steroids control these volumes [Gulledge and Deviche, 1997;Dloniak and Deviche, 2001]. ...
... Castration of males in breeding condition causes HVC and Area X to shrink to a similar degree as naturally occurs at the end of the breeding season [Gulledge and Deviche, 1997]. Further, T treatment to newly castrated or intact photoregressed adult males maintains or increases, respectively, SCR volumes, confirming that sex steroids control these volumes [Gulledge and Deviche, 1997;Dloniak and Deviche, 2001]. ...
In seasonally breeding adult male songbirds, the volumes of several song control regions (SCRs) change seasonally in parallel with plasma testosterone (T) levels and decrease following gonadectomy. Testosterone treatment to castrates prevents this decrease, indicating T dependency. During the breeding season, second-year (SY: birds entering their first breeding season) free-ranging male Dark-eyed Juncos (Junco hyemalis) have smaller testes than older (after second-year, ASY: birds entering at least their second breeding season) birds. SY males also have lower plasma T concentrations than ASY males at the beginning of the breeding season. We investigated differences in song structure of the two age groups and the relationship between age differences in gonadal function and SCR sizes. The average number of syllables per song, syllable duration, trill rate, song duration, and variability in song duration were age-independent. Two brain regions that are thought to be involved primarily in song learning and perception were 13 and 18% larger, respectively, in SY than in ASY males, the opposite of what would be expected based solely on reproductive measures (testis mass and cloacal protuberance width). In contrast, the volumes of two regions that directly control song expression did not differ with age. The lack of age-related size differences in regions that are required for song production may indicate that male juncos of all ages have similar brain space requirements for motor production. Where there were size differences, they were restricted to regions primarily controlling vocal behavior acquisition/perception, suggesting that first time breeders need more brain space than experienced breeders to acquire crystallized song and/or acoustically perceive aspects of their environment.
... The song nuclei of male GWC S will grow in response to spring environmental conditions in the field or to gradual increases in photoperiod in the laboratory, without T implants (Soma et al., 1998;). Increases in circulating T are primarily responsible for this growth (Gulledge and Deviche, 1997; Smith et al., 1997a; Ball, 2000). Plasma T levels increase slowly over several days in both the field and laboratory, however, and the timing of this increase varies considerably between individual birds (Wingfield and Farner, 1978;). ...
... Our study demonstrates that afferent input is also necessary for the growth of adult brain nuclei in response to seasonal hormonal and photoperiod cues; seasonal growth is a common feature of adult vertebrate brains (for review, see). Previous research demonstrated that seasonal growth of the song circuits is primarily regulated by changes in plasma T levels (Gulledge and Deviche, 1997; Smith et al., 1997a; Ball, 2000). We found that lesions of HVc blocked or decreased the LDTinduced growth of its efferent targets RA and area X in the growth group. ...
The neural circuits that regulate song behavior in adult songbirds undergo pronounced seasonal changes in morphology, primarily in response to changes in plasma testosterone (T). Most song nuclei have T receptors. We asked whether seasonal growth and maintenance of nuclei within these circuits are direct responses to the effects of T or its metabolites or are mediated indirectly via the effects of T on afferent nuclei. Photosensitive white-crowned sparrows were exposed to one of three treatments. (1) The neostriatal nucleus HVc (also known as the "high vocal center") was lesioned unilaterally, and the birds were exposed to long-day (LD) photoperiods and breeding levels of T for 30 d. (2) Birds were exposed to LD plus T (LD+T) for 30 d; then HVc was lesioned, and the birds were killed after an additional 30 d exposure to LD+T. (3) HVc was lesioned, and the sparrows were housed on short-day (SD) photoperiods in the absence of T treatment for 30 d. In both LD+T groups, the direct efferent targets of HVc, the robust nucleus of the archistriatum (RA) and area X, were smaller ipsilateral to the lesion. The lesion did not prevent growth of the hypoglossal motor nucleus, which does not receive direct afferent input from HVc. RA and area X were also smaller ipsilateral to the lesion in the SD birds. These results indicate that afferent input is required both for the growth of adult song circuits in response to typical breeding photoperiod and hormone conditions and for the maintenance of efferent nuclei in either their regressed or enlarged states.
... For example , songs produced by both wild and domesticated adult canaries (Serinus canarius) are stable during the spring breeding season, but are modified mainly during the fall and winter (Nottebohm et al., 1986, 1987; Leitner et al., 2001). These behavioral changes appear to be driven primarily by photoperiod–induced changes in T secretion (Smith et al., 1995, 1997; Gulledge and Deviche, 1997; Brenowitz et al., 1998; Ball, 2000; Tramontin et al., 2000). Vocal stability in the early spring is associated with high plasma T levels stimulated by increasing day length. ...
... For example , songs produced by both wild and domesticated adult canaries (Serinus canarius) are stable during the spring breeding season, but are modified mainly during the fall and winter (Nottebohm et al., 1986Nottebohm et al., , 1987 Leitner et al., 2001). These behavioral changes appear to be driven primarily by photoperiod–induced changes in T secretion (Smith et al., 1995Smith et al., , 1997 Gulledge and Deviche, 1997; Brenowitz et al., 1998; Ball, 2000;). Vocal stability in the early spring is associated with high plasma T levels stimulated by increasing day length. ...
Developmental changes in the composition and function of N-methyl-D-aspartate receptors (NMDARs) are believed to regulate neural plasticity. For example, in songbirds, vocal learning entails NMDAR activation, and the sensitive period for such learning in zebra finches (ZFs) parallels developmental changes in NMDAR density and phenotype within several song-related brain regions. In contrast to ZFs, canaries exhibit vocal plasticity recurrently throughout adulthood, prompted by seasonal changes in day length and testosterone (T) levels. We used in situ hybridization to determine if such changes in photoperiod affect NMDAR subunit expression in adult canaries. Birds were sacrificed while on short days (SD) when T levels were low, or on long days (LD) when T levels were high. Transcript levels for the constitutive NMDAR subunit (NR1) and two modulatory subunits (NR2A, NR2B) were measured in four song control nuclei: lMAN, Area X, HVc, and RA. NR1 and NR2A mRNA levels were comparable in SD and LD groups in all four song regions studied. However, NR2B mRNA levels within lMAN and RA were significantly higher in SD than in LD birds. Photoperiod did not affect NR2B transcript levels in Area X, HVc, or a nonsong region just lateral to lMAN. Our data support the hypothesis that changes in NMDAR subunit expression may contribute to the neural and behavioral reorganization that accompanies seasonal song remodeling in adulthood.
... Several song control nuclei express receptors for sex steroid hor-mones [9,15,38,39,54,83] and exhibit a prominent plasticity that parallels variations in song behavior. In seasonally breeding species, the volume of the song control nucleus HVC is larger under spring-like (long) photoperiods, when T levels and song displays are high, than under winter-like (short) photoperiods, when T levels and vocal output are low [14,19,27,43,63]. In adult males of some species, the volume of this song control nucleus is positively correlated to the size of the song repertoire [24,57] and/or to the length of the song bout [16]. ...
... The experimental increase of the T levels by implantation of a capsule containing crystalline T significantly increased the volume of the song nuclei HVC and RA as well as singing and the associated courtship display, wing waving. Wing waving was absent at this season in birds that had not been treated with exogenous T. These effects of T on neuroanatomy and reproductive behaviors have been largely documented in starlings and other songbird species [14,25,27,43,62]. ...
The male European starling (Sturnus vulgaris) is an open-ended learner that increases its repertoire throughout life. In parallel, the volume of high vocal center (HVC) is larger in older birds than in yearlings. We labeled with the thymidine analog 5'-bromodeoxyuridine (BrdU) the cells that are generated during the fall in the brain of adult males that were 2 or more years old and in yearling males that were treated with exogenous testosterone (T) or kept intact before BrdU administration. In all subjects, the singing rate was recorded and BrdU-labeled cells were quantified in HVC, in proliferative areas of the ventricular zone (VZ) and in auditory regions. BrdU-containing cells were observed in all brain regions investigated. They were significantly more numerous in the VZ of the T-treated yearlings than in any other group. In older birds, a reduced number of labeled cells was specifically observed in the VZ close to the anterior commissure. No group difference was detected in auditory processing areas or in HVC. These data show for the first time a positive influence of T on the production of new cells at the VZ level in a male songbird and a decrease of this process with age. Furthermore, in T-treated birds, a correlation was observed between the HVC volume and the number of differentiated (round) BrdU-positive cell numbers in HVC on the one hand and song rate on another hand supporting the notion that singing activity is causally related to the T-induced growth of this song control nucleus.
... Studies performed in multiple species have established that circulating testosterone (T) is the most potent physiological factor controlling this seasonal anatomical plasticity. Castration significantly attenuates the seasonal growth of selected song nuclei Gulledge and Deviche, 1997;Smith et al., 1997a). Exogenous T can "rescue" the effects of castration, and induce song nucleus growth in animals experiencing nonbreeding environmental conditions (Nottebohm, 1980;Johnson and Bottjer, 1993;Rasika et al., 1994;Smith et al., 1997a). ...
... Seasonal anatomical changes in the song control system have been demonstrated in every species of sea-sonally breeding songbird examined . The primary endocrine cue that controls this plasticity is circulating T (Nottebohm, 1980;Johnson and Bottjer, 1993;Rasika et al., 1994;Gulledge and Deviche, 1997;Smith et al., 1997a). The enzymes, however, that convert T to bioactive metabolites such as DHT and E 2 , are present in the adult songbird brain, and the activities of these enzymes change seasonally Schlinger, 1997a;Riters et al., 2001). ...
In seasonally breeding songbirds, the brain regions that control song behavior undergo dramatic structural changes at the onset of each annual breeding season. As spring approaches and days get longer, gonadal testosterone (T) secretion increases and triggers the growth of several song control nuclei. T can be converted to androgenic and estrogenic metabolites by enzymes expressed in the brain. This opens the possibility that the effects of T may be mediated via the androgen receptor, the estrogen receptor, or both. To test this hypothesis, we examined the effects of two bioactive T metabolites on song nucleus growth and song behavior in adult male white-crowned sparrows. Castrated sparrows with regressed song control nuclei were implanted with silastic capsules containing either crystalline T, 5alpha-dihydrotestosterone (DHT), estradiol (E(2)), or a combination of DHT+E(2). Control animals received empty implants. Song production was highly variable within treatment groups. Only one of seven birds treated with E(2) alone was observed singing, whereas a majority of birds with T or DHT sang. After 37 days of exposure to sex steroids, we measured the volumes of the forebrain song nucleus HVc, the robust nucleus of the archistriatum (RA), and a basal ganglia homolog (area X). All three steroid treatments increased the volumes of these three song nuclei when compared to blank-implanted controls. These data demonstrate that androgen and estrogen receptor binding are sufficient to trigger seasonal song nucleus growth. These data also suggest that T's effects on seasonal song nucleus growth may depend, in part, upon enzymatic conversion of T to bioactive metabolites.
... The song control system of songbirds is extremely sensitive to hormonal manipulations. Lower levels of testosterone generally result in small song control nuclei and decreases in singing activity and song repertoire [5,40,41,65,86]. Given this sensitivity, we expected that DDT exposure would result in decreases in the volume of the song control nuclei. ...
... Although increases in stress and direct neurotoxicity could have affected HVC and RA in a similar fashion to the forebrain and brain as a whole (see above), an equally plausible explanation for these changes is endocrine disruption. Both HVC and RA contain relatively high concentrations of androgen receptors [32,56] and the volume of both regions increase with testosterone [2,7,40,80]. p,p -DDE is a potent androgen receptor antagonist and inhibits androgen-induced transcriptional activ- ity [51]. Robins exposed to p,p -DDE are therefore analogous to experimental approaches where birds have been castrated and have correspondingly lower HVC and RA volumes [7]. ...
Dichlorodiphenyltrichloroethane (DDT) is a persistent organochlorine compound found worldwide that causes significant anatomical, physiological and behavioural abnormalities in humans and wildlife. However, little is known about whether environmental exposure to DDT affects the brain. Here, we show that environmental exposure to DDT alters the brains of American Robins (Turdus migratorius) in several ways. Increasing levels of DDT resulted in: (i) smaller brain and relative forebrain volumes; (ii) a reduction in the size of two song nuclei, nucleus robustus arcopallialis (RA) and HVC; and (iii) a drastic reduction in neuronal size and overall volume of nucleus intercollicularis (ICo), a structure that is critical for normal sexual behaviour. These changes likely result from stress, direct neurotoxicity and androgen receptor antagonism by the primary metabolite of DDT, p,p'-DDE and this is corroborated by analyses of brain region volumes and p,p'-DDE levels. Our results therefore demonstrate that environmental exposure to DDT is correlated with significant changes in the brain and specifically those structures related to mating and song. Given the magnitude of these changes in the brain and the fact that environmental DDT exposure was restricted to early development, we conclude that both humans and wildlife that live in DDT contaminated environments may be at risk of neurological damage.
... In addition to the development of the gonads, the SCRs also grow in the spring (Nottebohm, 1981;Kirn et al., 1989;Smith, 1996;Smith et al., 1997a) and T has been identified as a primary initiator of this growth (Nottebohm, 1980;Brenowitz et al., 1991;Rasika et al., 1994;Gulledge and Deviche, 1997;Smith et al., 1997b). Other factors that change in the spring, such as increasing photoperiod (Bernard and Smith et al., 1997b;Whitfield-Rucker and Cassone, 2000;Dloniak and Deviche, 2001) or changes in singing behavior Li et al., 2000;Alvarez-Borda and Nottebohm, 2002; also stimulate SCR growth independently of, or in addition to, circulating T levels. ...
... In the present study, T treatment increased HVC volume by 28%. This increase is smaller than reported in other species because of T treatment (Bernard and Gulledge andDeviche, 1997, Smith et al., 1997b). Furthermore, we found the HVC volume in free-living adult male House Finches to be 73% larger in March than in December (personal observations). ...
In songbirds, testosterone (T) mediates seasonal changes in the sizes and neuroanatomical characteristics of brain regions that control singing (song control regions; SCRs). One model explaining the mechanisms of the growth of one SCR, the HVC, postulates that in the spring increasing photoperiod and circulating T concentrations enhance new neuron survival, thus increasing total neuron number. However, most research investigating the effects of T on new neuron survival has been done in autumn. The present study investigated the effects of photoperiod and T treatment on SCR growth and new neuron survival in the HVC in photosensitive adult male House Finches, Carpodacus mexicanus, under simulated spring-like conditions. Birds were castrated, given T-filled or empty Silastic capsules and maintained on short days (SD; 8L:16D) or long days (LD; 16L:8D). To mark new cells, birds received bromodeoxyuridine injections 11 days after experimental manipulations began and were sacrificed 28 days later. Testosterone treatment increased the sizes of two SCRs, the HVC and Robust nucleus of the arcopallium (RA). Exposure to LD did not affect HVC volume, but did increase RA volume. Testosterone treatment increased the total number of HVC neurons, but did not affect the number of new HVC neurons. Thus, T initiates SCR growth and increases neuron survival, but effects of T on new neuron incorporation may be limited in photosensitive birds under spring-like conditions. These results provide new insight into the effects of photoperiod and T treatment on vernal SCR growth and new neuron incorporation and support current models explaining this growth.
... The avian song control system is one of the best-studied models available to investigate interactions between gonadal steroids and environmental factors on brain plasticity. In many northern temperate zone songbirds, the brain regions controlling singing behavior (song control regions; SCRs) are larger in the spring than in the fall, coinciding with the breeding season and increases in photoperiod, circulating testosterone (T) and singing behavior (Nottebohm, 1981;Brenowitz et al., 1991Brenowitz et al., , 1998Smith, 1996;Gulledge and Deviche, 1997;Smith et al., 1997b). In these species, the primary cue that stimulates the reproductive system and initiates breeding behaviors is the increase in photoperiod, although other cues such as temperature, food availability or social factors often play a role in determining the exact timing of breeding (Wingfield and Kenagy, 1991). ...
... HVC was 23% larger during than before the breeding period. This increase is smaller than reported in other free-living songbirds in which HVC volume increased by up to 188% during the spring breeding season (Smith, 1996;Gulledge and Deviche, 1997;Brenowitz et al., 1998). Furthermore, the seasonal increase in HVC volume in Rufous-winged Sparrows was not associated with an increase in total HVC neuron number. ...
In most temperate zone songbirds, exposure to increasing photoperiod in the spring stimulates the reproductive system and induces reproductive behaviors. Additionally, the brain regions that control singing (song control regions; SCRs) are larger during the breeding season, thus paralleling changes in the activity of the reproductive system. However, in some birds, environmental factors other than photoperiod initiate breeding. For example, free-living male Rufous-winged Sparrows develop their testes in March due to increasing photoperiod, but have relatively low plasma T until after they begin to breed, usually in July, during the monsoon period when day length is declining. We tested the hypothesis that SCRs grow and singing behavior increases after the monsoon rains begin. We captured adult male Rufous-winged Sparrows in July 2002, 7 days before and 20 days after the monsoon rains began, euthanized birds in the field, collected their brains, and measured SCR volumes from sections immunostained for the neuronal marker NeuN. In June and July 2006, we measured song rates in the field before and after the monsoon rains. SCR volumes were larger and singing behavior increased after the onset of the monsoon rains, coinciding with the initiation of breeding. Unlike in other species studied so far, SCR volumes grew as day length was decreasing. Comparative studies utilizing species that do not breed when day length is increasing may provide information on the relative contributions of various environmental factors to SCR neuroplasticity.
... The three pathways converge in the HVC nucleus, which plays a fundamental role in song learning and production (Mello, 2004;Reiner et al., 2004b). It has been observed that vocal areas such as the HVC, RA, and Area X show significant variations in size and shape, even within the same order of birds, and that these differences are closely related to the breeding season (Scharff and Nottebohm, 1991;Smith, 1996;Gulledge and Deviche, 1997;Smith et al., 1997;Brenowitz et al., 1998;Soma et al., 1999;Gahr, 2000;Poirier et al., 2008;Hall et al., 2010;Vellema et al., 2010Vellema et al., , 2011Fitch and Jams, 2015). These morphological variations between species and orders are pertinent to understanding brain organization concerning to song regions and their impact on the specific vocal capabilities of each species. ...
The house wren shows complex song, and the rufous-tailed hummingbird has a simple song. The location of vocal brain areas supports the song’s complexity; however, these still need to be studied. The astrocytic population in songbirds appears to be associated with change in vocal control nuclei; however, astrocytic distribution and morphology have not been described in these species. Consequently, we compared the distribution and volume of the vocal brain areas: HVC, RA, Area X, and LMAN, cell density, and the morphology of astrocytes in the house wren and the rufous-tailed hummingbird. Individuals of the two species were collected, and their brains were analyzed using serial Nissl- NeuN- and MAP2-stained tissue scanner imaging, followed by 3D reconstructions of the vocal areas; and GFAP and S100β astrocytes were analyzed in both species. We found that vocal areas were located close to the cerebral midline in the house wren and a more lateralized position in the rufous-tailed hummingbird. The LMAN occupied a larger volume in the rufous-tailed hummingbird, while the RA and HVC were larger in the house wren. While Area X showed higher cell density in the house wren than the rufous-tailed hummingbird, the LMAN showed a higher density in the rufous-tailed hummingbird. In the house wren, GFAP astrocytes in the same bregma where the vocal areas were located were observed at the laminar edge of the pallium (LEP) and in the vascular region, as well as in vocal motor relay regions in the pallidum and mesencephalon. In contrast, GFAP astrocytes were found in LEP, but not in the pallidum and mesencephalon in hummingbirds. Finally, when comparing GFAP astrocytes in the LEP region of both species, house wren astrocytes exhibited significantly more complex morphology than those of the rufous-tailed hummingbird. These findings suggest a difference in the location and cellular density of vocal circuits, as well as morphology of GFAP astrocytes between the house wren and the rufous-tailed hummingbird.
... Seasonal patterns of circulating T correlate positively with the seasonal growth pattern of the song nuclei (Nottebohm, 1981;Smith, 1996;Smith et al., 1997c;Brenowitz et al., 1998;Soma et al., 1998;. Castration severely attenuates the seasonal growth of the song regions Gulledge and Deviche, 1997;Smith et al., 1997b). Exogenous T induces growth of the song nuclei in castrated males and in nonbreeding males in the fall and winter (Nottebohm, 1980a;Johnson and Bottjer, 1993;Rasika et al., 1994;Smith et al., 1997b;Wennstrom et al., 2001). ...
Birdsong is a complex learned behavior performed by the oscine passerine birds. Birds sing in reproductive and aggressive contexts, but there is a great diversity in song behavior across species, seasons, and sexes. Song learning and production are controlled by a specialized neural circuit, the song control system, that is unique to this group of birds. The growth, maturation, and adult function of this circuit depend on hormonal signals, especially the reproductive steroid hormones. This chapter reviews studies examining the neural control of song and functions of endocrine systems that influence the song control system. They reveal how sex steroids can act to build motor and learning pathways and then stimulate plasticity of these circuits to modify song throughout adult life. Much of the observed behavioral diversity can be accounted for by individual differences in the neural distribution of steroid receptors or in age, sex, or seasonal differences in the gonadal secretion of sex steroids. Songbirds may also synthesize steroids in nongonadal sites and use nontraditional steroids or cellular mechanisms to control song. The evolution in songbirds of multiple mechanisms to synthesize and respond to sex steroids contributes to a growing body of work expanding traditional concepts about the relationship between hormones, brain, and behavior.
... Minor changes in their song repertoire can also happen at later stages (Marler et al. 1962;Titus et al. 1997b). Accordingly, brain nuclei involved in song learning are large during the first year of life, then small during the nonbreeding season, and increase in size seasonally during each breeding season, possibly to facilitate learning to recognize neighbors' songs (Corbitt and Deviche 2005;Gulledge and Deviche 1997). ...
Male dark-eyed juncos sing simple, trilled LRS, with much lower syllable diversity than in other junco species. Development of LRS is peculiar in that some song types are socially learned and shared with other males in the population while others are improvised or invented during development. The input of these novel songs explains the low levels of song sharing among males and buffers against geographic differentiation by cultural mechanisms. In fact, while dark-eyed junco LRS can diverge rapidly, for example under changing acoustical conditions of habitats, LRS differs minimally across the large geographic distribution of subspecies in North America, indicating little potential for mediating reproductive isolation. Simpler LRS than in related species and the use of improvised or invented songs, with the consequent low song sharing among males, are functionally unexpected for a species with the ecological characteristics of dark- eyed juncos. Yet these song traits seem responsible for the low song divergence across subspecies. Explaining those traits functionally is a challenge for future research.
In contrast, SRS of dark-eyed juncos is a quiet, complex vocalization that differs substantially from LRS and is particularly important during courtship. Owing to the fact that SRS is directed to a close receiver, it is likely less affected by selection for efficient sound transmission than LRS, which may facilitate divergence between populations, for example in response to differences in female preferences. Similarly to LRS, the likelihood that SRS will diverge rapidly and serve as a reliable indicator of population origin will depend heavily on how much of SRS is socially learned, an important topic for future study. It is unlikely that SRS is the sole determinant of mating success in juncos, and thus the relative importance of junco courtship signals in each modality (acoustic, visual, olfactory) must be considered to fully understand the potential for premating isolation through divergent courtship signals.
... The seasonal onset of dawn-song production occurred during the period of the shortest day-length of the equatorial region and was accompanied by low circulating levels of testosterone (Figs. 1, 3). This is in contrast to patterns seen in most temperate-zone songbirds, where seasonal activation of singing is achieved by the increase of gonadal testosterone production in concordance with increasing photoperiod [26][27][28]. ...
... Second, seasonal plasticity of singing and song structure and of song nuclei anatomy in males of photoperiodic species is, at least in part, regulated by changes in testosterone levels (e.g. Bernard & Ball, 1997;Gulledge & Deviche, 1997;Small et al., 2007;Smith, Brenowitz, & Wingfield, 1997;Tramontin, Wingfield, & Brenowitz, 2003). Third, exogenous testosterone increases song repertoire size and singing rate in seasonally nonreproductive males (Van Hout, Pinxten, Darras, & Eens, 2012) and exogenous testosterone metabolites modify song nuclei anatomy (Hall & MacDougall-Shackleton, 2012). ...
Variation in song structure and song production of birds are thought to relate to variation of both androgen levels and neural nuclei in the song system, as typically these nuclei are larger in males than in females, vary in size among males and are sensitive to steroid hormones. We investigated the relationships among song and note structure, singing rate, androgen levels and the sizes of two song nuclei, the higher vocal centre (HVC) and the robust nucleus of the arcopallium (RA) in male and female red-backed fairy-wrens, Malurus melanocephalus. Males of this duetting species express three discrete reproductive phenotypes that differ in plumage colour and behaviour. Although HVC and RA structure differed between the sexes, there were no sex differences in note structure and complexity of songs, although females differed from some male types in song rate and frequency characteristics. Both auxiliary males and females had significantly lower androgen levels than the two breeding male phenotypes. Male reproductive phenotypes had similar song characteristics and HVC and RA structure, but differed in androgen levels. Sexes and male phenotypes varied in song rate, but these differences did not correspond to differences in androgen levels. Thus, sex differences in song nuclei anatomy and androgen levels were not associated with differences in song structure and singing rate; and, the differences in androgen levels among male phenotypes were not reflected in differences in singing rate, song structure or the song nuclei. We conclude that, similar to other recent findings, the sexes of the red-backed fairy-wren can produce similar song and express similar singing behaviour despite differences in song system structure and circulating androgen levels; singing and song system anatomy appear not to be part of the suite of traits associated with differences in androgen levels in male red-backed fairy-wrens.
... In duetting species, these brain regions tend not to be sexually dimorphic ( [6], but see [13]). In seasonally breeding songbirds, volumes of song nuclei, as well as the medial preoptic nucleus, are often larger during the breeding season, when males sing a more stereotyped song with greater frequency [7,15,18,30,32,35]. ...
This study investigated relationships among disruption of normal vocal learning, brain derived neurotrophic faction (BDNF), and the morphology of song nuclei in juvenile male zebra finches. The tracheosyringeal nerves were bilaterally transected at post-hatching day 20-25, so that the animals could not properly develop species-typical vocalizations. BDNF protein and the projection from HVC to the robust nucleus of the arcopallium (RA) were quantified during the sensorimotor integration phase of song development. The manipulation decreased the number of BDNF cells in HVC and RA, the volume of these areas defined by BDNF labeling, and the projection from HVC to RA. BDNF was not affected in Area X or the lateral magnocellular nucleus of the anterior nidopallium (LMAN). Thus, inhibition of a bird's ability to practice and/or to hear its own typically developing song during development specifically diminishes BDNF expression in cortical motor regions required for song production.
... Vernal increases in photoperiod correlate with both an increase in plasma T and growth of the song-control system [5]. Conversely, reduction of plasma T via castration induces regression of song-control system nuclei that is reversed with subsequent T replacement [7,8] and exposure to long days characteristic of the breeding season (photostimulation) in castrated adult male white-crowned sparrows does not stimulate song-control system growth [9]. Although overwhelming evidence has implicated T's important role in controlling song-control system growth, other factors have been found to modulate the efficacy of T to induce such plasticity. ...
The song-control system is a network of discrete nuclei in the songbird brain that controls the production and learning of birdsong and exhibits some of the best-studied neuroplasticity found in the adult brain. Photoperiodic growth of the song-control system during the breeding season is driven, at least in part, by the gonadal steroid testosterone. When acting on neural tissue, however, testosterone can be metabolized into 5α-dihydrotestosterone (DHT) or 17β-estradiol (E2), which activate different hormonal signaling pathways. By treating adult starlings with both testosterone metabolites and metabolite antagonists, we attempted to isolate the effects of androgen and estrogen treatment on neuroplasticity during photostimulation in male and female European starlings (Sturnus vulgaris). Photostimulation resulted in a large HVC volume typical of the breeding season in all treatments independent of hormone treatment. E2 had additional effects on HVC growth by reducing neuron density and enhancing early survival of new neurons recruited to HVC in females but did not significantly affect HVC volume. Conversely, DHT reduced the migration of new neurons, assessed by the expression of doublecortin, to HVC. DHT also increased syrinx mass and maintained RA (robust nucleus of the arcopallium) cytoarchitecture in the presence of aromatase inhibitors. In addition, we document the first evidence of sex-specific neuroplastic responses of the song-control system to androgens and estrogens. These findings suggest that the contributions of DHT and E2 signaling in songbird neuroplasticity may be regulated by photoperiod and that future studies should account for species and sex differences in the brain.
... In male canaries, RA is larger in the spring, when circulating levels of T are elevated and song production is at its peak; in the fall, when T levels are low, RA becomes smaller while the overall size of the brain remains constant (Nottebohm 1981 ). Seasonal changes in HVc, RA, area X, and the tracheosyringeal portion of the hypoglossal nerve nucleus (nXIIts) are observed in many species of songbirds , including white-crowned sparrows (Zonotrichia leucophrys) (Smith et al. 1995; Brenowitz et al. 1998 ), rufous-sided towhees (Pipilo erythrophthalmus ) (Brenowitz et al. 1991; Smith 1996 ), dark-eyed juncos (Junco hyemalis ) (Gulledge and Deviche 1997), European starlings (Sturnus vulgaris) (Bernard and Ball 1995), orange bishops (Euplectes franciscanus) (Arai et al. 1989), and red-winged blackbirds (Agelaius phoeniceus) (Kirn et al. 1989). Although the original studies demonstrating seasonal fluctuations in the volume of song-control nuclei were criticized on methodological grounds (Gahr 1990), subsequent studies using multiple staining methods have largely confirmed the original results ( Bottjer 1993, 1995; Bernard and Ball 1995; Smith et al. 1997a Smith et al. , 1997b Soma et al. 1999a). ...
It is clear that hormones play a critical role in triggering vocal production as well as in the development of neural and
muscular substrates for vocal production. The acoustic perception of vocalizations is also likely to be influenced by hormones,
although more research in this area is needed. The study of the neuroendocrine basis of acoustic communication provides an
excellent opportunity to understand the effect of neuromodulation on the expression of discrete behavior. The future challenges
that we face are twofold. First, extensive catalogs of pairwise parameters (hormone as independent variable and behavior and
physiological phenomena as dependent variable) need to be integrated to make better sense of how hormonal changes at physiological
levels lead to the expression of behavior. Comparative approaches as well as bottom-up approaches—by focusing on lower-order
neurons with identified function—are expected to yield fruitful results. Second, we must recognize that the hormone-behavior
relation is not unidirectional; hormones not only regulate vocal production and perception of acoustic signals, but the very
act of vocalizing and/or perceiving vocalizations can modify the hormonal state. The endocrine basis of acoustic communication
of animals in their natural environment—with extended interactions between individuals—is likely to be much more complex and
will provide a different kind of understanding of these very powerful ways to affect behavior.
... The seasonal variability in song behavior is accompanied by structural changes in the brain regions that control song learning and production. The volumes of the neostriatal nucleus HVc, the robust nucleus of the archistriatum (R A), area X of the parolfactory lobe, and the tracheosyringial portion of the hypoglossal nucleus (nX IIts) can be as much as 188% larger in breeding birds than in nonbreeding birds (Nottebohm, 1981;Arai et al., 1989;Kirn et al., 1989;Brenowitz et al., 1991;Rucker and Cassone, 1991;Bernard and Ball, 1995;Smith et al., 1995Smith et al., , 1997aSmith, 1996;Gulledge and Deviche, 1997). An increase in circulating levels of testosterone caused by increasing daylength is thought to be the primary proximate cue that induces growth of the song system and changes in song behavior (Smith et al., 1997b). ...
In seasonally breeding birds, the vernal growth of the song system is thought to result primarily from increased daylength and the associated increase in circulating testosterone. Other environmental factors such as social cues between mates influence the timing of reproduction, but less is known about how social cues might affect the song system and song behavior. We used white-crowned sparrows (Zonotrichia leucophrys gambelii) to test the hypothesis that the presence of a female in breeding condition influences song nuclei and song behavior of adult males. There were four treatment groups: (1) eight males housed individually in the same room on long days and paired with estradiol-implanted females; (2) eight males housed similarly on long days but without females; (3) four males isolated on long days; and (4) four males isolated on short days. The volumes of two song nuclei, HVc and RA, were significantly larger in males housed with females than in any other treatment group. Males isolated on short days had smaller HVc, RA, and area X volumes than all other groups. The volumes of Rt (a thalamic nucleus not involved in song) and the telencephalon did not differ among groups. Plasma androgen levels did not differ among the three long-day, social treatment groups at the times sampled, but were lower in the short-day isolates. Males paired with females sang at a higher maximum rate than males housed together, who sang at a higher rate than long-day isolates. These results suggest that seasonal plasticity in the adult song system is influenced by social cues.
... Castration does affect this (Figs. 5C and 5D) and other species' song control nuclei (Smith et al., 1997;Gulledge and Deviche, 1997). Finally, the third model (Fig. 6C) reflects a synergistic interaction between the photoperiodic timing system and the feedback from gonadal steroids. ...
The primary and secondary sexual characteristics of many species of passerine birds undergo dramatic seasonal variation in response to the change in the length of photoperiod. Among the many physiological processes that undergo seasonal changes, bird song and the song control system underlying it undergo similar seasonal variation in size and function. The mechanisms of this seasonal variation are largely unknown but are at least partially due to steroidal action from the gonads. The present study determined the relative roles played by the gonads and the photoperiodic timing system that controls gonadal development on song control nuclei in the brain of the male house sparrow, Passer domesticus. Sparrows maintained in short photoperiods (SD) possessed small regressed testes. Transfer to long photoperiods (LD) for 6 weeks evoked a dramatic increase in testes size, but, after 20 weeks under the same conditions (LDLD), testes completely collapsed. Song control nuclei HVC and RA were smaller in SD than in LD but regressed only moderately in LDLD. Castration of sparrows in SD reduced the amplitude of the seasonal variation but did not completely abolish it. The data support the view that the song control system of the house sparrow is regulated by the photoperiodic timing system independently of gonadal influence, but that the gonads augment seasonal regulation of song, presumably via steroidal hormone secretion.
... The seasonal pattern of circulating testosterone correlates positively with the seasonal growth pattern of the song control circuitry 3,37,38,40,41,63 . Castration strongly attenuates the seasonal growth of the song nuclei 42,44,46 . Exogenous testosterone can induce song-nucleus growth in castrated males and nonbreeding males in fall and winter 44,71,75,84,85 . ...
Seasonal plasticity of structure and function is a fundamental feature of nervous systems in a wide variety of animals that occupy seasonal environments. Excellent examples of seasonal brain changes are found in the avian song control system, which has become a leading model of morphological and functional plasticity in the adult CNS. The volumes of entire brain regions that control song increase dramatically in anticipation of the breeding season. These volumetric changes are induced primarily by vernal increases in circulating sex steroids and are accompanied by increases in neuronal size, number and spacing. In several species, these structural changes in the song control circuitry are associated with seasonal changes in song production and learning. Songbirds provide important insights into the mechanisms and behavioral consequences of plasticity in the adult brain.
... Previous studies have demonstrated that circulating T is a critical endogenous cue that controls seasonal plasticity in the song control system Ball et al., 2002). Treatment with T can increase the volumes of HVC, RA, and X (e.g., Smith et al., 1997b;Gulledge and Deviche, 1997). Testosterone, however, can be converted to E 2 in the brain by aromatase (Riters et al., 2001;Schlinger and Brenowitz, 2002). ...
Songbirds show dramatic neural plasticity as adults, including large-scale anatomical changes in discrete brain regions ("song control nuclei") controlling the production of singing behavior. The volumes of several song control nuclei are much larger in the breeding season than in the nonbreeding season, and these seasonal neural changes are regulated by plasma testosterone (T) levels. In many cases, the effects of T on the central nervous system are mediated by neural conversion to estradiol (E(2)) by the enzyme aromatase. The forebrain of male songbirds expresses very high levels of aromatase, in some cases adjacent to song control nuclei. We examined the effects of aromatase inhibition and estrogen treatment on song nuclei size using wild male songbirds in both the breeding and nonbreeding seasons. In breeding males, aromatase inhibition caused the volume of a telencephalic song control nucleus (HVC) to decrease, and this effect was partially rescued by concurrent estrogen replacement. In nonbreeding males, estradiol treatment caused HVC to grow to maximal spring size within 2 weeks. Overall, these data suggest that aromatization of T is an important mediator of song control system plasticity, and that estradiol has neurotrophic effects in adult male songbirds. This study demonstrates that estrogen can affect adult neural plasticity on a gross anatomical scale and is the first examination of estrogen effects on the brain of a wild animal.
... Seasonal changes in neural morphology are accompanied by changes in the stereotypy and duration of song (Brenowitz et al., 1998; Smith et al., 1995), and in the metabolic capacity of song nuclei (Wennstrom et al., 2001). Seasonal changes in the song system are primarily regulated by changes in the circulating levels of testosterone (T), and its metabolites in the brain (Bernard et al., 1997; Gulledge and Deviche, 1997; Smith et al., 1997a,b). Each breeding season, as day length increases, the testes grow and secrete higher levels of T. Most of the song nuclei express steroid receptors (Fig. 1). ...
Many animals exhibit seasonal changes in behavior and its underlying neural substrates. In seasonally breeding songbirds, the brain nuclei that control song learning and production undergo substantial structural changes at the onset of each breeding season, in association with changes in song behavior. These changes are largely mediated by photoperiod-dependent changes in circulating concentrations of gonadal steroid hormones. Little is known, however, about whether changes in the electrophysiological activity of neurons accompany the dramatic morphological changes in the song nuclei. Here we induced seasonal-like changes in the song systems of adult white-crowned sparrows and used extracellular recording in acute brain slices from those individuals to study physiological properties of neurons in the robust nucleus of the arcopallium (RA), a pre-motor nucleus necessary for song production. We report that: RA neurons from birds in breeding condition show a more than twofold increase in spontaneous firing rate compared to those from nonbreeding condition; this change appears to require both androgenic and estrogenic actions; and this change is intrinsic to the RA neurons. Thus, neurons in the song circuit exhibit both morphological and physiological adult seasonal plasticity.
... Blue tit HVC and RA increase in size from winter to the breeding season in the field (Caro et al., 2005), and when black-capped chickadees are exposed to artificial light cycle changes in the laboratory , photostimulated birds also have a larger song system than photorefractory and photosensitive birds (MacDougall-Shackleton et al., 2003). In both of those cases, the size of the seasonal effect was smaller, however, than the effect size typically reported for other temperate songbirds in the wild [e.g., for HVC, blue tit: f ¼ 0.63; black-capped chickadee: f ¼ 0.56; white-crowned sparrow (Zonotrichia leucophrys nuttalli): f ¼ 2.58 (Brenowitz et al., 1998 ); rufous-sided towhee (Pipilo erythrophthalmus ): f ¼ 1.1 (Brenowitz et al., 1991); dark-eyed junco (Junco hyemalis): f ¼ 1.79 (Gulledge and Deviche, 1997)]. This might indicate that seasonal changes in parids in general are smaller than in other songbirds studied to date. ...
Most temperate songbird species sing seasonally, and the brain areas involved in producing song (the song system) vary in size alongside the changes in behavior. Black-capped chickadees (Poecile atricapillus) also sing seasonally, and we find that there are changes in the stereotypy and the length of the fee-bee song from the nonbreeding to the breeding season. Yet despite these changes, we fail to find any evidence of seasonal changes in the song system. The song system of males is larger than that of females, as is typical in songbirds, but the ratio between the sexes is small compared to other species. We suggest three hypotheses to explain our failure to find seasonal variation in the chickadee song system.
... During the breeding season, some of these regions including the nidopallial nucleus high vocal center (HVC) and the robust nucleus of the arcopallium (RA) become up to 200% larger than during the nonbreeding season (Tramontin and Brenowitz, 2000). This enlargement is primarily due to increased testosterone (Gulledge and Deviche, 1997;Tramontin and Brenowitz, 2000) and it may also be influenced by increased singing (Ball et al., 2002;Sartor and Ball, 2005). In free-living Rufous-winged Sparrows, HVC and RA volumes increase between pre-breeding and breeding birds, when song rates also increase . ...
Prolonged exposure to conspecific song stimulates gonadal function and reproductive hormone secretion in female birds but few studies have investigated the physiological effects of conspecific song exposure on males outside of short-term, aggressive interactions. We exposed male Rufous-winged Sparrows, Aimophila carpalis, either to conspecific song (CS Song), to heterospecific song (Black-throated Sparrow, Amphispiza bilineata; HS Song), or to no recorded song (No Song) for 59 consecutive days (two h per day). Birds were exposed to short days (8L:16D) for the first 21 days of treatment and were then transferred to long days (13L:11D) for the remaining 38 days. During long day exposure, CS Song birds experienced faster growth of testes than HS Song and No Song birds. HS Song birds also grew their testes faster than No Song birds. Plasma luteinizing hormone (LH) and testosterone did not differ between CS Song and No Song birds. However, plasma LH was higher in HS Song birds compared to other groups. There were no differences in hypothalamic immunocytochemical labeling for gonadotropin-releasing hormone, its precursor proGnRH, or gonadotropin-inhibitory hormone, nor were there differences in two song control nuclei volumes (HVC and RA) between CS Song and No Song treatment groups. Furthermore, we found no effect of heterospecific song on free-living Rufous-winged Sparrow aggressive behaviors. These data indicate that long-term exposure to auditory stimuli, such as song, can influence the reproductive system of male songbirds and different types of auditory stimuli can have differential effects on reproductive function.
... Seasonal-like plasticity in the song control system is modulated by changes in photoperiod and circulating steroid sex hormones, with important contributions coming from both of these factors ( Figure 3). Very early in the breeding season, increasing day length activates the hypothalamic-pituitary gonadal axis, which stimulates growth of the testes and elevates circulating levels of T. This increase in circulating T primarily regulates song control system growth; T induces growth under both SD and LD photoperiod conditions (Smith et al., 1997;Bernard et al., 1997;Gulledge et al., 1997;further reviewed in Brenowitz, 2004; for an alternate view see Ball et al., 2004), and T levels below breeding maxima can induce growth of the song system (Tramontin et al., 2001). LD photoperiod and systemic T induces song control system growth even when the bird has been deafened and sings at a very low rate . ...
Birdsong is regulated by a series of discrete brain nuclei known as the song control system. In seasonally-breeding male songbirds, seasonal changes in steroid sex hormones regulate the structure and electrophysiology of song control system neurons, resulting in dramatic changes in singing behavior. Male songbirds can be brought into the laboratory, where circulating levels of steroid hormone and photoperiod can be abruptly manipulated, providing controlled conditions under which rapid "seasonal-like" changes in behavior and morphology can be carefully studied. In this mini-review, we discuss the steroidal and cellular mechanisms underlying seasonal-like growth and regression of the song control system in adult male Gambel's white-crowned sparrows (Zonotrichia leucophrys gambelii), and its impact on song behavior. Specifically, we discuss recent advances concerning: (1) the role of androgen and estrogen receptors in inducing seasonal-like growth of the song control system; (2) how photoperiod modulates the time course of testosterone-induced growth of the song control system; (3) how bilateral intracerebral infusion of androgen and estrogen receptor antagonists near the song control nucleus HVC prevents seasonal-like increases in song stereotypy but not song rate; and (4) the steroidal and cellular mechanisms that mediate rapid regression of the song control system. Throughout this mini-review we compare data collected from white-crowned sparrows to that from other songbird species. We conclude by outlining avenues of future research.
One of the most fascinating developments in the field of neuroscience in the second half of the 20th century was the discovery of the endogenous capacity of the brain for reorganization during adult life. Morphological and functional mechanisms underlying brain plasticity have been extensively explored and characterized. However, our understanding of the functional significance of these plastic changes is still fragmentary. This book shows that brain plasticity plays an essential role in the regulation of hormonal levels. The second aim is to propose that hormones orchestrate the multiple endogenous plastic events of the brain for the generation of adequate physiological and behavioral responses in adaptation to and in prediction of changing life conditions. The book starts by introducing the conceptual backgrounds on the interactions of hormones and brain plasticity. It then devotes itself to the analysis of the role of brain plasticity in the regulation of the activity of endocrine glands. It examines different hormonal influences on brain plasticity. Then, it goes on to cover the interactions of hormones and brain plasticity along the life cycle under physiological and pathological conditions.
Birdsong is a complex learned behavior performed by the oscine passerine birds. Birds sing in reproductive and aggressive contexts, but there is great diversity in song behavior across species, seasons, and sexes. Song learning and production are controlled by a collection of neural circuits, the song control system, that is unique to this group of birds. The growth, maturation, and adult function of this circuit depends on hormonal signals, especially the reproductive steroid hormones. This chapter reviews studies examining the neural control of song and functions of endocrine systems that influence the song-control system. They reveal how sex steroids can act to build motor and learning pathways and then stimulate plasticity of these circuits to modify song throughout adult life. Much of the observed behavioral diversity can be accounted for by individual differences in the neural distribution of steroid receptors or in age, sex, or seasonal differences in the gonadal secretion of sex steroids. Songbirds may also synthesize steroids in nongonadal sites and use nontraditional steroids or cellular mechanisms to control song. The evolution in songbirds of multiple mechanisms to synthesize and respond to sex steroids contributes to a growing body of work expanding traditional concepts about the relationship between hormones, brain, and behavior.
Birds, unlike mammals, do not use the annual profile of pineal melatonin secretion to coordinate their reproductive efforts with a favorable time of year. Melatonin in birds mediates the entrainment of circadian activity rhythms, and thus helps to time hatching of eggs and facilitate migration. However, the role of melatonin as a reliable indicator of day length for seasonal processes has remained equivocal for many years. Recently, the influence of melatonin on two physiological processes involved in aspects of seasonal reproduction has been identified in European starlings: 1) the regulation of seasonal changes in immune function, and 2) neuroplasticity in the song control system. Melatonin can enhance cell-mediated immune function and acts as an inhibitory hormone on the song control system. Melatonin receptor (MelR) density in a forebrain song control nucleus, Area X, is regulated as a function of reproductive state; there is marked downregulation of MelR in Area X during the breeding season in starlings. Seasonal regulation of immune function and neural plasticity within the song control system, and the efficacy of the action of melatonin on these two processes, appears to be modified by the same central, thyroid-dependent mechanism that controls the reproductive state of birds. These data indicate that the interaction of day length and hormones of different classes affects the ability of melatonin to affect seasonal processes in birds. The downstream consequences of MelR regulation within the song control system are discussed with regard to the cellular action of melatonin and its possible interaction with immediate-early genes and transcription factors. Microsc. Res. Tech. 53:63–71, 2001. © 2001 Wiley-Liss, Inc.
It is probably not surprising to most of us that the endocrine system plays a significant role in controlling the singing behavior of birds. We are familiar with the song of birds as a conspicuous acoustic feature of our environment during the avian breeding season. We often witness song when it is produced by birds (males) that are aggressively establishing and defending territories and that are advertising to available females. Thus, it is easy to imagine that song is likely to be stimulated by gonadal hormones. However, the ways in which gonadal sex steroids influence the various parts of the brain at various stages of the bird's life to influence song are complex and far from being completely understood. In this review, I will highlight some of the significant discoveries that have contributed to our view that the songbird brain is a significant and dynamic target of sex steroids. I will also describe what we have learned about properties of the endocrine system and the brain and how they each contribute to making androgens or estrogens available to particular parts of the songbird brain. Finally, I will describe some new research directions that may help answer some unresolved issues about hormonal effects on the songbird brain. © 1997 John Wiley & Sons, Inc. J Neurobiol 33: 619–631, 1997
There is extensive plasticity of the song behavior of birds and the neuroendocrine circuit that regulates this behavior in adulthood. One of the most pronounced examples of plasticity, found in every species of seasonally breeding bird examined, is the occurrence of large seasonal changes in the size of song control nuclei and in their cellular attributes. This seasonal plasticity of the song circuits is primarily regulated by changes in the secretion and metabolism of gonadal testosterone (T). Both androgenic and estrogenic sex steroids contribute to seasonal growth of the song system. These steroids act directly on the forebrain song nucleus HVC, which then stimulates growth of its efferent target nuclei transsynaptically. Seasonal growth and regression of the song circuits occur rapidly and sequentially following changes in circulating T and its metabolites. As the neural song circuits change across seasons, there are changes in different aspects of song behavior, including the structural stereotypy of songs, their duration, and the rate of production. The burden of evidence supports a model in which changes in song behavior are a consequence rather than a cause of the changes in the song circuits of the brain. Seasonal plasticity of the song system may have evolved as an adaptation to reduce the energetic demands imposed by these regions of the brain outside the breeding season, when the use of song for mate attraction and territorial defense is reduced or absent. The synaptic plasticity that accompanies seasonal changes in the song system may have acted as a preadaptation that enabled the evolution of adult song learning in some species of birds.
We determined seasonal changes in blood parasite infections in a free-living population of Dark-eyed Juncos (Junco hyemalis) breeding in interior Alaska (65 °N; 148 °W). The common parasites found in blood smears were Leucocytozoon fringillinarum (56%), Trypanosoma avium (33%), and Haemoproteus fringillae (9%). In males, parasite prevalences were relatively high at arrival on breeding grounds and increased during the breeding season. Intensity of infection with Leucocytozoon also increased between spring and summer, and then decreased at the time of migration (September). This decrease did not occur in adult females. Elevated prevalences during the breeding season probably reflected the addition of new cases via vector activity to positive status resulting from spring relapse. We observed neither an association between parasite species nor a consistent relationship between parasite intensity and body condition. To further study relationships between reproductive system activity and parasite infections, we compared prevalences in adult males that were undergoing their first cycle of gonadal development and regression (males in their second calendar year, or SY) with those of older males (males in their third or more calendar year, i.e., after-second-year males or ASY). Circulating testosterone concentrations declined in both groups between arrival on breeding grounds (end of April-early May) and the end of the reproductive period (July), and they were higher in May in ASY than in SY males. At the peak of the breeding season (June), ASY males also had a higher parasite prevalence than SY males. This difference may have resulted from immunosuppressive effects of gonadal hormones and/or from behavioral differences between SY and ASY males such that older males were exposed to more insect vectors than younger males. J. Exp. Zool. 289:456–466, 2001. © 2001 Wiley-Liss, Inc.
The adoption of foreign song elements occurs under natural conditions in various songbird species including the house sparrow Passer domesticus, even though it may go largely unnoticed by humans. House sparrows singing canary song have been known by hobbyists for a long time. My study is the first to analyse the imitative abilities of house sparrows in detail. I used an integrative approach considering features that are particularly important for the degree of vocal learning that can be displayed by a species. These included (1) a genetic predisposition, (2) body condition of the parents, (3) food availability during early ontogeny, (4) social factors, (5) neuronal mechanisms, (6) hormonal states, and (7) body size and morphology of the vocal tract. House sparrows singing canary-like songs provide a rich tool for further integrative approaches. I suggest an interpretation combining all the above features under the perspective of female choice. Instead of searching for a „key adaptation“ or single explanation for the imitative ability (song learning ability) in passerines, it might be more appropriate to focus on the multiplicity of factors involved in song production that - shaped by different selective forces - promote the highly specific song adaptations. Schon seit Jahrhunderten sind Haussperlinge bei Vogelliebhabern als gelehrige Imitatoren fremder Laute und Gesänge bekannt. Am häufigsten wird von Sperlingen berichtet, die von Kanarienvögeln aufgezogen wurden und den Kanariengesang lernten. Wissenschaftlern hingegen blieb dieses Wissen bislang weitgehend verborgen. In dieser Arbeit wird erstmals der wissenschaftliche Nachweis erbracht, dass Sperlinge tatsächlich den Kanariengesang lernen und produzieren. Dazu habe ich einen integrativen Forschungsansatz verwendet, der folgende Aspekte umfasst (1) Einflüsse der Aufzucht durch Kanarienvögel oder Sperlinge; (2) Gesänge von Haussperlingen, aufgezogen von Kanarienvögeln oder Sperlingen; (3) Gehirnstrukturen (HVc, RA), welche dem Gesang zugrunde liegen; (4) Einflüsse von Steroidhormonen (Testosteron, DHEA) auf die Gesangsproduktion; (5) Einflüsse des Stimmapparates auf die Gesangsproduktion. Summa summarum zeigt diese Arbeit, dass eine Verhaltensweise wie ‚Singen’ auf dem komplexen Zusammenspiel vieler verschiedener Faktoren beruht, von denen keiner vernachlässigt werden darf: (a) Der ‚kanarisch’ singende Hausperling offenbart sich als ideales Subjekt für einen integrativen Forschungsansatz, der - mindestens - Neurobiologie, Endokrinologie, Verhaltensbiologie, funktionale Morphologie, und Life History verbindet; (b) Beim Vergleichen des Gesang von verschiedenen Vogelarten sollte zukünftig nicht nur auf phylogenetische Nähe bzw. Ferne korrigiert werden, sondern auch auf die unterschiedliche Körpergröße; (c) Gesang sollte folglich nicht mehr nur als eine einheitliche Anpassung betrachten werden, sondern als hoch spezialisiertes Ergebnis vieler verschiedener, in Wechselwirkung stehender Anpassungen, geformt unter unterschiedlichen Selektionsdrücken.
Studies concerning the song control system (SCS) in songbirds generally focus on males due to their prodigious song production. Both seasonal and age related differences have been found in the size of male SCS regions. Among those studies that have addressed females some level of sexual size dimorphism has been found, with females generally having smaller SCS area than males. Among those species where female song has been studied, typically females either sing much less than males, or they duet with their mates, but in general do not produce independent song. Here we present information on seasonal and sex differences in SCS in the northern cardinal (Cardinalis cardinalis) a species where both sexes sing, females sing independent of their mates, and song is produced by males over a prolonged period of time (7-8 months). We collected brains from free-living adult cardinals, both in the late non-breeding season and during the early breeding season, and measured three song control nuclei; HVC, Area X and RA. There were sex differences in all three areas assessed at the two time points considered. Additionally, there was a seasonal difference in both sexes for all areas assessed. In both time points male SCS nuclei were 1.5-2.0 times larger than female SCS nuclei. These data show that even in those species with independent female song there may still exist sex differences in the SCS nuclei. Similarity in song between the sexes could be related to differences in hormone receptors or hormone levels in the brain, while the small-observed changes in SCS area in males may allow for early breeding season song production and song production outside of the breeding season.
It is probably not surprising to most of us that the endocrine system plays a significant role in controlling the singing behavior of birds. We are familiar with the song of birds as a conspicuous acoustic feature of our environment during the avian breeding season. We often witness song when it is produced by birds (males) that are aggressively establishing and defending territories and that are advertising to available females. Thus, it is easy to imagine that song is likely to be stimulated by gonadal hormones. However, the ways in which gonadal sex steroids influence the various parts of the brain at various stages of the bird's life to influence song are complex and far from being completely understood. In this review, I will highlight some of the significant discoveries that have contributed to our view that the songbird brain is a significant and dynamic target of sex steroids. I will also describe what we have learned about properties of the endocrine system and the brain and how they each contribute to making androgens or estrogens available to particular parts of the songbird brain. Finally, I will describe some new research directions that may help answer some unresolved issues about hormonal effects on the songbird brain.
There is extensive diversity among the 4000 species of songbirds in different aspects of song behavior, including the timing of vocal learning, sex patterns of song production, number of songs that are learned (i.e., repertoire size), and seasonality of song behavior. This diversity provides unparalleled opportunities for comparative studies of the relationship between the structure and function of brain regions and song behavior. The comparative approach has been used in two contexts: (a) to test hypotheses about mechanisms of song control, and (b) to study the evolution of the control system in different groups of birds. In the first context, I review studies in which a comparative approach has been used to investigate sex differences in the song system, the relationship between the number of song types a bird sings and the size of the song nuclei, and seasonal plasticity of the song control circuits. In the second context, I discuss whether the vocal control systems of parrots and songbirds were inherited from a common ancestor or independently evolved. I also consider at what stage in the phylogeny of songbirds the hormone-sensitive forebrain circuit found in modern birds first evolved. I conclude by identifying directions for future research in which a comparative approach would be productive.
Seasonal plasticity in the morphology of telencephalic nuclei that control song behavior has been reported for diverse species of songbirds. The only published report of a lack of seasonal changes in the song nuclei of a seasonally breeding bird is that of Baker et al. in the Nuttall's subspecies of white-crowned sparrow (Zonotrichia leucophrys nuttalli). In this study, they brought wild birds into the laboratory and exposed them to either "summer" or "winter" photoperiods. Previous studies have shown that exposing wild-caught white-crowned sparrows to long-day photoperiods in the laboratory may not induce circulating concentrations of testosterone (T) as high as those seen in wild breeding birds. Changes in circulating T are primarily responsible for the seasonal morphological changes in the song nuclei. To determine whether there is seasonal plasticity of the song system in this subspecies, we measured circulating T, morphological attributes of the song nuclei, and song behavior in wild Nuttall's white-crowned sparrows during the spring and fall. Testis size and circulating T concentrations were greater in spring than fall birds. The absolute volumes of the song nuclei HVc, RA, and Area X, and their volumes relative to those of either the total telencephalon or three thalamic nonsong nuclei, were significantly greater in the spring than fall sparrows. Song behavior also changed seasonally; fall birds sang shorter songs than did spring birds. These results show that there is seasonal plasticity of the song system in wild Nuttall's white-crowned sparrows. Seasonal plasticity can now be regarded as a common feature of the seasonally breeding songbirds studied thus far.
Previously, we found that, unlike adults, adolescent male dark-eyed juncos (Junco hyemalis) maintained large Area X volumes despite having low plasma testosterone concentrations. Other studies indicate that photoperiod may act independently of testosterone to modulate vocal control region (VCR) volumes in adult songbirds. In the present study, we investigated the effects of testosterone and photoperiod on the volumes of four VCRs in adolescent male juncos. To test the hypothesis that VCR volumes in these males are testosterone independent, we treated birds exposed to short days with testosterone and later compared their VCR volumes with those of birds exposed to short days without testosterone. To examine whether photoperiod alone could affect VCR volumes independent of testosterone, we measured these volumes in photorefractory birds exposed to long photoperiod without testosterone. Administering testosterone induced singing, yet increased the volume of only one VCR, the robust nucleus of the anterior neostriatum (RA). In contrast, long photoperiod increased several VCR volumes (Area X, higher vocal center, and RA) despite low testosterone levels, but did not induce singing. Our results suggest a limited role for testosterone, but an important role for photoperiod, in controlling VCR volumes in adolescent male juncos. In addition, the results demonstrate that singing behavior can be induced in adolescent males without a concomitant increase in most VCR volumes.
Neuroplasticity in the vocal control system of songbirds is strongly influenced by seasonal fluctuations in circulating testosterone. These seasonally plastic telencephalic structures are implicated in the learning and production of song in songbirds. The role of the indoleamine melatonin in seasonal adaptations in birds has remained unclear. In this experiment, European starlings were castrated to remove the neuromodulating activity of gonadal steroids and were exposed to different photoperiods to induce reproductive states characteristic of different seasonal conditions. Long days increased the volume of the song-control nucleus high vocal center compared with its volume on short days. Exogenous melatonin attenuated the long-day-induced volumetric increase in high vocal center and also decreased the volume of another song-control nucleus, area X. This effect was observed regardless of reproductive state. To our knowledge, this is the first direct evidence of a role for melatonin in functional plasticity within the central nervous system of vertebrates.
Previous investigations have identified regions of the avian brain that contain immunoreactive vasotocinergic (VT-ir) cell bodies and fibers. These studies exclusively used domesticated species, and the relevance of the findings for free-living birds has not been established. The present study used immunocytochemistry to determine the neuroanatomical distribution of the VT-ir system in the brain of a well-studied male passerine bird (dark-eyed junco, Junco hyemalis) obtained from a natural population in interior Alaska (65 degrees N, 147 degrees W). VT-ir cell bodies were observed in several brain regions (paraventricular and supraoptic nuclei, nucleus of the stria terminalis), where they have been described in other oscine species. VT-ir fibers were widespread in many brain regions and were especially abundant in the medial preoptic nucleus, the basal region of the septum, and the hypothalamic-neurohypophyseal tract. Fibers were also present in brain regions that are involved in the control of vocal behavior including the ventromedial capsular region of the nucleus robustus archistriatalis and the dorsomedial portion of the mesencephalic nucleus intercollicularis. The widespread brain distribution of VT-ir cell bodies and fibers in juncos generally resembles that of domestic birds and suggests a role for this neuropeptide in the control of reproductive behavior and physiology.
Melatonin was recently identified as playing a role in fine-tuning the effects of gonadal steroids in the regulation of seasonal neuroplasticity within the telencephalic song control system of European starlings. The present study investigated possible seasonal regulation of melatonin receptors (MelR) within the starling song control system, in the presence or absence of gonadal steroids. Brains were sampled from photosensitive starlings exposed to short days, photostimulated starlings exposed to long days and photorefractory starlings also exposed to long days. Each condition contained a group of gonad-intact birds and a group of castrated birds. Melatonin receptor distribution was assessed in vitro by 125-iodomelatonin (IMEL) receptor autoradiography. In general, MelR distribution was similar to that described in other songbird species. However, there was a striking downregulation of MelR in the song control nucleus Area X of intact and castrated photostimulated birds on long days compared to their photorefractory counterparts on the same long days and to the short-day groups. Downregulation of MelR occurred independently of gonadal steroids. Nevertheless, superimposed on this general pattern of MelR downregulation during photostimulation, IMEL binding was observed in a medial subdivision of Area X when gonadal steroids were present. Downregulation of MelR in Area X during the short breeding season has implications for seasonal regulation of the song control system. Subsequent upregulation of MelR as birds become photorefractory, in the absence of any change in photoperiod, gonadal steroids or melatonin signal is the first description of photoperiod-independent regulation of MelR in adults of any vertebrate class.
Alpha-synuclein is a small, highly conserved protein in vertebrates that has been linked to several neurodegenerative diseases. The avian song control system is one of the model systems in which the protein was independently discovered. Alpha-synuclein is dynamically regulated in the song system during song learning, a process in which sex steroids play a central role. We compared alpha-synuclein mRNA expression in the brains of 12 adult male chipping sparrows (Spizella passerina) treated with either testosterone or blank s.c. implants. We saw pronounced upregulation of alpha-synuclein mRNA in, as well as an increase in the volume of, the song control nucleus area X in response to exogenous testosterone. To our knowledge this is the first report of steroid regulation of synuclein gene expression in any model system.
There is pronounced seasonal plasticity in the morphology of the neural circuits that regulate song behavior in adult songbirds, primarily in response to changes in plasma testosterone (T) levels. Most song nuclei have androgen receptors. Afferent input from the telencephalic nucleus HVc (also known as the "high vocal center") is necessary for seasonal growth of the direct efferent target nuclei RA and area X. We asked here whether T-stimulated growth of HVc is sufficient to induce growth of its efferent nuclei. Intracerebral T implants were placed unilaterally near HVc or RA in photosensitive adult male white-crowned sparrows for one month. The T implant near HVc produced significant growth of the ipsilateral (but not contralateral) HVc, RA, and area X, and increased neuronal number in the ipsilateral HVc. The T implant near RA did not produce selective growth of ipsilateral RA, HVc, or area X. Intracerebral T implants did not elevate plasma T levels, nor did they stimulate growth of two peripheral androgen sensitive targets, the syrinx and the cloacal protuberance. These results suggest that seasonal growth of the adult song circuits results from T acting directly on HVc, which then stimulates the growth of RA and area X transynaptically.
In songbirds, the initiation of song behaviour and the neural substrate of this system are highly influenced by gonadal steroids. Receptors for gonadal steroid hormones, such as androgens and oestrogens, have been localized within select nuclei of the song system. An important step in steroid receptor action is the recruitment of nuclear receptor coactivators. The coactivator, cAMP response element binding protein (CREB)-binding protein (CBP), has been implicated in both androgen and oestrogen receptor transactivation. Although the role of CBP in transcriptional mechanisms has been widely studied, little is known about CBP expression in the brain. The association between the distribution of CBP and oestrogen receptors in the hippocampus has been related to long-term memory. However, the distribution of brain CBP has not been related to the expression of gonadal steroid receptors in a system as relevant to reproductive behaviour as the avian song system. Western immunoblotting of European starling (Sturnus vulgaris) brain tissue reveals a band at 265 kDa. Immunohistochemical localization of CBP in starling brain indicates wide, but heterogeneous expression. CBP-immunoreactive (CBP-ir) cells define the boundaries of song control nuclei. In HVc (sometimes called the High Vocal Center) and the robust nucleus of the archistriatum (RA), there is a higher density of CBP-ir cells within the boundaries of these nuclei than in adjacent neostriatum or archistriatum, for HVc and RA, respectively. We also report that the distribution of CBP-ir cells varies among different nuclei within the song control system. CBP-ir cells within area X (also a part of the song system) and HVc are densely packed into clusters, whereas cells can be easily discriminated in RA. CBP is also highly expressed in hypothalamic areas, indicating that areas rich in steroid receptors also contain CBP. These data suggest that CBP is important for modulating transcriptional activities in the song system and other sites in the songbird brain that express gonadal steroid receptors.
Many commercial bird diets are made with soy products that contain phytoestrogens (i.e., plant compounds that have weak agonist activity at estrogen receptors), but the effects of these compounds on bird physiology and behavior are largely unknown. The primary phytoestrogens present in soy are the isoflavones genistin and diadzin, which have been shown to affect reproductive measures in many taxa. Two groups of wild-caught male Dark-eyed Juncos (Junco hyemalis) were fed a diet either made with water-washed soy protein (soy(+)) or made with soy protein that had been alcohol-washed to extract isoflavones (soy(-)). Both groups exhibited a photoperiodic response to long days. Plasma luteinizing hormone (LH) concentrations increased within the first week of long day (LD) exposure for both groups, and over the course of the experiment LH was higher in the soy(+) group, although concentrations for both groups were lower than have been reported in free-living juncos. The rate of cloacal protuberance (CP) growth was significantly affected by diet, with the soy(-) birds beginning to increase their CPs about a week faster than soy(+) birds after exposure to LD. There was no group difference in food intake, fat score, body mass, or behavioral measures during the study or in testis weight at the end of the study. Although effects of dietary phytoestrogens detected were subtle (i.e., rate of CP growth), those investigating subtle effects of hormonally active substances (e.g., endocrine disruptors) or environmental cues affecting the reproductive axis in songbirds may want to consider eliminating phytoestrogens from their experimental diets.
Song production in song birds is controlled by an efferent pathway. Appended to this pathway is a "recursive loop" that is necessary for song acquisition but not for the production of learned song. Since zebra finches learn their song by imitating external models, we speculated that the importance of the recursive loop for learning might derive from its processing of auditory feedback during song acquisition. This hypothesis was tested by comparing the effects on song in birds deafened early in life and birds with early lesions in either of two nuclei--Area X and the lateral magnocellular nucleus of the anterior neostriatum (LMAN). These nuclei are part of the recursive loop. The three treatments affected song development differently, as reflected by various parameters of the adult song of these birds. Whereas LMAN lesions resulted in songs with monotonous repetitions of a single note complex, songs of Area X-lesioned birds consisted of rambling series of unusually long and variable notes. Furthermore, whereas song of LMAN lesioned birds stabilized early, song stability as seen in intact birds was never achieved in Area X-lesioned birds. Early deafness also resulted in poorly structured and unstable song. We conclude that Area X and LMAN contribute differently to song acquisition: the song variability that is typical of vocal development persists following early deafness or lesions of Area X but ends abruptly following removal of LMAN. Apparently, LMAN plays a crucial role in fostering the kinds of circuit plasticity necessary for learning.
The vocal control system of oscine songbirds has some perplexing properties--e.g. laterality, adult neurogenesis, neuronal replacement--that are not predicted by common views of how vocal learning takes place. Similarly, we do not understand the relation between the direct pathway for the control of learned song and the recursive pathway necessary for song learning. Some of the paradoxes of the vocal system of birds may disappear once the relation between the perception and production of learned vocalizations is better understood. To some extent, perception and production may be two closely related states of a same system.
Seasonal variation in the size of song nuclei in the brains of male songbirds may be related to the ability to learn to sing new songs as adults. This hypothesis was tested with the rufous-sided towhee (Pipilo erythrophthalmus), a species in which song repertoires are stable after 1 yr of life. Towhees were hand raised in the laboratory and tutored with normal towhee songs. After song repertoires were recorded at 1 yr of age, photoperiods were manipulated so that 10 male towhees experienced short days and 10 males experienced long days. Circulating hormone concentrations and anatomical attributes of song nuclei were then measured. Photoperiod-related differences in the song nuclei of these towhees were as large as those seen in "open-ended learners" (i.e., species that continue to learn new songs as adults). Seasonal changes of the adult song system may thus occur without disrupting existing song repertoires and without the development of new songs. The synaptic plasticity provided by such seasonal variation, however, may enable song learning by adult birds.
The 4-5-mo hibernation season of golden-mantled ground squirrels consists of extended torpor bouts interspersed with brief, periodic intervals of normothermic arousal. Plasma levels of testosterone (T), luteinizing hormone (LH), and follicle-stimulating hormone (FSH) and degree of scrotal pigmentation were measured in torpid and aroused male ground squirrels throughout a season of hibernation and in active animals after the termination of torpor. T was basal in torpid animals; beginning 3 weeks before torpor ended, T was elevated in normothermic males during the first half of periodic arousals but returned to basal levels before animals reentered torpor. After the last (terminal) arousal from torpor, T levels were moderately elevated for 4 wk and maximal for the next 6 wk before they returned to basal values. LH patterns were similar to those of T; however, levels of T and LH were positively correlated only in aroused or posthibernation males. FSH levels remained constant and low during most of the heterothermic season but increased in several torpid males within 3 days of terminal arousal. FSH levels peaked 2 wk after the end of heterothermy. Scrotal pigmentation developed over the first 4 wk after terminal arousal. Maturation of reproductive function occurs during the 4 wk after termination of heterothermy, but elevated levels of T during arousals and variable levels of FSH in the last days of torpor suggest that activation or increased sensitivity of the hypothalamic-pituitary-gonadal axis is important in the termination of heterothermy in ground squirrels.
New neurons are added to the high vocal center (HVC) of adult male and female canaries. Exogenous testosterone induces a marked increase in HVC size in adult female canaries, though the mechanisms responsible for this increase remain unknown. To understand the mechanisms, we analyzed the effects of testosterone on neuronal recruitment in the female HVC. Intact adult female canaries received Silastic implants that were empty or filled with testosterone. Birds in the short-survival group received the Silastic implant, followed by a single injection of [3H]thymidine 2 days later, and were killed on the following day. Birds in the long-survival group were injected once a day for 5 days with [3H]thymidine and received the Silastic implant 20 and 40 days later. These birds were killed 60 days after the first injection of [3H]thymidine. The number of 3H-labeled ventricular zone cells above, rostral, or caudal to HVC was not affected by the hormone treatment in the short-survival birds, suggesting that testosterone did not affect neuronal production. However, the number of 3H-labeled HVC neurons that projected to robust nucleus of the archistriatum (RA) in the long-survival birds was three times greater in the hormone-treated than in the control group, though the total number of RA-projecting cells did not change significantly. Testosterone also induced an increase in the size of the HVC cells that project to RA. Thus, these experiments suggest that testosterone affects the recruitment and/or survival of newly generated RA-projecting HVC neurons but does not affect their production.
We have traced central nervous pathways controlling bird son in the canary using a combination of behavioral and anatomical techniques. Unilateral electrolytic brain lesions were made in adult male canaries whose son had been previously recorded and analysed on a sound spectrograph. After severral days of postoperative recording, the birds were sacrificed and their brains processed histologically for degeneration staining with the Fink-Heimer technique. Although large lesions in the neostriatum and rostral hyperstriatum had no effect on song, severe song deficits followed damage to a discrete large-celled area in the caudal hyperstriatum ventrale (HVc). Degenerating fibers were traced from this region to two other discrete nuclei in the forebrain: one in the parolfactory lobe (area X, a teardrop-shaped small-celled nucleus) and a round large-celled nucleus in the archistriatum (RA). Unilateral lesions of X had no effect on song; lesions of RA, however, caused severe song deficits. Degenerating fibers from RA joined the occipitomesencephalic tract and had widespread ipsilateral projections to the thalamus, nucleus intercollicularis of the midbrain, reticular formation, and medulla. It is of particular interest that direct connections were found onto the cells of the motor nucleus innervating the syrinx, the organ of song production. Unilateral lesions of n. intercollicularis (previously implicated in the control of vocal behavior) had little effect on song.
In many species of passerine songbirds, males learn their song during defined periods of life. Female song in often reduced or absent, as are the brain regions controlling song. Sexual differences in the brain arise because of the action of sex steroids, which trigger the formation of some neural pathways (especially the pathway from the higher vocal center to the robust nucleus) and prevent the atrophy of others in males. These neural changes occur during periods of developmental song learning and can recur during periods of learning in adult birds. The process of learning is correlated with major increases or decreases in the number of neurons in specific neuronal populations, suggesting that the formation or loss of specific neural pathways regulates the ability to learn. Species differences in sexual differentiation and learning allow informative cross-species comparisons of neural structure and behavior. © 1992 John Wiley & Sons, Inc.
The present investigation used stable area-specific, neuronal properties instead of Nissl stain to delineate the boundaries of the nucleus hyperstriatalis caudal c (HVc) in the telencephalon of the adult male canary. Immunocytochemical procedures combined with retrograde tracing labeled a large population of perennial long-projecting neurons that contain estrogen receptors in the canary HVc. The HVc area defined by the distribution of these neurons was congruent with the HVc area defined in Nissl-stained sections during the breeding period. The HVc area defined in Nissl-stained preparations showed an extensive seasonal change in size, confirming previous results Nottebohm: Science, 214:1368–1370, '81. In contrast, the HVc area defined by the distribution of the estrogen receptor containing long-projection neurons showed little or no seasonal change in size. Because these neurons are permanent, the HVc seems to be of rather constant size year round. The internal morphology of the HVc, however, undergoes seasonal alterations, which are reflected in changes in size of the HVc area distinguishable in Nissl-stained sections. The combination of cytoarchitectural criteria of Nissl-stained preparations with area-specific cytochemical and hodological markers to delineate the boundaries of a brain nucleus might give new insights in the partitioning and neural plasticity of brain areas.
Perhaps the best way to determine whether and how traits of organisms are currently adaptive is to alter them experimentally and compare the relative fitness of altered and unaltered individuals. We call this method phenotypic engineering. To the extent that natural selection moulds organisms on a trait-by-trait basis, we would expect fitness of unmanipulated (control) individuals to be higher than that of experimentally altered individuals. However, other outcomes are possible and of interest. If, for example, a single trait were altered and the fitness of manipulated and unmanipulated organisms were found to be similar, we might conclude that selection is not currently operating on the altered trait. Phenotypic engineering with hormones describes an experimental approach to the study of adaptive variation in suites of traits that are hormonally mediated and correlated in their expression. A likely outcome of such manipulations is that some traits would be altered so as to elevate fitness but that changes in other, correlated traits would lower fitness. If the net effect were to depress fitness, a process by which natural selection shapes and maintains organisms as integrated units would be demonstrated. We have employed this approach in studies of the Dark-eyed Junco Junco hyemalis, a small passerine whose reproductive success varies with the abundance of nest predators. We treated males with testosterone, documented the phenotypic consequences and related these to various measures of fitness. Summarizing results to date: Behavioural comparison of males treated with testosterone (T-males) and control males (C-males) shows that T-males sing more frequently, are less attentive to offspring, have larger home ranges and are more attractive to females. Physiologically, testosterone accelerates entry into breeding condition in spring (loss of winter lipid stores) and results in higher levels of corticosterone. If exposure to testosterone is prolonged beyond the breeding season, pre-basic moult is delayed or prevented. We are currently comparing T- and C-males with respect to corticosteroid binding proteins, sperm reserves, response to nestling vocalizations and neuroanatomy. The relationship between testosterone-induced phenotypic variation and fitness is still under study. When treatment extends well beyond the breeding season, testosterone significantly reduces survivorship; otherwise it does not. With respect to apparent reproductive success (i.e. estimates of paternity that are not based on genetic analysis), more young leave the nests of C-males than of T-males, but treatment groups do not differ in the number of young that reach independence. Preliminary data on realized reproductive success (i.e. number of genetic offspring sired) suggest that production as the result of extra-pair fertilizations is greater in T- than in C-males but that T-males lose paternity of more of the offspring of their social mates to other males. Continued investigation will, we hope, reveal the factors governing the trade-offs between male mating effort and parental effort and between survival and current reproduction, as well as the frequency with which the typical phenotype outperforms one that has been experimentally altered.
In this study we assessed sex differences in the volume of two vocal control nuclei, the high vocal center (HVC) and the robust nucleus of the archistriatum (RA) in zebra finches (Taeniopygia guttata) exposed to various endocrine treatments (neonatal treatment with an aromatase inhibitor and/or an adult treatment with testosterone). The boundaries of these nuclei were defined in sections stained for Nissl substance and compared to alternate sections stained with an immunocytochemical procedure for two neuropeptides, methionine enkephalin and vasoactive intestinal polypeptide. A high density of immunoreactive fibers for methionine enkephalin and vasoactive intestinal polypeptide completely covered the high vocal center in male and female zebra finches and these fibers were not observed in the surrounding neostriatum. With the use of these markers to define the boundary of the high vocal center, it became possible to reconstruct its volume. Positively staining perikarya were not apparent within the boundaries of this nucleus. Immunoreactive fibers for vasoactive intestinal polypeptide and enkephalin also allowed one to define the boundary of the robust nucleus of the archistriatum but they did not fill the entire area of the nucleus as is the case for the high vocal center. When the volumes of both nuclei were reconstructed based on enkephalin or vasoactive intestinal polypeptide immunoreactivity, the presence of a marked sex difference in the volume of these nuclei was confirmed. Neonatal and adult endocrine manipulations did not affect the volumes of these two nuclei measured in Nissl-stained material nor did they affect the volumes as defined based on the peptidergic innervations of the nuclei. Also, the volumetric estimates of these two nuclei derived from sections stained by immunocytochemistry were in good agreement in all groups of birds with the values obtained based on an analysis of the Nissl-stained material. These results illustrate the usefulness of employing a variety of histochemical markers to define a brain area when investigating brain variation and plasticity.
Birds sing to communicate. Male birds use song to advertise their territories and
attract females. Each bird species has a unique song or set of songs. Song conveys
both species and individual identity. In most species, young birds learn some features
of adult song. Song develops gradually from amorphous to fixed patterns of
vocalization as if crystals form out of liquid. Learning of a song proceeds in two
steps; birds commit the song to memory in the first stage and then they vocally
reproduce it in the second stage. The two stages overlap each other in some species,
while they are separated by several months in other species. The ability of a bird to
commit a song to memory is restricted to a period known as the sensitive phase. Vocal
reproduction of the memorized song requires auditory feedback. Birds deafened
before the second stage cannot reproduce the memorized song. Birds change vocal
output until it matches with the memorized song, which thus serves as a template.
Birds use a built-in template when a tutor model is not available. Exposure to a
tutor model modifies this innate template.
In many high latitude-breeding avian species, reproductive and wintering seasons are separated by migratory periods that involve dramatic physiological and behavioral adjustments such as hyperphagia and fat deposition. The endocrine mechanisms responsible for these adjustments have been extensively studied, yet remain only partly understood. The currently available information indicates that food consumption and/or fattening can be experimentally modulated by multiple hormones including testosterone, prolactin, glucocorticoids, and opioids. These hormones may control migratory functions through mutual interactions rather than independently. Little is known, however, concerning the nature of these interactions and their relative importance in the control of annual cycles in natural conditions. This paper focuses on the role of gonadal androgens in the control of migratory functions, and it summarizes the information which is available on the physiological and behavioral interactions between these androgens and other hormones.
Plasma levels of immunoreactive luteinizing hormone (irLH) and 5 steroid hormones have been measured through the course of the winter breeding season and vernal and autumnal migration in both sexes of the White-crowned Sparrow, Zonotrichia leucophrys gambelii. Birds were captured in mist nets or traps on wintering grounds in Washington and California and on the breeding area in the vicinity of Fairbanks, Alaska. Blood samples were collected from a wing vein as soon after capture as possible. Birds were then individually marked with a unique combination of 1 or 2 colored leg bands for identification in field observations and laparotomy performed to assess the reproductive state. After sampling, all birds were released for subsequent observation and recapture.
During autumn and winter, the levels of irLH and sex hormones in the plasma are low in both sexes. In spring (April and May), they begin to increase becoming maximal coincidentally with maximal gonadal weights, establishment of territory, mating and courtship. During incubation and feeding of young, plasma irLH and sex steroid levels decline to basal levels, but there is only a gradual decrease in weight of the testes. By the time parent birds are feeding fledglings, there is a rapid involution of the gonads followed closely by the onset of postnuptial molt.
Plasma levels of corticosterone are high in both sexes in January, but much lower in the early spring. In males during vernal migration, there is a dramatic increase to a high level that persists throughout the breeding season. In females, plasma hormone levels remain low during vernal migration, but then increase during the time of ovulation and oviposition. Basal levels in plasma corticosterone occur in both sexes during postnuptial molt. In contrast to vernal migration, a slight increase in plasma corticosterone occurs during autumnal migration in females, but not in males.
It is generally thought that most circuits of the adult central nervous system (CNS) are sculpted, in part at least, by selective elimination of some of the neurons present in an initial overabundant set. In this scenario, the birth of neurons precedes the period when brain functions, such as learning, first occur. In contrast to this form of brain assembly, we describe here the delayed development of the high vocal center (HVC) and one of its efferent pathways in canaries. The retrograde tracer Fluoro-Gold (FG) was injected into one of HVC's two efferent targets, the nucleus robustus archistriatalis (RA), to define the boundaries of HVC. The HVC grows markedly between 1 and 4 months, invading neighboring territories of the caudal telencephalon. During this same period, 0.43%-0.64% of the HVC neurons present at 1 year of age are labeled per day of [3H]-thymidine injection. [3H]-Thymidine labeling is a marker of cell birth, and during the first 4 months HVC neuron number increases, probably accounting for part of the HVC growth observed. Thereafter, the number of HVC neurons remains constant, but neuronal birth persists. We infer from this that neuronal replacement starts as early as 4 months after hatching and perhaps before then. About half of the neurons born after posthatching day 10 grow an axon to RA to form the main efferent pathway exiting from HVC. HVC growth, neurogenesis, axogenesis, and the observed replacement of neurons happen during the period of juvenile vocal learning. However, the recruitment of neurons that are still present at 1 year shows no particular inflections corresponding to the various stages in song learning, and continues at essentially the same rate after the more stereotyped adult song has been acquired. We suggest that a combination of neurogenesis and neuronal replacement provides unique advantages for learning.
Behavioral studies of song learning in birds continue to raise new problems for neuroethological investigation. Evidence is emerging for a new form of vocal plasticity, called 'action-based learning'. Motor patterns are overproduced during a particular phase of ontogeny, and are then subjected to attrition and selective reinforcement by various kinds of social stimulation as the young bird matures. This form of learning, analogous to operant conditioning, can occur at phases of development when the more traditional form of 'memory-based learning' is no longer possible. There is evidence that different physiological mechanisms are involved in the development and the maintenance of mature singing, with a transition occurring at the time of song crystallization. Neural events associated with the developmental stabilization of motor patterns are worthy of more study.
Birdsong is a learned behavior controlled by a distinct set of brain nuclei. The song nuclei known as area X, the medial nucleus of the dorsolateral thalamus (DLM), and the lateral magnocellular nucleus of the anterior neostriatum (L-MAN) form a pathway that plays an important but unknown role in song learning. One function served by this circuit might be auditory feedback, which is critical to normal song development. We used single unit recordings to demonstrate that all three of these nuclei contain auditory neurons in adult male zebra finches (Taeniopygia guttata). These neurons are song selective: they respond more robustly to the bird's own song than to songs of conspecific individuals, and they are sensitive to the temporal structure of song. Auditory neurons so highly specialized for song within a pathway required for song learning may play a role in the auditory feedback essential in song development. Recordings in the robust nucleus of the archistriatum (RA), the nucleus to which L-MAN projects, showed that RA also contains highly song-selective neurons. RA receives a direct projection from the caudal nucleus of the ventral hyperstriatum (HVc) as well as from L-MAN. We investigated the contributions of these two inputs to auditory responses of RA neurons by selectively inactivating one or both inputs. Our results suggest that there is a song-selective pathway directly from HVc to RA in addition to the circuit via L-MAN. Thus the songbird brain contains multiple auditory pathways specialized for song, and these circuits may vary in their functional importance at different stages of learning.
Estrogens and androgens each have unique effects but act together for the neural differentiation and control of sexual behaviors in male vertebrates, such as the canary. The neuronal basis for these synergistic effects is elusive because the spatial relation between estrogen target cells and androgen target cells is unknown. This study localized estrogen receptor (ER)-containing cells by using immunocytochemistry and androgen receptor (AR)-containing cells by using autoradiography in the same sections of the male canary brain. Three cell types, those containing only ER, those containing only AR, and those containing both ER and AR, were found in tissue-specific frequencies. The midbrain nucleus intercollicularis exhibited the highest number of cells expressing both ER and AR, whereas ER and AR are expressed only in disjunctive cell populations in the forebrain nucleus hyperstriatalis ventrale, pars caudale. Synergistic effects of androgens and estrogens for the neural behavorial control could result from cells containing both ER and AR (intracellular) and from neural circuits containing ER and AR in different cells (intercellular).
Area X, a large sexually dimorphic nucleus in the avian ventral forebrain, is part of a highly discrete system of interconnected nuclei that have been implicated in either song learning or adult song production. Previously, this nucleus has been included in the song system because of its substantial connections with other vocal control nuclei, and because its volume is positively correlated with the capacity for song. In order to directly assess the role of Area X in song behavior, this nucleus was bilaterally lesioned in both juvenile and adult zebra finches, using ibotenic acid. We report here that lesioning Area X disrupts normal song development in juvenile birds, but does not affect the production of stereotyped song by adult birds. Although juvenile-lesioned birds were consistently judged as being in earlier stages of vocal development than age-matched controls, they continued to produce normal song-like vocalizations. Thus, unlike the lateral magnocellular nucleus of the anterior neostriatum, another avian forebrain nucleus implicated in song learning, Area X does not seem to be necessary for sustaining production of juvenile song. Rather, the behavioral results suggest Area X is important for either the acquisition of a song model or the improvement of song through vocal practice.
Immunohistochemistry was used to map the distribution of four neuropeptides in song control regions of two songbird species, the European starling (Sturnus vulgaris) and the song sparrow (Melospiza melodia). We searched for positively stained cell bodies or apparent terminals containing vasoactive intestinal peptide (VIP), methionine-enkephalin (MET), cholecystokinin (CCK), and substance P (SUB P). Intraventricular colchicine pretreatment was administered to enhance the visualization of peptide-containing cell bodies. Four areas implicated in the central control of song were examined. Three of these areas are sexually dimorphic telencephalic nuclei characteristic of songbirds: the caudal nucleus of the ventral hyperstriatum (HVc), the robust nucleus of the archistriatum (RA), and the magnocellular nucleus of the anterior neostriatum (MAN). The fourth region is the mesencephalic nucleus intercollicullaris (ICo), common to all birds, which contains the dorsomedial nucleus (DM) that appears to be specifically involved in the motor control of song.
Previous work in songbirds has delimited a neural system responsible for song production and control. Earlier studies have suggested that functional capacity in the song system may be related to the mass of the system in an animal's brain, and that adult plasticity in this neural system may be related to adult capacity for behavioral modification. We now test these hypotheses in adult red-winged blackbirds (Agelaius phoeniceus), a species in which song is produced primarily by males, new song types are added to the male's repertoire in adulthood, and there are substantial differences among males in song complexity. We find that the song system in males is much larger than in females. Song system nuclei become smaller in both sexes as the animals experience shorter days. We do not find any association between repertoire size and size of any of the song system structures examined. Thus, although sex differences in song may be related to differences between sexes in the mass of song system structures, individual differences in song do not appear to be directly related to mass within males. Seasonal change in song system structures in male redwings is consistent with there being a relation between adult plasticity in anatomy and in behavior; the large seasonal change in these structures in females suggests large seasonal changes in the function of these nuclei.
In zebra finches the song control nuclei hyperstriatum ventralis pars caudalis (HVc) and area X of the lobus parolfactorius (LPO), continue to add new neurons during the juvenile period of song learning. Normally, males add many more of these new cells than do females (who do not sing), leading to pronounced sexual dimorphism within these regions. Exposing females to estradiol (E2) shortly after hatching masculinizes the HVc and area X and such females sing in response to later androgen stimulation. We investigated whether exposing female hatchlings to E2 stimulates the incorporation of HVc and area X neurons born during the juvenile period, and whether later androgen stimulation further influences addition of these late-generated neurons. Females were implanted with E2 on day 3 and received either empty or dihydrotestosterone (DHT)-filled capsules on day 25. These females, and normal males and females received [3H]thymidine daily between 20 and 40 days and were killed at 65 days. Autoradiographic analyses of HVc and area X-LPO revealed that neuron number, as well as the incidence and number of thymidine-labeled neurons was increased in E2-treated females to levels approaching those typical of males. DHT did not further influence these measures in females. These data indicate that E2 promotes either the production, migration, or survival of HVc and area X neurons born during the juvenile period.
During song learning in birds, neurons are added to some song nuclei and lost from others. Previous studies have been unable to distinguish whether these neural changes are uniquely associated with memorizing a song model (sensory acquisition) or vocal practice (sensorimotor learning). In this study we measured changes in neuron number within song nuclei of swamp sparrows, a species in which the two phases of song learning are nonoverlapping. Male swamp sparrows were collected as hatchlings and tape-tutored from approximately 22 to 62 days of age. Swamp sparrows memorize about 60% of their song material during this period, but do not begin practicing this learned material until approximately 275 days of age. Birds were sacrificed at 23, 41, 61, 71, 274, or 340 days of age. During sensory acquisition, neuron number increased drastically in both the caudal nucleus of the ventral hyperstriatum (HVc) and Area X. The period of sensorimotor learning was not associated with any further changes in neuron number within these regions. We were unable to detect any significant changes in neuron number within the magnocellular nucleus of the neostriatum or the robust nucleus of the archistriatum during either stage of song learning. These results raise the possibility that ongoing addition of HVc and Area X neurons may encourage, and thereby temporally restrict, song acquisition.
Estrogens play an important role in the activation and differentiation of vocal behavior in male zebra finches. In the present experiment, we conducted a series of in vitro binding assays to quantify estrogen receptor concentrations in individual hypothalamic and vocal control nuclei. Receptor concentrations were measured in cytosol fractions obtained from castrated males and, since adrenalectomy is not a viable possibility in this species, in castrated males treated with 1,4,6-androstatriene-3,17-dione (ATD), an inhibitor of estrogen synthesis. Specific, high-affinity estrogen binding was detected in both untreated castrates and castrates treated with ATD. Although ATD treatment had no effect on estrogen receptors in hypothalamic-preoptic tissue, ATD-treated males had significantly higher levels of [3H]estrogen binding in 3 vocal control nuclei: the dorsomedial portion of the intercollicular nucleus (DM), the magnocellular nucleus of the anterior neostriatum (MAN), and Area X. Low levels of estrogen binding were also detected in cytosol from the caudal portions of the ventral hyperstriatum (HVc) and the robust nucleus of the archistriatum (RA) of both untreated and ATD-treated castrates. In most brain regions examined, estrogen receptor levels were lower than androgen receptor levels measured in previous experiments. The presence of both androgen- and estrogen-concentrating neurons in these areas provides compelling evidence for the interaction of androgens and estrogens in the neural control of male vocal behavior in this species.
Male birdsong is generally regarded as a secondary sexual characteristic under the control of gonadal steroids. Song typically waxes and wanes with the seasonal cycle of testicular growth and regression and decreases after adult castration. Testosterone therapy reinstates song, induces it in females, augments it in intact males, and spring testosterone profiles correlate with seasonal song production. Thus, testosterone has been viewed as a major factor in song acquisition and production acting either directly, or after aromatization within the brain. We show here, however, that song learning and early phases of the development of singing both take place in castrated male birds with no significant levels of testosterone in their blood plasma. Testosterone seems to be required for song crystallization, however. Oestradiol was unexpectedly still present after castration, evidently from a non-testicular source, throughout the period of male song acquisition.
Male birdsong is a sexually dimorphic behavior characterized by learned dialects. In a combined study of learning in relation to steroid levels in the plasma, changes in estradiol and testosterone levels were correlated with the timing of the sensitive period for song acquisition and with successive stages in song development. Male swamp sparrows were trained with a changing series of live singing tutors from 26 days to 1 year of age. Song acquisition was concentrated between 26 and 47 days of age (57%). By 85 days of age 71% of acquisition was completed; some occurred as late as 300 days. There were two major periods when testosterone levels were elevated. The first, from 30-80 days, encompassed most of the period of song acquisition. The second, from 260 to at least 360 days of age, coincided with song development. Estradiol levels were elevated from 18 to 170 days of age, encompassing almost all of the period of song acquisition. A marked estradiol peak between 40 and 50 days coincided with a trough in testosterone levels and a hiatus in song acquisition. The strong correlation between the second period of elevated testosterone and song motor development suggests a causal connection, with levels peaking in mid-development and declining during mature song production. Estradiol levels were elevated at the start of the study and remained so during early subsong production, from 30 to 165 days. They then fell to baseline, remaining there throughout the resumption of subsong and plastic song production at 250-326 days. Both estradiol and testosterone are candidates for possibly affecting song acquisition.
Young male canaries become sexually mature in late winter, 8-12 months after hatching. During the months between hatching and sexual maturity they develop adult song. The successive stages in the development of adult song are subsong, plastic song, and stable or full song. Once stable song is achieved it lasts for the duration of the breeding season. After the end of the breeding season there is a recurrence of song instability during summer and early fall. This plastic song is followed, once more, by stable song. New song syllables are added to the song of adult male canaries and some of the earlier syllables disappear. The song repertoire sung at 2 years of age is substantially larger, and different, from that sung during the first breeding season, when the birds were 1 year old. A comparable change occurs between the second and third breeding seasons. Most of the syllables acquired by adult males are formed during the summer-fall period of song instability. Developmental and seasonal changes in song are accompanied by anatomical changes in two forebrain nuclei known to be involved in song control, the hyperstriatum ventralis, pars caudalis (HVc), and the robust nucleus of the archistriatum (RA). HVc and RA grow during the subsong and plastic song periods of song development. These nuclei reach adult size by the time stable adult song is first produced, and retain this size during the breeding season. However, the size of HVc and RA diminishes by late summer, when it becomes comparable to that of a 3- to 4-month-old bird. This reduction in size is temporary and has been corrected by the following breeding season. It is suggested that these seasonal changes in volume reflect circuit changes which are under hormonal control, and that these changes are related to processes of learning and, possibly, forgetting. Despite earlier reports of left hemispheric dominance in canary song production, we failed to find any evidence of right-left systematic differences in the size of HVc and RA during development or in adulthood. Various hypotheses relating song learning to changes in the underlying anatomy are offered.
A stereotaxic atlas of the telencephalon, diencephalon and mesencephalon of the canary, Serinus canaria, was prepared for use in anatomical and behavioral experiments. Canaries have a complex vocal and behavioral repertoire many of whose components are under hormonal control in the male, and are therefore useful for many physiological and anatomical experiments. They are available commercially, breed easily in captivity, are quite hardy and respond well to anesthetic and surgical procedures.
The atlas consists of 30 frontal plates from the frontal pole to the level of the motor nucleus of the trigeminus. One sagittal plate is included for reference purposes. Six birds (three males and three females) with marking lesions were used to make the atlas. Their brains were embedded in albumin-gelatin media, cut at 50 and 25μ and stained with cresyl violet for cell bodies, Weil stain for myelinated fibers and the Fink-Schneider method for unmyelinated fibers. Plates were drawn from the cresyl violet series and labeled using all three stains.
The completed atlas was tested for accuracy by making 12 small lesions in a number of predetermined discrete loci in several birds and evaluating their placement. Eleven of these lesions were found to be within the targeted structure. The results of this test, combined with the results of experiments in over 50 birds, have shown the atlas to be accurate in 80% of all cases.
The magnocellular nucleus of the anterior neostriatum is a forebrain nucleus of passerine birds that accumulates testosterone
and makes monosynaptic connections with other telencephalic nuclei that control song production in adult birds. Lesions in
the magnocellular nucleus disrupted song development in juvenile male zebra finches but did not affect maintenance of stable
song patterns by adult birds. These results represent an instance in which lesions of a discrete brain region during only
a restricted phase in the development of a learned behavior cause permanent impairment. Because cells of the magnocellular
nucleus accumulate androgens these findings raise the possibility that this learning is mediated by hormones.
Male canaries that have reached sexual maturity can, in subsequent years, learn new song repertoires. Two telencephalic song control nuclei, the hyperstriatum ventrale, pars caudale, and nucleus robustus archistriatalis are, respectively, 99 and 76 percent larger in the spring, when male canaries are producing stable adult song, than in the fall, at the end of the molt and after several months of not singing. It is hypothesized that such fluctuations reflect an increase and then reduction in numbers of synapses and are related to the yearly ability to acquire new motor coordinations.
Two vocal control nuclei of the canary telencephalon, hyperstriatum ventrale, pars caudale (HVc) and nucleus robustus archistriatalis (RA), are larger in males, that learn complex songs, than in females, that normally do not sing. HVc and RA can be induced to grow by 90% and 53%, respectively, in adult gonadectomized females under the influence of testosterone, as these birds acquire male-like song. The magnitude of this effect is comparable, though of reversed sign, to that following early castration in males. This system is unique in the extent to which gross neural plasticity normally associated with early development can be induced in adulthood.
Previous studies have found opioid peptide-like immunoreactivity in avian vocal control regions, but whether these regions contain receptors for opioid peptides has not been examined. To address this question, we used quantitative in vitro autoradiography to determine the anatomical distribution and to measure the densities of mu, delta, and kappa opioid receptors in vocal control regions (area X, higher vocal center, and nucleus intercollicularis) of adult male dark-eyed juncos (Junco hyemalis). To evaluate whether opioid receptor densities in these regions depend on the activity of the reproductive system, we also measured these densities in birds collected during the spring, summer, and fall. We found area X, the higher vocal center, and nucleus intercollicularis to contain the three receptor types under study, but opioid receptor densities did not vary seasonally in any of these regions. The presence of specific opioid receptors in avian vocal control regions suggests the participation of opioids in the control of vocal behavior. This participation may consist of short-term (e.g., auditory processing) and/or long-term (e.g., neuronal plasticity) influences.
Brain nuclei that control song are larger in male canaries, which sing, than in females, which sing rarely or not at all. Treatment of adult female canaries with testosterone (T) induces song production and causes song-control nuclei to grow, approaching the volumes observed in males. For example, the higher vocal center (HVC) of adult females approximately doubles in size by 1 month following the onset of T treatment. Male HVC projects to a second telencephalic nucleus, RA (the robust nucleus of the archistriatum), which projects in turn to the vocal motor neurons. Whether HVC makes a similar connection in female canaries is not known, although HVC and RA are not functionally connected in female zebra finches, a species in which testosterone does not induce neural or behavioral changes in the adult song system. This experiment investigated whether HVC makes an efferent projection to RA in normal adult female canaries, or if T is necessary to induce the growth of this connection. In addition, we examined whether T-induced changes in adult female canary brain are reversible. Adult female canaries received systemic T implants that were removed after 4 weeks; these birds were killed 4 weeks after T removal (Testosterone-Removal, T-R). Separate groups of control birds received either (a) T implants for 4 weeks which were not removed (Testosterone-Control, T-C) or (b) empty implants (Untreated-Control, O-C). Crystals of the fluorescent tracer DiI were placed in the song-control nucleus HVC in order to anterogradely label both efferent targets of HVC, RA and Area X. Projections from HVC to RA and Area X were present in all treatment groups including untreated controls, and did not appear to differ either qualitatively or quantitatively. Thus, formation of efferent connections from HVC may be prerequisite to hormone-induced expression of song behavior in adult songbirds. The volumes of RA and Area X were measured using the distribution of anterograde label as well as their appearance in Nissl-stained tissue. RA was larger in T-treated control birds than in untreated controls. Experimental birds in which T was given and then removed (T-R) had RA volumes closer in size to untreated controls (O-C). Because the volume of RA in T-treated controls (T-C) was larger than that of birds that did not receive T (O-C), we conclude that the volume of RA increased in both T-C and T-R birds but regressed upon removal of T in T-R birds.(ABSTRACT TRUNCATED AT 400 WORDS)
Several landmark discoveries have shaped the recent study of brain substrates for birdsong. The failure of deaf birds to reproduce a song from memory lent support for the concept of a song template. An attempt to test this idea resulted in the discovery of lateralization of song control. Search for the brain sites of lateralization and auditory control of voice led to the discovery of the main song control nuclei. Neurophysiological studies have unequivocally shown that auditory information reaches the song control system, but the exact pathway by which the song control system receives auditory inputs needs further investigation. The finding that lesions of the lateral magnocellular nucleus of the anterior neostriatum or area X affect song development in young birds but not the maintenance of song in adults suggested a role of the anterior forebrain pathway to RA in song learning. Another area of research in which much progress has been made concerns the relationships between the vocal and respiratory systems. The archistriatal and midbrain vocal nuclei innervate some of the respiratory centers in the medulla. The old questions of 'mini-breath' during fast singing and independent control of the two sides of the syrinx have been resolved. Finally, comparisons of the vocal and auditory systems between taxa indicate that different groups may use different neural circuits to achieve similar vocal-auditory behavior.
Estrogens play an important role in the control and differentiation of species-typical behavior and in endocrine homeostasis of birds, but the distribution and evolution of cells that contain estrogen receptors in the avian brain are poorly understood. This study therefore surveys 26 species in the avian orders Anseriformes (1 species), Galliformes (2), Columbiformes (3), Psittaciformes (1), Apodiformes (2), and Passeriformes (3 suboscines, 14 oscines). Indirect immunocytochemistry with the estrogen receptor (ER) antibody H222Spy revealed a general pattern of ER-antibody-immunoreactive cells (ER-IRC) in all 26 species, with ER-IRC in consistent, well-defined locations in the limbic forebrain, the midbrain striatum, the hippocampus, the hindbrain, and especially in the preoptic area and the tuberal hypothalamus. For some species, the microdistribution of ER-IRC in some of these general areas differed, such as in the hippocampus and the anterior hypothalamus of suboscine species and in the preoptic area of the Japanese quail. Brains of oscine songbirds of both sexes, unlike brains of nonsongbirds, had ER-IRC in three specific structures of the nonlimbic forebrain: in the area surrounding the nucleus robustus archistriatalis; in the rostral forebrain; and, for all individuals, in the caudale neostriatum, including the nucleus hyperstriatalis ventrale, pars caudale (HVc). Among songbird families or subfamilies, adult males of the Estrildinae had much lower numbers of ER-IRC in HVc than did adult males of the Fringillidae, Paridae, Sturnidae, and Ploceinae. Differences occurred, too, among closely related species: the songbird canary (Serinus canaria) had an ER-IRC area in the rostral forebrain that was lacking in all other songbird species, including other cardueline finches. The cells with ER that are found only in the songbird forebrain but not in reptiles, nonpasserine birds, and nonoscine passerine birds very likely coevolved with steroid-dependent differentiation of vocal control areas. The songbird-specific expression of ER in the forebrain could be an example in which taxon-specific behavior is due to taxon specific neurochemical properties of the brain.
Male canaries revise their vocal repertoire every year. Early work indicated that the volume and neuron number of the song-control nucleus HVC (Higher Vocal Center) declined in late-summer/fall as birds added and deleted syllables from their repertoire, and increased in spring as the set of song syllables stabilized to a fixed number. Seasonal variation in serum testosterone levels suggested that these changes in brain and behavior were regulated by testosterone (T). However, although initial studies describing growth and regression of HVC used Nissl-staining to define its borders, recent experiments that have measured the distribution of identified populations of HVC cells (projection neurons, hormone target cells) suggest that there are no seasonal changes in HVC volume or neuron number. In order to clarify the role of T in the regulation of HVC morphology, we castrated male canaries, maintained them on short (fall-like) days, and treated them with either T, antisteroid drugs, or nothing. After 1 month of treatment, we used a double-labeling technique to characterize HVC projection neurons and androgen target cells. The results showed that hormonal manipulation influenced HVC volume, the density and size of HVC cells, and the absolute number and percentage of androgen target cells in HVC. Hormonal manipulation did not influence the absolute number of cells in HVC. Moreover, the distribution of projection neurons, androgen target cells, and the Nissl-defined borders of HVC were closely aligned in all experimental groups, indicating that exposure to T and/or its metabolites (estradiol and dihydrotestosterone) regulates the overall size of HVC by affecting the distributions of both projection neurons and androgen target cells. Analysis of double-labeling results suggests that T specifically influences both cell size and the ability to accumulate androgen among HVC neurons that project to the robust nucleus of the archistriatum (RA). The results of this study show that steroid hormones exert potent effects on HVC morphology in male canaries, but differences between our results and studies of seasonal males suggest there may be additional factors that can regulate HVC morphology.
White-throated sparrows are unusual among songbirds in that they occur in two color morphs, white-striped and tan-striped, determined by a chromosomal inversion and maintained by negative assortative mating. These differ in several reproductive behaviors, including amount of singing: white-striped males sing frequently, tan-striped females never sing, and tan-striped males and white-striped females sing an intermediate amount. The present study measures the volumes of several nuclei in the avian song system and relates these to color morph and to sex. We find that robustus archistristalis and the tracheosyringeal part of the hypoglossal nucleus, nuclei closely involved in song production, are larger in white-striped than in tan-striped birds. We also find morph differences for nuclei in the rostral division of the song system, nuclei believed to be less directly involved in song production. We find sex differences throughout the song system as has been reported in other songbirds. Relationships between structure and function in the song system are discussed.
Bird song is a complex, learned behavior. Vocal learning in sparrows involves several different processes that occur in a distinct temporal pattern over the course of the first year of life. Songs are acquired without practice during a sensitive period within the first 3 months of life and rehearsal of the acquired song does not begin until 7 or 8 months of age. The function of the storage period between song acquisition and production is not known. We set out to investigate its significance by administering testosterone, known to stimulate production of adult song, to birds at 100 days of age after song acquisition was completed but some 5 months prior to normal song onset. Most testosterone-treated birds produced abnormal songs resembling those of males raised in acoustic isolation suggesting that, in sparrows, events occurring during the storage phase play a significant role in vocal learning.
In males of several songbird species, the morphology of forebrain nuclei that control song changes seasonally. The only seasonally breeding songbird in which seasonal changes in the structure of song control nuclei have been reported not to occur is the nonmigratory Nuttall's subspecies of white-crowned sparrow. In the present study, we manipulated photoperiod and plasma testosterone concentrations in captive male white-crowned sparrows of the migratory Gambel's subspecies. Males exposed to photoperiods and plasma testosterone concentrations typical of those experienced by wild breeding males had larger song control nuclei than males held on a winter photoperiod. We also found seasonal changes in stereotype of spectral and temporal parameters of song in wild Gambel's white-crowned sparrows. We hypothesize that seasonal changes in the song control nuclei may correlate with seasonal changes in song stereotypy.
Most studies of seasonal changes in the avian song control system have used Nissl stains to characterize the nuclei. More recent work has indicated that changes in nucleus volume evident in Nissl-stained tissue are not always apparent when investigated with other histochemical criteria. In this experiment, we used two different markers (Nissl stain and alpha 2-adrenergic receptor autoradiography) to characterize changes in the song system of European starlings (Sturnus vulgaris). Fluctuating levels of circulating testosterone (T) appear to be causally related to seasonal changes in the song system. Therefore, we used photoperiod manipulations to place male starlings into different physiological conditions. Photosensitive male starlings were placed on 11L:13D or 16L:8D photoperiods for at least 5 months. Birds on 11L:13D have enlarged gonads and circulating T. In contrast, starlings maintained on 16L:8D initially show marked gonadal growth. However, after about 6-8 weeks the birds are photorefractory (i.e., the gonads are regressed and T falls to undetectable levels). The volume of the high vocal center (HVC) was 44% larger in the 11L:13D than in 16L;8D birds in Nissl-stained tissue. The density of alpha 2-adrenergic receptors as determined by in vitro receptor autoradiography with [3H]p-amino-clonidine (PAC) is higher in HVC than in the surrounding neostriatum, clearly delineating the boundaries of the nucleus. We reconstructed the volume of HVC using PAC stained tissue. Thus, two histochemical markers indicate a photoperiodic difference in HVC volume of male starlings.
Seasonal changes in the brain nuclei that control song behavior in songbirds are among the most striking examples of plasticity in the adult vertebrate brain. Although seasonal changes in the size of these brain nuclei have been found in several species in captivity, results on seasonal changes in the song nuclei of wild songbirds have been equivocal. In the present study, I measured plasma testosterone (T) concentrations and the size of song nuclei across seasons in wild male rufous-sided towhees (Pipilo erythrophthalmus). I found seasonal changes in both T concentrations and the size of song nuclei that were as large as or larger than those observed in this species in captivity. These results demonstrate that seasonal plasticity of the song nuclei occur in wild, as well as captive, songbirds.
Seasonal plasticity in the morphology of telencephalic nuclei that control song behavior has been reported for diverse species of songbirds. The only published report of a lack of seasonal changes in the song nuclei of a seasonally breeding bird is that of Baker et al. in the Nuttall's subspecies of white-crowned sparrow (Zonotrichia leucophrys nuttalli). In this study, they brought wild birds into the laboratory and exposed them to either "summer" or "winter" photoperiods. Previous studies have shown that exposing wild-caught white-crowned sparrows to long-day photoperiods in the laboratory may not induce circulating concentrations of testosterone (T) as high as those seen in wild breeding birds. Changes in circulating T are primarily responsible for the seasonal morphological changes in the song nuclei. To determine whether there is seasonal plasticity of the song system in this subspecies, we measured circulating T, morphological attributes of the song nuclei, and song behavior in wild Nuttall's white-crowned sparrows during the spring and fall. Testis size and circulating T concentrations were greater in spring than fall birds. The absolute volumes of the song nuclei HVc, RA, and Area X, and their volumes relative to those of either the total telencephalon or three thalamic nonsong nuclei, were significantly greater in the spring than fall sparrows. Song behavior also changed seasonally; fall birds sang shorter songs than did spring birds. These results show that there is seasonal plasticity of the song system in wild Nuttall's white-crowned sparrows. Seasonal plasticity can now be regarded as a common feature of the seasonally breeding songbirds studied thus far.
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