Article

Melatonin Binding in the House Sparrow Song Control System: Sexual Dimorphism and the Effect of Photoperiod

January 1997
Hormones and Behavior 30(4):528-37

January 1997
30(4):528-37

DOI:10.1006/hbeh.1996.0056

Source
PubMed

Authors:

Vincent M Cassone

University of Kentucky

Avian song is a sexually dimorphic behavior which is regulated seasonally. This regulation involves the construction and growth of song control structures: the high vocal center (HVC), nucleus robustus archistrialis (RA), nucleus magnocellularis anterior (MAN), and Area X. Song behavior and its neural correlates are controlled by steroid-dependent and independent processes. The avian circadian system is known to be involved in both daily processes and seasonal reproduction. A major part of this system is the circadian secretion of melatonin by the pineal gland. To determine possible interactions of the circadian and song control systems, the distribution and density of 2-[125I]iodomelatonin (IMEL) binding, an indicator of melatonin sensitivity, were determined in male and female house sparrow brains. Specific binding was found in visual system centers of both genders, but binding in HVC, RA, and Area X was present only in males. Binding in MAN was present in both sexes. Although the effects of short and long photoperiods on male house sparrow IMEL binding in song structures revealed no systematic changes, there were significant differences in binding under different photoperiods in HVC and RA. IMEL binding in the tectofugal nucleus rotundus, however, was consistently highest under short day conditions. IMEL binding in song control nuclei was independent of testicular influence, since castration did not affect it significantly. The data point to a role for the circadian system of house sparrows in song control, but a specific role for melatonin in the daily or seasonal regulation of the song control system in birds, could not be determined.

The influence of melatonin on birdsong and its underlying neuronal correlates

Thesis

Jan 2016

Susanne Seltmann

The role of the pineal gland in the photoperiodic control of bird song frequency and repertoire in the house sparrow, Passer domesticus

Article

Apr 2014

Temperate zone birds are highly seasonal in many aspects of their physiology. In mammals, but not in birds, the pineal gland is an important component regulating seasonal patterns of primary gonadal functions. Pineal melatonin in birds instead affects seasonal changes in brain song control structures, suggesting the pineal gland regulates seasonal song behavior. The present study tests the hypothesis that the pineal gland transduces photoperiodic information to the control of seasonal song behavior to synchronize this important behavior to the appropriate phenology. House sparrows, Passer domesticus, expressed a rich array of vocalizations ranging from calls to multisyllabic songs and motifs of songs that varied under a regimen of different photoperiodic conditions that were simulated at different times of year. Control (SHAM) birds exhibited increases in song behavior when they were experimentally transferred from short days, simulating winter, to equinoctial and long days, simulating summer, and decreased vocalization when they were transferred back to short days. When maintained in long days for longer periods, the birds became reproductively photorefractory as measured by the yellowing of the birds’ bills; however, song behavior persisted in the SHAM birds, suggesting a dissociation of reproduction from the song functions. Pinealectomized (PINX) birds expressed larger, more rapid increases in daily vocal rate and song repertoire size than did the SHAM birds during the long summer days. These increases gradually declined upon the extension of the long days and did not respond to the transfer to short days as was observed in the SHAM birds, suggesting the pineal gland conveys photoperiodic information to the vocal control system, which in turn regulates song behavior.

Melatonin Affects the Temporal Pattern of Vocal Signatures in Birds

Article

Mar 2012
J PINEAL RES

In humans and other animals, melatonin is involved in the control of circadian biological rhythms. Here, we show that melatonin affects the temporal pattern of behavioral sequences in a noncircadian manner. The zebra finch (Taeniopygia guttata) song and the crow of the Japanese quail (Coturnix japonica) are courtship vocalizations composed of a stereotyped sequence of syllables. The zebra finch song is learned from conspecifics during infancy, whereas the Japanese quail crow develops normally without auditory input. We recorded and analyzed the complete vocal activity of adult birds of both species kept in social isolation for several weeks. In both species, we observed a shortening of signal duration following the transfer from a light-dark (LD) cycle to constant light (LL), a condition known to abolish melatonin production and to disrupt circadian rhythmicity. This effect was reversible because signal duration increased when the photoperiod was returned to the previous LD schedule. We then tested whether this effect was directly related to melatonin by removal of the pineal gland, which is the main production site of circulating melatonin. A shortening of the song duration was observed following pinealectomy in LD. Likewise, melatonin treatment induced changes in the temporal structure of the song. In a song learning experiment, young pinealectomized finches and young finches raised in LL failed to copy the temporal pattern of their tutor's song. Taken together, these results suggest that melatonin is involved in the control of motor timing of noncircadian behavioral sequences through an evolutionary conserved neuroendocrine pathway.

Melatonin duration gates photoperiodic vocal state change in a songbird

Article

Nov 2019

Seasonally breeding animals concentrate courtship to a particular time of year such that their offspring will be reared in a favorable environment. In house sparrows, Passer domesticus, primary (gonads) and secondary (song, plumage, beak color, etc) sexual characteristics are expressed differentially depending on the photoperiod. Removal of the pineal gland (PINX) has no effect on seasonal rhythms in gonad size but alters the photostimulated increase in vocal rate and complexity. Administration of long durations of melatonin, indicative of short days of winter, prevents seasonal recrudescence of song control nuclei in photostimulated house sparrows. In this study, male PINX house sparrows were exposed to three durations of melatonin while song and locomotor behavior were recorded as they were transitioned from short photoperiod to equinoctial photoperiods of spring. Birds receiving short duration melatonin or vehicle control increased dawn and dusk choruses as well as call complexity. Long durations of melatonin prevented this expansion to a spring‐like vocal state observed in birds receiving the short duration of melatonin or vehicle control. The daily distribution of locomotor activity, beak color and testis size were unaffected by treatment. Vocal state change was defined by our measures in two capacities: (i) increased dawn and dusk choruses, and (ii) an increase in calls associated with territory and mate attraction compared to the winter‐like “social song”. We conclude that house sparrows use the calendar information provided by melatonin duration to control seasonal vocalization behavior, independent of effects on and of the gonads.

Differential Expression of Melatonin Receptor Subtypes MelIa, MelIb and MelIc in Relation to Melatonin Binding in the Male Songbird Brain

Article

Nov 2014
BRAIN BEHAV EVOLUT

Previous autoradiography studies illustrated that several areas of the avian brain can bind the pineal hormone melatonin. In birds, there are three melatonin receptor (MelR) subtypes: MelIa, MelIb and MelIc. To date, their brain distribution has not been studied in any passerine bird. Therefore, we investigated mRNA distribution of MelR subtypes in adjacent sections of the brain of two songbirds, the blackcap and the zebra finch, in parallel with that of 2-[(125)I]-iodomelatonin (IMEL) binding sites in the same brains. The general pattern of receptor expression shown by in situ hybridization of species-specific probes matched well with that of IMEL binding. However, the expression of the three subtypes was area specific with similar patterns in the two species. Some brain areas expressed only one receptor subtype, most brain regions co-expressed either MelIa with MelIb or MelIa with MelIc, whereas few areas expressed MelIb and MelIc or all three receptor subtypes. Since many sensory areas, most thalamic areas and subareas of the neopallium, a cortex analogue, express MelR, it is likely that most sensory motor integration functions are melatonin sensitive. Further, the area-specific expression patterns suggest that the regulatory role of melatonin differs among different brain areas. Since subareas of well-defined neural circuits, such as the visual system or the song control system, are equipped with different receptor types, we hypothesize a diversity of functions for melatonin in the control of sensory integration and behavior. © 2014 S. Karger AG, Basel.

Duration of melatonin regulates seasonal plasticity in subtropical Indian weaver bird, Ploceus philippinus

Article

Jan 2014
GEN COMP ENDOCR

Day length regulates seasonal plasticity connected with reproduction in birds. Rhythmic pineal melatonin secretion is a reliable indicator of the night length, hence day length. Removal of rhythmic melatonin secretion by exposure to constant bright light (LLbright) or by pinealectomy renders several species of songbirds including Indian weaver bird (Ploceus philippinus) arrhythmic. Present study investigated whether rhythmic melatonin is involved in the regulation of key reproductive neuropeptides (GnRH I and GnIH) and reproduction linked neural changes, viz. song control nuclei, in Indian weaver birds. Two experiments were performed using birds in an arrhythmic condition with low (under LLbright) or no (in the absence of pineal gland) endogenous melatonin. In experiment I, three groups of birds (n = 5 each) entrained to 12L:12D were exposed to LLbright (25 lux) for two weeks. Beginning on day 15 of LLbright, a control group received vehicle for 16 h and two treatment groups were given melatonin in drinking water for 8 h or 16 h. In experiment II, one group of sham-operated and three groups of pinealectomized birds (n = 5 each) entrained to 12L:12D were exposed to constant dim light (LLdim, 0.5 lux). Beginning on day 15 of LLdim, three groups received similar treatment as in experiment I. Birds were perfused after thirty cycles of the melatonin treatment, and brain sections were immunohistochemically double-labeled for GnRH I and GnIH or Nissl stained. Activity was recorded throughout the experiments, while body mass and testes were measured at the beginning and end of the experiment. Birds were synchronized with melatonin cycles and measured the duration of melatonin as “night”. Pinealectomized birds that received 16 h of melatonin had significantly higher GnIH-ir cells than those received 8 h melatonin; there was no difference in the GnRH I immunoreactivity between two treatment groups however. Intact birds that received long duration melatonin cycles exhibited small song control nuclei, specifically the high vocal center (HVC) and the robust nucleus of the arcopallium (RA), while birds that received short duration melatonin or no melatonin exhibited large HVC and RA. Thus, melatonin possibly regulates seasonal reproduction via GnIH secretion, and also controls seasonal neuroplasticity in the song control system in songbirds.

Duration of melatonin regulates seasonal plasticity in subtropical Indian weaver bird, Ploceus philippinus

Article

Jun 2014

Melatonin action in a midbrain vocal-acoustic network

Article

Nov 2013
J EXP BIOL

Melatonin is a well-documented time-keeping hormone that can entrain an individual's physiology and behavior to the day-night cycle, though surprisingly little is known about its influence on the neural basis of social behavior, including vocalization. Male midshipman fish (Porichthys notatus) produce several call types distinguishable by duration and by daily and seasonal cycles in their production. We investigated melatonin's influence on the known nocturnal- and breeding season-dependent increase in excitability of the midshipman's vocal network (VN) that directly patterns natural calls. VN output is readily recorded from the vocal nerve as a "fictive call." Five days of constant light significantly increased stimulus threshold levels for calls electrically evoked from vocally active sites in the medial midbrain, supporting previous findings that light suppresses VN excitability, while 2-iodomelatonin (2-IMel; a melatonin analogue) implantation decreased threshold. 2-IMel also increased fictive call duration evoked from medial sites as well as lateral midbrain sites that produced several-fold longer calls irrespective of photoregime or drug treatment. When stimulus intensity was incrementally increased, 2-IMel increased duration only at lateral sites, suggesting melatonin action is stronger in the lateral midbrain. For animals receiving five days of constant darkness, known to increase VN excitability, systemic injections of either of two mammalian melatonin receptor antagonists increased threshold and decreased duration for calls evoked from medial sites. Our results demonstrate melatonin modulation of vocal network excitability and suggest that social context-dependent call types differing in duration may be determined by neuro-hormonal action within specific regions of a midbrain vocal-acoustic network.

Avian Circadian Organization: A Chorus of Clocks

Article

Oct 2013
FRONT NEUROENDOCRIN

Vincent M Cassone

Circannual Transitions in Gene Expression: Lessons from Seasonal Adaptations

Article

Aug 2013

Circannual timing is important for the coordination of seasonal activities, particularly promoting the survival of individuals in adverse conditions through adaptive physiological and behavioral changes. This includes optimizing the survival of offspring by coordinating reproductive efforts at appropriate times. Thus, timing is very important for overall fitness. In this chapter, we provide several examples of circannually timed events, including mammalian hibernation, discussing the physiological changes that accompany these events, and some of the known genes and pathways underlying these changes. We then describe five candidate systems that are potentially involved in circannual timing. Finally, we discuss several recent advances in molecular biology and animal husbandry that have made the use of nonmodel organisms for research more feasible, which will hopefully promote and encourage further advancement in the knowledge of circannual timing.

Time's arrow flies like a bird: Two paradoxes for avian circadian biology

Article

Feb 2009
GEN COMP ENDOCR

Biological timekeeping in birds is a fundamental feature of avian physiology, behavior and ecology. The physiological basis for avian circadian rhythmicity has pointed to a multi-oscillator system of mutually coupled pacemakers in the pineal gland, eyes and hypothalamic suprachiasmatic nuclei (SCN). In passerines, the role of the pineal gland and its hormone melatonin is particularly important. More recent molecular biological studies have pointed to a highly conserved mechanism involving rhythmic transcription and translation of "clock genes". However, studies attempting to reconcile the physiological role of pineal melatonin with molecular studies have largely failed. Recent work in our laboratory has suggested that melatonin-sensitive physiological processes are only loosely coupled to transcriptional oscillations. Similarly, although the pineal gland has been shown to be critical for overt circadian behaviors, its role in annual cycles of reproductive function appears to be minimal. Recent work on the seasonal control of birdsong, however, suggests that, although the pineal gland does not directly affect gonadal cycles, it is important for seasonal changes in song. Experimental analyses that address these paradoxes will shed light on the roles the biological clock play in birds and in vertebrates in general.

Constant light and pinealectomy disrupt daily rhythm in song production and negatively impact reproductive performance in zebra finches

Article

Mar 2024
PHOTOCH PHOTOBIO SCI

We assessed the circadian clock control of singing and reproductive performance in zebra finches. Experiment 1 examined changes in body mass, testis size, and plasma corticosterone and testosterone levels in male birds exposed to constant light (LL, 100 lx) and constant darkness (DD, 0.5 lx), with controls on 12L:12D (L = 100 lx, D = 0.5 lx). There was a significant increase in the body mass and testis size under LL and a decrease in testis size under the DD. Using a similar design, experiment 2 assessed the persistence of the circadian rhythm in singing along with activity–rest pattern in cohort I birds that were entrained to 12L:12D and subsequently released in DD or LL, and in cohort II birds that were entrained to 12L:12D and following pinealectomy were released in DD. Both activity and singing patterns were synchronized with the light phase under 12L:12D, free-ran with a circadian period under DD, and were arrhythmic under the LL. There was an overall decreased and increased effect on singing under DD and LL, respectively, albeit with differences in various song parameters. The pinealectomy disrupted both activity and singing rhythms but did not affect singing or the overall song features. Pinealectomized bird pairs also exhibited a significant reduction in their nest-building and breeding efforts, resulting in a compromised reproductive performance. These results suggest a circadian clock control of singing and more importantly demonstrate a role of the pineal clock in breeding behaviors, leading to a compromised reproductive performance in diurnal zebra finches.

Circannual cycles and photoperiodism

Chapter

Jan 2022

Birds have evolved in an ever-changing world in which seasonal changes impose abiotic and biotic factors in a rhythmic fashion, predictably creating both beneficial and deleterious selective pressures. As a result, birds, like most free-living organisms, have adapted circannual biological clocks to maximize their fitness, coordinating complex annual phenologies of reproduction, molt, migration, and metabolism. At least some of the annual cyclicity in birds is due to the expression of endogenous circannual oscillators, which are revealed in laboratory conditions as rhythms with periods of approximately but not exactly one year. These circannual rhythms are entrained to 365 days by the presentation changing durations of the light cycle or photoperiod. Integrally related to entrainment of circannual cycles is the photoperiodic control of annual cycles. The mechanisms by which both circannual rhythms and photoperiodic time measurement are generated have been studied extensively. Specialized photoreceptors residing in multiple loci in the brain are responsible for entrainment and photoperiodic induction of reproduction, molt, migration, birdsong, and other processes, and structures associated with circadian organization have also been implicated. While the mechanisms of circannual rhythms are not known, molecular mechanisms underlying photoperiodic time measurement and annual cycles of reproduction involve circadian clocks in the hypothalamus and pineal gland, involving the expression of circadian clock genes, and the regulation of thyroid-mediated cellular processes. These mechanisms are compared and contrasted with those underlying annual cycles in mammals and fish.

Circadian rhythms

Chapter

Jan 2022

Birds have evolved in a rhythmic environment in which the daily rotation of the Earth imposes daily changes in illumination, temperature, magnetic field, barometric pressure and other abiotic factors. This fact induces daily changes in biotic aspects of the environment as well, including the presence of predators, prey, parasites, food and mates. Thus, birds, as do most free-living organisms, have evolved an endogenous biological timing system, or biological clock, to both predict environmental changes and temporally coordinate multiple physiological processes. This circadian system comprises internal oscillators that are capable of generating rhythms of molecular, physiological and behavioral processes with a period of approximately (circa) 24 hrs (dian) in birds maintained under constant environmental conditions such as constant darkness of constant dim light, which are entrained to the 24-hr period via specialized photoreceptive element in the brain. The circadian system itself is comprised of at least 3 sets of circadian pacemakers residing in the lateral eyes, the hypothalamic suprachiasmatic nuclei and the pineal gland, which together integrate overt circadian rhythms. The role of the pineal gland in many birds, particularly in passerine birds, is an important feature of circadian organization through its daily and circadian biosynthesis of melatonin. Melatonin’s sites and mechanisms of action are discussed as well as the molecular mechanisms by which circadian rhythms are generated.

Evidence That Artificial Light at Night Induces Structure-Specific Changes in Brain Plasticity in a Diurnal Bird

Article

Full-text available

Jul 2021

We recently reported that artificial light at night (ALAN), at ecologically relevant intensities (1.5, 5 lux), increases cell proliferation in the ventricular zone and recruitment of new neurons in several forebrain regions of female zebra finches (Taeniopygia guttata), along with a decrease of total neuronal densities in some of these regions (indicating possible neuronal death). In the present study, we exposed male zebra finches to the same ALAN intensities, treated them with 5′-bromo-2′-deoxyuridine, quantified cell proliferation and neuronal recruitment in several forebrain regions, and compared them to controls that were kept under dark nights. ALAN increased cell proliferation in the ventricular zone, similar to our previous findings in females. We also found, for the first time, that ALAN increased new neuronal recruitment in HVC and Area X, which are part of the song system in the brain and are male-specific. In other brain regions, such as the medial striatum, nidopallium caudale, and hippocampus, we recorded an increased neuronal recruitment only in the medial striatum (unlike our previous findings in females), and relative to the controls this increase was less prominent than in females. Moreover, the effect of ALAN duration on total neuronal densities in the studied regions varied between the sexes, supporting the suggestion that males are more resilient to ALAN than females. Suppression of nocturnal melatonin levels after ALAN exhibited a light intensity-dependent decrease in males in contrast to females, another indication that males might be less affected by ALAN. Taken together, our study emphasizes the importance of studying both sexes when considering ALAN effects on brain plasticity.

Seasonal Reproduction in Vertebrates: Melatonin Synthesis, Binding, and Functionality Using Tinbergen's Four Questions

Article

Full-text available

Mar 2018
MOLECULES

One of the many functions of melatonin in vertebrates is seasonal reproductive timing. Longer nights in winter correspond to an extended duration of melatonin secretion. The purpose of this review is to discuss melatonin synthesis, receptor subtypes, and function in the context of seasonality across vertebrates. We conclude with Tinbergen's Four Questions to create a comparative framework for future melatonin research in the context of seasonal reproduction.

Seasonal Reproduction in Vertebrates: Melatonin Synthesis, Binding, and Functionality Using Tinbergen’s Four Questions

Article

Full-text available

Mar 2018
MOLECULES

GABAA Receptor-Mediated Neurotransmission in the Suprachiasmatic Nucleus

Article

Sep 2015

GABAergic neurotransmission is a fundamental component of the suprachiasmatic nucleus (SCN) neural network, and virtually all SCN neurons communicate using GABA as a neurotransmitter. GABAergic neurotransmission plays a critical role in light-induced phase shifts, synchronization of the dorsal and ventral SCN, and, although controversial, synchronization of the circadian phase of individual SCN neurons. The circadian clock regulates the strength of GABAa receptor- mediated neurotransmission although the signaling mechanisms mediating this regulation are not known. GABA released from axon terminals acts on synaptic GABAA receptors producing postsynaptic currents that have a rapid onset and offset and desensitize in the continued presence of GABA. In the SCN, the postsynaptic GABAA receptor-mediated currents may be excitatory or inhibitory depending on the time of day. Once released GABA is removed from the synaptic cleft by specific sodium-chloride-dependent transporters (GAT). Some GABA can diffuse out of the synaptic cleft and act on extrasynaptic GABAa receptors. These extrasynaptic GABAa receptors have high affinity for GABA and show little or no desensitization. They mediate a –tonic— GABAa current that could modulate the input-output characteristics of individual SCN neurons. While significant scientific questions remain about the roles of GABAergic neurotransmission in the circadian timing signals, recent findings have yielded important advances in our understanding of GABAergic neurotransmission in the SCN.

Circannual Cycles and Photoperiodism

Chapter

Dec 2015

Annual cycles of exposure of the northern and southern hemispheres to solar irradiation due to the Earth's axis and the asymmetric revolution of the Earth around the sun results in dramatic changes in the environment in temperate and circumpolar regions, called "seasons." Seasons vary in the length of photoperiod, ambient temperature, and precipitation as well as changes in biotic environmental factors, such as food and competition. Birds exhibit profound annual cycles in their phenology due to their complex life cycles and heavy investment on rearing of young, resulting in annual cycles in courtship, reproduction, migration, molt, and other aspects of their biology that are strictly regulated by endogenous circannual clocks, synchronized by the length of the photoperiod and other factors. Tropical zone birds also exhibit annual cycles according to their seasons, but the mechanisms by which these are regulated are unknown. The mechanisms by which temperate zone birds detect changes in photoperiod include extraretinal photoreceptors residing in the preoptic area, lateral septum, and tuberal hypothalamus. The mechanisms by which birds measure photoperiodic time depend upon the physiological process being measured as well as the species of bird. Annual cycles of reproduction appear to be independent of pineal melatonin, in sharp contrast to the situation in mammals. Instead, photoreceptors within the tuberal hypothalamus itself and possibly preoptic area entrain a circadian clock within this area of the brain and induce transcriptional changes downstream to effect hypophysial outflow of gonadotropins and reproductive recrudescence. In contrast, annual changes in structures associated with bird song appear to be regulated by pineal melatonin, at least in part. Thus, annual cycles in birds are regulated by a complex integration of diverse photoreceptors and oscillators. This is an area ripe for future molecular and physiological analyses.

Kidney-Specific Reduction of Oxidative Phosphorylation Genes Derived from Spontaneously Hypertensive Rat

Article

Full-text available

Aug 2015
PLOS ONE

Mitochondrial (Mt) dysfunction contributes to the pathophysiology of renal function and promotes cardiovascular disease such as hypertension. We hypothesize that renal Mt-genes derived from female spontaneously hypertensive rats (SHR) that exhibit hypertension have reduced expression specific to kidney cortex. After breeding a female Okamoto-Aoki SHR (SAP = 188mmHg) with Brown Norway (BN) males (SAP = 100 and 104 mmHg), hypertensive female progeny were backcrossed with founder BN for 5 consecutive generations in order to maintain the SHR mitochondrial genome in offspring that contain over increasing BN nuclear genome. Mt-protein coding genes (13 total) and nuclear transcription factors mediating Mt-gene transcription were evaluated in kidney, heart and liver of normotensive (NT: n = 20) vs. hypertensive (HT: n = 20) BN/SHR-mtSHR using quantitative real-time PCR. Kidney cortex, but not liver or heart Mt-gene expression was decreased ~2-5 fold in 12 of 13 protein encoding genes of HT BN/SHR-mtSHR. Kidney cortex but not liver mRNA expression of the nuclear transcription factors Tfam, NRF1, NRF2 and Pgc1alpha were also decreased in HT BN/SHR-mtSHR. Kidney cortical tissue of HT BN/SHR-mtSHR exhibited lower cytochrome oxidase histochemical staining, indicating a reduction in renal oxidative phosphorylation but not in liver or heart. These results support the hypothesis that renal cortex of rats with SHR mitochondrial genome has specifically altered renal expression of genes encoding mitochondrial proteins. This kidney-specific coordinated reduction of mitochondrial and nuclear oxidative metabolism genes may be associated with heritable hypertension in SHR.

The Effects of Melatonin on Brain Arginine Vasotocin: Relationship to Sex and Seasonal Differences in MT1 in Green Treefrogs (Hyla cinerea)

Article

May 2015
J NEUROENDOCRINOL

The neuroendocrine mechanisms by which animals synchronise their physiological state with environmental cues are vital to timing life-history events appropriately. One important endocrine transducer of environmental cues in vertebrates is the pineal hormone melatonin, secretion of which is directly sensitive to photoperiod and temperature. Melatonin modulates arginine vasotocin immunoreactive (ir) cell number in the brain of green treefrogs (Hyla cinerea) during the summer breeding season, and this modulation is sexually dimorphic. In this study, we asked if melatonin's influence on vasotocin varies seasonally. We show that treatment of nonreproductive male green treefrogs with melatonin-filled silastic implants for 4 wks during the winter does not alter vasotocin-ir cell number in any brain region (i.e., nucleus accumbens, amygdala, preoptic area, suprachiasmatic nucleus, or ventral hypothalamus). Taken together, these results suggest that melatonin's influence on AVT is associated with sex and seasonal variation in melatonin receptor expression. We tested this hypothesis by using immunohistochemistry to characterize the distribution of melatonin type 1a receptor (MT1) in the brain of reproductive and nonreproductive male and female frogs. We quantified MT1-ir cell number in regions known to contain AVT cell populations. Reproductive males had significantly more MT1-ir cells than nonreproductive males in all brain regions, including the combined nucleus accumbens, diagonal band of Broca and septum, striatum, amygdala, combined preoptic area and suprachiasmatic nucleus, and ventral hypothalamus. In the accumbens region, where melatonin's effect on AVT is known to be sexually dimorphic, males had significantly more MT1-ir cells than females during the summer breeding season. Based on these findings, we suggest that MT1 plays a role in mediating the interactions between melatonin and vasotocin that regulate seasonal and sexually dimorphic changes in sociosexual behaviour. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.

Reversing song behavior phenotype: Testosterone driven induction of singing and measures of song quality in adult male and female canaries (Serinus canaria)

Article

Sep 2014

In songbirds, such as canaries (Serinus canaria), the song control circuit has been shown to undergo a remarkable change in morphology in response to exogenous testosterone (T). It is also well established that HVC, a telencephalic nucleus involved in song production, is significantly larger in males than in females. T regulates seasonal changes in HVC volume in males and exposure to exogenous T in adult females increases HVC volume and singing activity such that their song becomes more male-like in frequency and structure. However, whether there are sex differences in the ability of T to modulate changes in the song system and song behavior has not been investigated in canaries. In this study, we compared the effects of increasing doses of T on singing and song control nuclei volumes in adult male and female American Singer canaries exposed to identical environmental conditions. Males were castrated and all birds were placed on short days (8L:16D) for 8weeks. Males and females were implanted either with a 2, 6 or 12mm long Silastic™ implant filled with crystalline T or an empty 12mm implant as control. Birds were then housed individually in sound attenuated chambers. Brains were collected from six birds from each group after 1week or 3weeks of treatment. Testosterone was not equally effective in increasing singing activity in both males and females. Changes in song quality and occurrence rate took place after a shorter latency in males than in females however, females did undergo marked changes in a number of measures of song behavior if given sufficient time. Males responded with an increase in HVC volume at all three doses. In females, T-induced changes in HVC volume only had limited amplitude and these volumes never reached male-typical levels a suggesting that there are sex differences in the neural substrate that responds to T.

Melatonin: An internal signal for daily and seasonal timing

Article

Full-text available

May 2014

Melatonin is secreted only during night, irrespective of the habitat of an organism and the site of its synthesis and secretion, and hence known as "darkness hormone". Elevated melatonin levels reflect the nighttime. In vertebrates, the main site of melatonin production is the pineal gland. Species in which melatonin is also secreted from sources other than the pineal, as in some birds, relative contributions of different melatonin producing tissues to the blood melatonin level can vary from species to species. Melatonin acts through its receptors, which are members of the G protein-coupled (GPCR) superfamily. Three melatonin receptors subtypes MT1 (mella), MT2 (mellb), and MT3 (mellc) have been identified in different brain areas and other body organs of vertebrates. Melatonin synthesis and secretion are circadianly rhythmic. Changes and differences in specific features of melatonin signal can vary among species, and under a variety of natural environmental conditions. Two major physiological roles of melatonin are established in vertebrates. First, melatonin is involved in the circadian system regulated behavioural and physiological functions. Second, it is critical for the photoperiodic system. Besides, melatonin has been implicated in various ways both directly and indirectly to human health, including jet lag, sleep, immune system and cancer.

Thyroid hormone and seasonal regulation of reproduction

Article

May 2013
FRONT NEUROENDOCRIN

Takashi Yoshimura

Organisms living outside the tropics use changes in photoperiod to adapt to seasonal changes in the environment. Several models have contributed to an understanding of this mechanism at the molecular and endocrine levels. Subtropical birds are excellent models for the study of these mechanisms because of their rapid and dramatic response to changes in photoperiod. Studies of birds have demonstrated that light is perceived by a deep brain photoreceptor and long day-induced thyrotropin (TSH) from the pars tuberalis (PT) of the pituitary gland causes local thyroid hormone activation within the mediobasal hypothalamus (MBH). The locally generated bioactive thyroid hormone, T3, regulates seasonal gonadotropin-releasing hormone (GnRH) secretion, and hence gonadotropin secretion. In mammals, the eyes are the only photoreceptor involved in photoperiodic time perception and nocturnal melatonin secretion provides an endocrine signal of photoperiod to the PT to regulate TSH. Here, I review the current understanding of the hypothalamic mechanisms controlling seasonal reproduction in mammals and birds.

Season- and context-dependent sex differences in melatonin receptor activity in a forebrain song control nucleus

Article

Nov 2012
HORM BEHAV

There are dense populations of melatonin receptors in large areas of the songbird brain, in particular in the visual system and the song control system. Melatonin has therefore been implicated in neuroplasticity of the song control system. Previously we demonstrated large changes in activity of melatonin receptor in Area X, a forebrain song control nucleus involved in song learning and production. In a laboratory environment, melatonin receptor activity was down-regulated in male and female European starlings during photostimulation (a simulated breeding season). The functional significance of this large change in Area X is unclear, so we sought to elucidate it by tracking melatonin receptor activity in male and female starlings housed in a semi-natural environment and permitted to breed. Males and females all exhibited high melatonin receptor activity in Area X during short days at the start of the breeding season, and maintained this high activity during photostimulation until females laid eggs. At this point the females down-regulated melatonin receptor activity in Area X, whereas the males maintained high activity until later on in the breeding season. Mel 1b was the most abundantly expressed of the 3 known melatonin receptor subytpes in Area X. There was a positive correlation between the expression of Mel 1b and the transcription factor ZENK, indicating that high melatonin receptor expression is correlated with high activity of Area X. Overall, we observed a gradual termination of activity in Area X as the breeding season progressed, but the timing of termination was different between the sexes.

The Bird of Time: Cognition and the Avian Biological Clock

Article

Full-text available

Mar 2012

Avian behavior and physiology are embedded in time at many levels of biological organization. Biological clock function in birds is critical for sleep/wake cycles, but may also regulate the acquisition of place memory, learning of song from tutors, social integration, and time-compensated navigation. This relationship has two major implications. First, mechanisms of the circadian clock should be linked in some way to the mechanisms of all these behaviors. How is not yet clear, and evidence that the central clock has effects is piecemeal. Second, selection acting on characters that are linked to the circadian clock should influence aspects of the clock mechanism itself. Little evidence exists for this in birds, but there have been few attempts to assess this idea. At its core, the avian circadian clock is a multi-oscillator system comprising the pineal gland, the retinae, and the avian homologs of the suprachiasmatic nuclei, whose mutual interactions ensure coordinated physiological functions, which are in turn synchronized to ambient light cycles (LD) via encephalic, pineal, and retinal photoreceptors. At the molecular level, avian biological clocks comprise a genetic network of "positive elements" clock and bmal1 whose interactions with the "negative elements" period 2 (per2), period 3 (per3), and the cryptochromes form an oscillatory feedback loop that circumnavigates the 24 h of the day. We assess the possibilities for dual integration of the clock with time-dependent cognitive processes. Closer examination of the molecular, physiological, and behavioral elements of the circadian system would place birds at a very interesting fulcrum in the neurobiology of time in learning, memory, and navigation.

Circadian Regulation of Bird Song, Call, and Locomotor Behavior by Pineal Melatonin in the Zebra Finch

Article

Full-text available

Apr 2012
J BIOL RHYTHM

As both a photoreceptor and pacemaker in the avian circadian clock system, the pineal gland is crucial for maintaining and synchronizing overt circadian rhythms in processes such as locomotor activity and body temperature through its circadian secretion of the pineal hormone melatonin. In addition to receptor presence in circadian and visual system structures, high-affinity melatonin binding and receptor mRNA are present in the song control system of male oscine passeriform birds. The present study explores the role of pineal melatonin in circadian organization of singing and calling behavior in comparison to locomotor activity under different lighting conditions. Similar to locomotor activity, both singing and calling behavior were regulated on a circadian basis by the central clock system through pineal melatonin, since these behaviors free-ran with a circadian period and since pinealectomy abolished them in constant environmental conditions. Further, rhythmic melatonin administration restored their rhythmicity. However, the rates by which these behaviors became arrhythmic and the rates of their entrainment to rhythmic melatonin administration differed among locomotor activity, singing and calling under constant dim light and constant bright light. Overall, the study demonstrates a role for pineal melatonin in regulating circadian oscillations of avian vocalizations in addition to locomotor activity. It is suggested that these behaviors might be controlled by separable circadian clockworks and that pineal melatonin entrains them all through a circadian clock.

Anatomy of a songbird basal ganglia circuit essential for vocal learning and plasticity

Article

Mar 2010

Vocal learning in songbirds requires an anatomically discrete and functionally dedicated circuit called the anterior forebrain pathway (AFP). The AFP is homologous to cortico-basal ganglia-thalamo-cortical loops in mammals. The basal ganglia portion of this pathway, Area X, shares many features characteristic of the mammalian striatum and pallidum, including cell types and connectivity. The AFP also deviates from mammalian basal ganglia circuits in fundamental ways. In addition, the microcircuitry, role of neuromodulators, and function of Area X are still unclear. Elucidating the mechanisms by which both mammalian-like and unique features of the AFP contribute to vocal learning may help lead to a broad understanding of the sensorimotor functions of basal ganglia circuits.

Seasonal neuroplasticity of the song control system in tropical, flexibly, and opportunistically breeding birds

Article

Feb 2009
GEN COMP ENDOCR

The avian song control system is one of the primary models used to study neuroplasticity and neurogenesis in the adult vertebrate brain. A great deal of progress has been made in understanding the mechanisms controlling seasonal neuroplasticity of the song control system. However, relatively little work has been done to identify how prevalent this phenomenon is and if a diversity of environmental cues can regulate it. Photoperiod is the primary environmental cue used by mid- to high-latitude seasonally breeding birds to time growth of the song control system but many birds display flexible or opportunistic breeding patterns that are less reliant on photoperiodic cues. In addition, approximately 75% of birds are tropical and in only one such species has neuroplasticity of the song control system been studied. Our goal is to outline some of what is known and expand on the ways that studying tropical, flexibly, and opportunistically breeding birds can advance our understanding of plasticity in the song bird brain.

Testosterone and opioids interact to regulate feeding in a male migratory songbird

Article

Oct 1992

Pierre Deviche

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.

Circuits, hormones, and learning: Vocal behavior in songbirds

Article

Dec 1997

Species-typical vocal patterns subserve species identification and communication for individual organisms. Only a few groups of organisms learn the sounds used for vocal communication, including songbirds, humans, and cetaceans. Vocal learning in songbirds has come to serve as a model system for the study of brain-behavior relationships and neural mechanisms of learning and memory. Songbirds learn specific vocal patterns during a sensitive period of development via a complex assortment of neurobehavioral mechanisms. In many species of songbirds, the production of vocal behavior by adult males is used to defend territories and attract females, and both males and females must perceive vocal patterns and respond to them. In both juveniles and adults, specific types of auditory experience are necessary for initial song learning as well as the maintenance of stable song patterns. External sources of experience such as acoustic cues must be integrated with internal regulatory factors such as hormones, neurotransmitters, and cytokines for vocal patterns to be learned and produced. Thus, vocal behavior in songbirds is a culturally acquired trait that is regulated by multiple intrinsic as well as extrinsic factors. Here, we focus on functional relationships between circuitry and behavior in male songbirds. In that context, we consider in particular the influence of sex hormones on vocal behavior and its underlying circuitry, as well as the regulatory and functional mechanisms suggested by morphologic changes in the neural substrate for song control. We describe new data on the architecture of the song system that suggests strong similarities between the songbird vocal control system and neural circuits for memory, cognition, and use-dependent plasticity in the mammalian brain.

Profile: Multi-component signals in ant communication

Chapter

Nov 2010

Bert Hölldobler

Humans live in large and extensive societies and spend much of their time interacting socially. Likewise, most other animals also interact socially. Social behaviour is of constant fascination to biologists and psychologists of many disciplines, from behavioural ecology to comparative biology and sociobiology. The two major approaches used to study social behaviour involve either the mechanism of behaviour - where it has come from and how it has evolved, or the function of the behaviour studied. With guest articles from leaders in the field, theoretical foundations along with recent advances are presented to give a truly multidisciplinary overview of social behaviour, for advanced undergraduate and graduate students. Topics include aggression, communication, group living, sexual behaviour and co-operative breeding. With examples ranging from bacteria to social mammals and humans, a variety of research tools are used, including candidate gene approaches, quantitative genetics, neuro-endocrine studies, cost-benefit and phylogenetic analyses and evolutionary game theory.

Sex differences in seasonal brain plasticity and the neuroendocrine regulation of vocal behavior in songbirds

Article

Jun 2022
HORM BEHAV

Birdsong is controlled in part by a discrete network of interconnected brain nuclei regulated in turn by steroid hormones and environmental stimuli. This complex interaction results in neural changes that occur seasonally as the environment varies (e.g., photoperiod, food/water availability, etc.). Variation in environment, vocal behavior, and neuroendocrine control has been primarily studied in male songbirds in both laboratory studies of captive birds and field studies of wild caught birds. The bias toward studying seasonality in the neuroendocrine regulation of song in male birds comes from a historic focus on sexually selected male behaviors. In fact, given that male song is often loud and accompanied by somewhat extravagant courtship behaviors, female song has long been overlooked. To compound this bias, the primary model songbird species for studies in the lab, zebra finches (Taeniopygia guttata) and canaries (Serinus canaria), exhibit little or no female song. Therefore, understanding the degree of variation and neuroendocrine control of seasonality in female songbirds is a major gap in our knowledge. In this review, we discuss the importance of studying sex differences in seasonal plasticity and the song control system. Specifically, we discuss sex differences in 1) the neuroanatomy of the song control system, 2) the distribution of receptors for androgens and estrogens and 3) the seasonal neuroplasticity of the hypothalamo-pituitary-gonadal axis as well as in the neural and cellular mechanisms mediating song system changes. We also discuss how these neuroendocrine mechanisms drive sex differences in seasonal behavior. Finally, we highlight specific gaps in our knowledge and suggest experiments critical for filling these gaps.

“Singing” Fish Rely on Circadian Rhythm and Melatonin for the Timing of Nocturnal Courtship Vocalization

Article

Oct 2016
CURR BIOL

The patterning of social acoustic signaling at multiple timescales, from day-night rhythms to acoustic temporal properties, enhances sender-receiver coupling and reproductive success [1, 2, 3, 4, 5, 6, 7, 8]. In diurnal birds, the nocturnal production of melatonin, considered the major vertebrate timekeeping hormone [9, 10], suppresses vocal activity but increases song syllable duration over circadian and millisecond timescales, respectively [11, 12]. Comparable studies are lacking for nocturnal vertebrates, including many teleost fish species that are also highly vocal during periods of reproduction [4, 13, 14, 15, 16, 17, 18, 19, 20]. Utilizing continuous sound recordings, light cycle manipulations, hormone implants, and in situ hybridization, we demonstrate in a nocturnally breeding teleost fish that (1) courtship vocalization exhibits an endogenous circadian rhythm under constant dark conditions that is suppressed under constant light, (2) exogenous delivery of a melatonin analog under inhibitory constant light conditions rescues courtship vocal activity as well as the duration of single calls, and (3) melatonin receptor 1b is highly expressed in evolutionarily conserved neuroendocrine and vocal-acoustic networks crucial for patterning reproductive and vocal behaviors in fishes and tetrapods. Our findings, together with those in birds, show melatonin’s remarkable versatility as a timing signal in distantly related lineages. It exerts opposing effects on vocalization in nocturnal versus diurnal species at the circadian timescale but comparable effects at the finer timescale of acoustic features. We propose that melatonin’s separable effects at different timescales depends on its actions within distinct neural networks that control circadian rhythms, reproduction, and vocalization, which may be selected upon over evolutionary time as dissociable modules to pattern and coordinate social behaviors.

Photoperiodic Regulation of Reproduction in Vertebrates

Article

Feb 2019

Organisms use changes in photoperiod for seasonal reproduction to maximize the survival of their offspring. Birds have sophisticated seasonal mechanisms and are therefore excellent models for studying these phenomena. Birds perceive light via deep-brain photoreceptors and long day–induced thyroid-stimulating hormone (TSH, thyrotropin) in the pars tuberalis of the pituitary gland (PT), which cause local thyroid hormone activation within the mediobasal hypothalamus. The local bioactive thyroid hormone controls seasonal gonadotropin-releasing hormone secretion and subsequent gonadotropin secretion. In mammals, the eyes are believed to be the only photoreceptor organ, and nocturnal melatonin secretion triggers an endocrine signal that communicates information about the photoperiod to the PT to regulate TSH. In contrast, in Salmonidae fish the input pathway to the neuroendocrine output pathway appears to be localized in the saccus vasculosus. Thus, comparative analysis is an effective way to uncover the universality and diversity of fundamental traits in various organisms. Expected final online publication date for the Annual Review of Animal Biosciences Volume 7 is February 15, 2019. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

A haphazard career

Article

Full-text available

Nov 2010

Ronald Noë

I was asked to explain why and how a Dutchman got to be a professor teaching animal behaviour in a French university. Someone must have thought that my story could provide some guidance for aspiring ethologists and behavioural ecologists. I am not so sure that my career path is one that should be followed, but perhaps someone can learn from my mistakes. I think I can now afford to write about them without much of a negative effect on my career. Not that I have bothered much about my ‘career’, but that is perhaps the core of my problem. I have never been good at preparing myself for the future, so after treading the mills of the Dutch educational system I found myself regularly confronted with steps in life that I should have prepared, if not better, then at least earlier. And so I ended up in a ‘cul de sac’. But let me start from the beginning. I can't tell you what kind of ‘—ist’ I am exactly at this point – primatologist, behavioural ecologist or evolutionary psychologist – but I went to the university to become an ethologist. The reason was simple: I liked animals a lot, and notably the furry ones. I definitely preferred seeing them alive, healthy and doing their own thing. I understood from books by the likes of Tinbergen, Lorenz, Wickler and Eibl-Eibesfeldt that ethologists did professionally what I liked to do anyway: watch animals behave.

Natural melatonin fluctuation and its minimally invasive simulation in the zebra finch

Article

Full-text available

Apr 2016

Melatonin is a key hormone in the regulation of circadian rhythms of vertebrates, including songbirds. Understanding diurnal melatonin fluctuations and being able to reverse or simulate natural melatonin levels are critical to investigating the influence of melatonin on various behaviors such as singing in birds. Here we give a detailed overview of natural fluctuations in plasma melatonin concentration throughout the night in the zebra finch. As shown in previous studies, we confirm that “lights off” initiates melatonin production at night in a natural situation. Notably, we find that melatonin levels return to daytime levels as early as two hours prior to the end of the dark-phase in some individuals and 30 min before “lights on” in all animals, suggesting that the presence of light in the morning is not essential for cessation of melatonin production in zebra finches. Thus, the duration of melatonin production seems not to be specified by the length of night and might therefore be less likely to directly couple circadian and annual rhythms. Additionally, we show that natural melatonin levels can be successfully simulated through a combination of light-treatment (daytime levels during subjective night) and the application of melatonin containing skin-cream (nighttime levels during subjective day). Moreover, natural levels and their fluctuation in the transition from day to night can be imitated, enabling the decoupling of the effects of melatonin, for example on neuronal activity, from sleep and circadian rhythmicity. Taken together, our high-resolution profile of natural melatonin levels and manipulation techniques open up new possibilities to answer various melatonin related questions in songbirds.

Genes and social behaviour: From gene to genome to 1000 genomes

Article

Nov 2010

Gene E. Robinson

Which comes first – passion for the scientific question or passion for the organism? For most biologists I think it's the former, but for me it was the latter. I became smitten with honey bees at the age of 18 and have never looked back. Once immersed in study, the question did come: how can a honey bee, with a brain the size of a grass seed, create a collective organisation in which all tasks are divided efficiently but flexibly among as many as 50 000 individuals? Honey bee division of labour is a spectacular example of social behaviour; trying to understand its mechanisms and evolution has motivated most of the research in my laboratory over the years and also has led periodically to rewarding expeditions into new scientific terrains. After starting with behavioural and endocrine analyses as a graduate student at Cornell University with Roger Morse, my postdoctoral studies with Robert Page at Ohio State University demonstrated for the first time heritable influences on division of labour (Robinson & Page 1988). Then mechanistic studies in my own lab at the University of Illinois revealed striking differences in brain chemistry and brain structure between bees performing different jobs, raising the possibility that these changes were orchestrated by changes in brain gene expression (Withers et al. 1993). To enhance our ability to discover insights into the mechanisms and evolution of this form of social behaviour, I decided in the mid 1990s to initiate a molecular component to our research programme.

Anonymous (and other) social experience and the evolution of cooperation by reciprocity

Article

Nov 2010

Michael Taborsky

Animals behave according to their previous social experience. This has been demonstrated in a wide range of species all across the animal kingdom (Rutte et al. 2006). Remarkably, this response to previous social interactions is not confined to experience with known individuals. It appears to be a much simpler trait than we might assume from our own intuition. If an animal fights with any conspecific, it will behave differently in future encounters, depending on whether it won or lost. These renowned winner and loser effects are among the most predictable traits in animal interactions (see Chapter 14). In humans, we term the psychological mechanism involved ‘self-confidence’. But, most interestingly, animals respond contingently upon social experience also in a sociopositive context. If they received help, they are more likely to help others as well, even if donors and receivers are completely unknown to each other. This generalised form of reciprocity has been demonstrated in humans and Norway rats so far (Bartlett & DeSteno 2006, Rutte & Taborsky 2007), but we assume it to be a general phenomenon, just like the ubiquitous winner and loser effects. In the early 1970s, after Hamilton's (1964) and Trivers' (1971) revelations on kin selection and reciprocity as key mechanisms of altruistic behaviour and advanced sociality, we were tempted to believe that the major riddles in this field had been solved. The vast literature that emerged on the evolutionary mechanisms of altruism and (eu)sociality since then, at both theoretical and empirical levels, proved us dead wrong.

Social behaviour and bird song from a neural and endocrine perspective

Article

Nov 2010

Overview Tinbergen (1963) proposed that in order to understand behaviour it is necessary to discover not only its adaptive function and phylogenetic history (now often referred to as ultimate causation) but also its development and physiology (proximate causation). In recent years there has been increasing appreciation of the importance of pursuing these four aims not only separately but also in an integrated manner that allows them to inform each other. Hormonal and neural mechanisms are best understood in an ecological and evolutionary context. An appreciation of how they work is essential both for understanding the ecology and evolution of behaviour, and for linking genes to behaviour. This chapter will discuss hormonal and neural bases of social behaviour, emphasising basic principles, recent trends and questions for the future, with a more extended discussion of bird song as a prime example of a social behaviour that has inspired a substantial body of integrative research. Special attention will be given to learned song and the songbird neural song system that underlies the learning, production and perception of song. As a neural system that is anatomically well defined, dedicated to an important category of social behaviour, and hormonally influenced, the song system is uniquely valuable for elucidating general principles of the mechanisms of social behaviour.

Avian Circadian Organization

Article

Sep 2015

Vincent M Cassone

In birds, biological clock function pervades all aspects ofbiology, controlling daily changes in sleep: wake, visual function, song, migratory patterns and orientation, as well as seasonal patterns of reproduction, song, and migration. The molecular bases for circadian clocks are highly conserved, and it is likely the avian molecular mechanisms are similar to those expressed in mammals, including humans. The central pacemakers in the avian pineal gland, retinae, and SCN dynamically interact to maintain stable phase relationships and then influence downstream rhythms through entrainment of peripheral oscillators in the brain controlling behavior and peripheral tissues. Birds represent an excellent model for the role played by biological clocks in human neurobiology; unlike most rodent models, they are diurnal, they exhibit cognitively complex social interactions, and their circadian clocks are more sensitive to the hormone melatonin than are those of nocturnal rodents.

Circadian Rhythms

Chapter

Full-text available

Dec 2015

Due to the daily rotation of the Earth on its axis, nearly all organisms are exposed to daily cycles of environmental factors, including the intensity and quality of light, temperature, and other abiotic or physical factors, as well as changes in biotic factors such as presence of predators, competitors, and food. Because of this, most organisms have evolved endogenous biological clocks that synchronize internal processes with external cycles and coordinate intrinsic processes. In birds, these biological clocks are particularly evident partly due to the fact that they are mostly diurnal and visible and also to the fact that these organisms strictly time all aspects of their lives. The biological clocks of birds comprise multiple circadian oscillators whose complex interactions are critical for self-sustained rhythmicity. These include the pineal gland, which influences the system through the secretion of the hormone melatonin, the retinae, and the hypothalamic suprachiasmatic nuclei. This circadian system is, in turn, synchronized or entrained to light-dark cycles via retinal and extraretinal photoreceptors in the pineal gland, lateral septum, preoptic area, and tuberal hypothalamus. This multi-oscillatory system synchronizes multiple behavioral and physiological processes that include brain metabolism, body temperature, endocrine processes, sleep-wake cycles, bird song, migration, and so on. The molecular mechanisms underlying these rhythms are currently being elucidated and appear to contain homologous transcriptional/translational feedback loops involving "clock genes" shared by all animals. Future prospects of integrating molecular with physiological and behavioral research depend on the development of transgenic technologies.

The Pineal Gland, Circadian Rhythms, and Photoperiodism

Chapter

Dec 2000

Sex steroid-independent effects of photostimulation on the song-control system of white-throated sparrows (Zonotrichia albicollis)

Article

Aug 2014
GEN COMP ENDOCR

Brain nuclei within the song-control system of songbirds are seasonally plastic during adulthood. These nuclei are larger in birds exposed to long, spring-like days than short, winter-like days. There is overwhelming evidence that this effect is mediated by testosterone (T). However, castration studies have also demonstrated that photostimulation has gonad-independent effects on song-control system plasticity, but these studies rarely control for extra-gonadal sources of T. In this study, we used anti-androgen and anti-estrogen treatments in combination with castration to determine the sex steroid-independent effects of photostimulation on HVC size and doublecortin immunoreactivity in white-throated sparrows (Zonotrichia albicollis). Birds were kept on short days or photostimulated for one month. Photostimulated birds were intact, castrated and treated with anti-androgens and anti-estrogens, or castrated and treated with T. HVC volumes of photostimulated birds were significantly larger than short-day birds. HVC volume of castrated birds given anti-androgens/-estrogens was significantly larger than short-day birds, indicating a sex steroid-independent effect of photostimulation. Similar results were observed for RA. The number of migrating neurons (immunoreactive for doublecortin) in HVC did not differ between treatment groups. Our data support the view that photostimulation alone can drive song-control system nuclei growth, and that concurrent exposure to T potentiates this growth. Moreover, these effects do not appear dependent on modulation of neuron migration.

Unraveling the enigma: The role of melatonin in seasonal processes in birds

Article

Apr 2001
MICROSC RES TECHNIQ

George Ed Bentley

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.

Molecular Neurobiology of Bird Song

Chapter

Dec 2006

David Clayton

Songbirds (oscines of Order Passeriformes) are emerging as a major focus of research in neurobiology. This review considers five broad research topics that are proving amenable to molecular biological analysis in songbirds: (1) molecular anatomy of a functioning neural system (the song system); (2) regulation of learning and memory formation; (3) brain circuit development, including roles for sex steroids and ongoing neurogenesis; (4) integration of social and environmental signals; (5) species diversity and evolution. Results from ∼400 references are considered, illustrating the enormous breadth and vitality of bird song molecular neurobiology.

The Neuroendocrinology and Neurochemistry of Birdsong

Chapter

Dec 2006

Birdsong is a complex learned motor skill that is used in the context of territory defense and mate choice. Songbirds have evolved a specialized neural circuit that controls the learning, production, and perception of song. Studies of the hormonal regulation of neurotransmitter systems in this specialized circuit provide an opportunity for neuroscientists to investigate the cellular neurochemistry of complex behaviors. In this review, we review the hormonal regulation of seasonal neuroplasticity in this circuit with special emphasis on the action of androgens including their estrogenic and androgenic metabolites. One theme that emerges is that androgens can induce seasonal changes in the morphology of the song circuit but that the ability of testosterone to be metabolized into androgenic or estrogenic metabolites also changes seasonally. The basic chemical neuroanatomy of the song system is reviewed and possible sites for the modulation of these transmitter systems by androgens are identified.

Melatonin Receptor Expression in the Zebra Finch Brain and Peripheral Tissues

Article

Mar 2012
CHRONOBIOL INT

The circadian endocrine hormone melatonin plays a significant role in many physiological processes, such as modulating the sleep/wake cycle and oxidative stress. Melatonin is synthesized and secreted during the night by the pineal gland and released into the circulatory system. It binds to numerous membrane, cytosolic, and nuclear receptors in the brain and peripheral organs. Three G-protein-linked membrane receptors (Mel1A, Mel1B, and Mel1C) have been identified in numerous species. Considering the importance of this hormone and its receptors, this study looks at the location and rhythmicity of these three avian melatonin receptors using reverse transcriptase-polymerase chain reaction (RT-PCR) mRNA analysis techniques. This study shows successful partial cloning of the three receptors, and gene expression analysis reveals significant rhythms of the Mel1A receptor in the cerebellum, diencephalon, tectum opticum, telencephalon, and retina. Significant rhythms were found in the diencephalon, pineal gland, retina, tectum opticum, and cerebellum of the Mel1B receptor, whereas Mel1C appeared not to be rhythmically expressed in brain tissues studied. Mel1A, Mel1B, and Mel1C receptor mRNAs were also present in peripheral tissues, showing tissue-specific expression patterns.

Seasonal and hormonal modulation of neurotransmitter systems in the song control circuit

Article

Sep 2009

In the years following the discovery of the song system, it was realized that this specialized circuit controlling learned vocalizations in songbirds (a) constitutes a specific target for sex steroid hormone action and expresses androgen and (for some nuclei) estrogen receptors, (b) exhibits a chemical neuroanatomical pattern consisting in a differential expression of various neuropeptides and neurotransmitters receptors as compared to surrounding structures and (c) shows pronounced seasonal variations in volume and physiology based, at least in the case of HVC, on a seasonal change in neuron recruitment and survival. During the past 30 years numerous studies have investigated how seasonal changes, transduced largely but not exclusively through changes in sex steroid concentrations, affect singing frequency and quality by modulating the structure and activity of the song control circuit. These studies showed that testosterone or its metabolite estradiol, control seasonal variation in singing quality by a direct action on song control nuclei. These studies also gave rise to the hypothesis that the probability of song production in response to a given stimulus (i.e. its motivation) is controlled through effects on the medial preoptic area and on catecholaminergic cell groups that project to song control nuclei. Selective pharmacological manipulations confirmed that the noradrenergic system indeed plays a role in the control of singing behavior. More experimental work is, however, needed to identify specific genes related to neurotransmission that are regulated by steroids in functionally defined brain areas to enhance different aspects of song behavior.

Distribution of 2-[I-125]iodomelatonin Binding in the Brain of Mexican Free-Tailed Bats (Tadarida brasiliensis)

Article

Full-text available

Mar 2009
BRAIN BEHAV EVOLUT

The neurohormone melatonin is an important signal for both time of day and time of year in many seasonally breeding animals. High densities of melatonin receptors have been found in the suprachiasmatic nucleus, median eminence, and the pituitary gland in almost all mammals investigated so far, and lower densities of melatonin receptors have also been localized to other brain regions varying in a species-specific fashion. Because species-specific differences in receptor distributions have been correlated with differences in behavior and ecology, a comparative study of how melatonin receptors are distributed in vertebrate brains can be useful to the understanding of the functional organization of neural circuits controlling daily and seasonal behaviors. In this study, we localized and characterized melatonin binding sites in the brain of the Mexican free-tailed bat (Tadarida brasiliensis) using in vitro autoradiography with 2-[(125)I]iodomelatonin. Tadarida brasiliensis is a nocturnal insectivorous mammal that seasonally migrates, reproduces once a year, and exhibits documented sexual dimorphisms in seasonal reproductive behaviors, most notably in courtship vocalizations. Prominent 2-[(125)I]iodomelatonin binding was found in the median eminence, suprachiasmatic nuclei, and hippocampus, similar to that observed in other mammals. High densities of binding were also localized to structures of the basal ganglia, including the caudate nucleus, putamen, and nucleus accumbens, a feature commonly observed in songbirds but not in mammals. Saturation analysis indicated that the observed binding sites had an affinity for melatonin typical of the binding properties for the Mel(1a) receptor subtype. We conclude that melatonin receptor distributions in the Mexican free-tailed bat brain appear to show similarities with the reproductive and circadian systems of other mammals and the basal ganglia of songbirds.

Response of the Reproductive Organs of the Japanese Quail to Pinealectomy and Melatonin Injections

Article

Full-text available

Mar 1967

IN recent years research on mammalian pineal physiology has been active. Melatonin elaborated by the pineal gland inhibits gonadal activity in rats (Wurtman et al., 1963a; Chu et al., 1964). The synthesis of melatonin in the rat pineal is controlled through environmental photoperioids, viz. it is accelerated by darkness and inhibited by light (Wurtman et al., 1963b). These diurnal changes in melatonin content of the pineal have been called the melatonin rhythm (Quay, 1964) Serotonin, the precursor of melatonin, also undergoes a marked diurnal change in the pineal (Quay, 1963), but there is no strict reciprocal correlation between the two rhythms. When rats were placed in continuous darkness or blinded, the melatonin rhythm was soon abolished, but the serotonin rhythm was maintained for more than 2 weeks, suggesting that the melatonin rhythm was under an exogenous control, whereas, serotonin rhythm was under an endogenous control (Snyder et al., 1964). Melatonin . . .

Birth of Projection Neurons in Adult Avian Brain May Be Related to Perceptual or Motor Learning

Article

Full-text available

Oct 1990

Projection neurons that form part of the motor pathway for song control continue to be produced and to replace older projection neurons in adult canaries and zebra finches. This is shown by combining [3H]thymidine, a cell birth marker, and fluorogold, a retrogradely transported tracer of neuronal connectivity. Species and seasonal comparisons suggest that this process is related to the acquisition of perceptual or motor memories. The ability of an adult brain to produce and replace projection neurons should influence our thinking on brain repair.

Seasonal changes in avian song nuclei without seasonal changes in song repertoire

Article

Full-text available

Jun 1991

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.

A Role of Melatonin in the Initial Stage of Photoperiodism in the Japanese Quail1

Article

Full-text available

Jun 1989

To estimate whether melatonin is involved in gonadal activity in the male quail, the dynamics of plasma melatonin at an early stage of the photoperiodic response were investigated. Nocturnal levels of melatonin were manipulated by treatment with anti-melatonin (anti-M). By means of 4 additional hours of photic stimulation of the brain (provided by a red light-emitting diode inserted through the back of the head) after the environmental lights (8L:16D, lights-on, 1000 h) were turned off, the elevation of levels of melatonin after lights-off was significantly suppressed on Days 1 and 2 (p less than 0.01); after 5 days of brain-lighting, gonadal growth first became noticeable. However, 4 h of brain-lighting before lights-on elicited no change in levels of melatonin or in gonadal growth. The injections of anti-M just before lights-off (at 1800 h) for the first 3 days caused significant gonadal growth (p less than 0.01), whereas injections at 2200, 0200, or 0600 h were without effect. In addition, 4 h of brain-lighting before lights-on became gonadostimulatory (p less than 0.01) when it was accompanied by the injection of anti-M at 1800 h, but remained without effect when anti-M was injected at 0600 h. These results suggest that melatonin is involved in the initial stage of photoperiodism in birds, and the timing of suppression of the elevation of melatonin levels is critical in gonadal development.

Is the avian circadian system a neuroendocrine loop? J

Article

Full-text available

Dec 1984

Avian circadian organization is a result of a complex interaction of photoreceptive and oscillatory components. The known components include the pineal gland, the lateral eyes, the suprachiasmatic nuclei (SCN), and extraocular brain photoreceptors. The pathways by which these components integrate circadian rhythmicity suggest a neuroendocrine loop in which the SCN inhibits pineal and ocular oscillators during the course of subjective day via a multisynaptic neuronal pathway which includes the superior cervical ganglia (SCG). During the night, the pineal in turn inhibits SCN activity via its secretion of the hormone melatonin into the blood circulation. This neuroendocrine loop, it is proposed, synchronizes multiple oscillators within each component and maintains the stability and precision of the system.

Neurogenesis in adult canary telencephalon is independent of gonadal hormone levels

Article

Full-text available

Jun 1993

Neurons generated in adulthood are found throughout the canary telencephalon. We are interested in the factors that control the rate of proliferation of stem cells that give rise to these new neurons. The rate of incorporation of newly generated neurons into vocal-control regions varies seasonally. This difference could reflect a higher rate of neurogenesis, a lower rate of cell death, or an altered migration. We examined the incidence of thymidine-labeled cells in the telencephalic ventricular zone of adult canaries as a function of variations in gonadal hormone levels. Adult female canaries maintained on a short-day photoperiod were anesthetized and gonadectomized. Four separate groups of birds received systemic exposure to either testosterone, estradiol, a combination of an anti-androgen and an inhibitor of estrogen synthesis, or nothing. All birds were also implanted with an osmotic minipump that released 3H-thymidine for 3 d and were killed 4 or 7 d following the onset of treatment. Analysis of autoradiograms revealed no differences between groups in the incidence of labeling within the ventricular zone either at the level of the anterior commissure or directly adjacent to the vocal-control nucleus HVC (higher vocal center). These results suggest that sex steroids do not regulate the rate of cell division in the ventricular zone. Seasonal differences in the incorporation of labeled cells into HVC may therefore be due to regulation of neurogenesis by photoperiodic factors other than gonadal steroids or to some other cellular mechanism, such as differential migration or survival of neurons.

Photoperiodic controls in the secretion of gonadotropins in birds

Article

Jan 1975
Am Zool

D. S. Farner

Avian Daybreak and Evening Song in Relation to Time and Light Intensity

Article

Jul 1961

Immunocytochemical localization of androgen receptors in the male songbird and quail brain

Article

Mar 1992
J COMP NEUROL

The distribution of androgen receptors was studied in the brain of the Japanese quail (Coturnix japonica), the zebra finch (Taeniopygia guttata), and the canary (Serinus canaria) by immunocytochemistry with a polyclonal antibody (AR32) raised in rabbit against a synthetic peptide corresponding to a sequence located at the N-terminus of the androgen receptor molecule. In quail, androgen receptor-immunoreactive cells were observed in the nucleus intercollicularis and in various nuclei of the preoptic-hypothalamic complex, namely, the nucleus preopticus medialis, the ventral part of the nucleus anterior medialis hypothalami, the nucleus paraventricularis magnocellularis, the nucleus ventromedialis hypothalami, and the tuberal hypothalamus. In the two songbird species, labeled cells were also observed in various nuclei in the preoptic-hypothalamic region, in the nucleus taeniae, and in the nucleus intercollicularis. Additional androgen receptor-immunoreactive cells were present in the androgen-sensitive telencephalic nuclei that are part of the song control system. These immunoreactive sells filled and outlined the boundaries of the hyperstriatum ventrale, pars caudalis, nucleus magnocellularis neostriatalis anterioris (both in the lateral and medial subdivisions), and nucleus robustus archistriatalis. The immunoreactive material was primarily present in cell nuclei but a low level of immunoreactivity was also clearly detected in cytoplasm in some brain areas. These studies demonstrate, for the first time, that androgen receptors can be detected by immunocytochemistry in the avian brain and the results are in general agreement with the binding data obtained by autoradiography with tritiated dihydrotestosterone. Immunocytochemical methods offer several advantages over autoradiography and their use for the study of the androgen receptor will greatly facilitate the analysis of steroid-sensitive systems in the avian brain.

Pineal regulation of circadian rhythms of 2-deoxy[14C]glucose uptake and 2[125I]iodomelatonin binding in the visual system of the house sparrow, Passer domesticus

Article

Dec 1993

The pineal gland and its hormone melatonin are crucial for the generation of circadian rhythms in several species of passerine birds. The sites and mechanisms by which they influence avian behavior are therefore of particular interest. Recent research employing several brain imaging techniques has indicated that the sites of melatonin action within the avian brain are wide-spread within the 4 major visual pathways. In this study, we have investigated whether the avian homologue of the mammalian suprachiasmatic nucleus, the visual suprachiasmatic nucleus (vSCN), and other visually sensitive structures express circadian rhythms of 2-deoxy[14C]glucose (2DG) uptake and 2[125I]iodomelatonin (IMEL) binding in house sparrows,Passer domesticus, under constant environmental conditions in the presence or absence of the pineal gland. The results indicate that 2DG uptake in the vSCN is oscillatory in sham-operated sparrows but damps to arrhythmicity in pinealectomized birds, suggesting this structure contains a damped circadian oscillator independent of pineal input. We have also asked whether IMEL binding is rhythmic under these conditions in the same brains. These results indicate IMEL binding is rhythmic in several structures in the circadian, tectofugal, thalamofugal visual pathways and that pinealectomy increases the level of IMEL binding 2–4 fold suggesting that IMEL binding is down regulated by endogenous melatonin. However, the circadian rhythm of this binding is only gradually abolished, suggesting it too is regulated by a non-pineal circadian clock. These data are discussed in the context of the behavioral neurobiology of avian circadian systems and the neuroendocrine loop model.

Daily melatonin administration synchronizes circadian patterns of brain metabolism and behavior in pinealectomized house sparrows, Passer domesticus

Article

Dec 1993

Recent research in our laboratory has indicated that in sparrows the visual suprachiasmatic nucleus (vSCN) is metabolically rhythmic such that 2-deoxy[14C]glucose (2DG) uptake and specific binding of 2[125I]iodomelatonin (IMEL) are high during subjective day for up to 10 circadian cycles in constant darkness (DD). These rhythms damp to arrhythmicity in pinealectomized birds (PINX). The present study was designed to test the hypothesis that exogenous melatonin rhythmically applied can restore disrupted behavioral and cerebral rhythmicity. Pinealectomized house sparrows were placed in constant dim light and allowed to become arrhythmic. Experimental birds received 0.86 mM melatonin in 0.01% ethanol (ETOH) to drink for 12 of every 24 h for 14 days. Control birds received 0.01% ETOH only. Behavioral rhythmicity was restored by melatonin but not by ETOH. Birds were injected with 2DG 6 or 18 h following the beginning of melatonin (for experimental birds: MT06 and MT18 respectively) or ETOH (for control birds: ET06 and ET18 respectively) administration, allowed to survive 1 h and killed for 2DG and IMEL autoradiography. The data indicated 2DG rhythmicity such that uptake was high at MT18 in vSCN and several visual, auditory and limbic system structures in birds receiving melatonin but not in birds receiving ETOH. Similarly, IMEL binding rhythms were restored in vSCN and other visual, auditory and limbic system structures in birds receiving melatonin but not in those receiving ETOH. These data indicate that melatonin cycles are responsible for generating and/or driving a wide array of cerebral metabolic rhythms and that this influence is inhibitory.

Daily and circadian regulation of 2-[125I]Iodomelatonin binding in the chick brain

Article

Oct 1992

The pineal gland and its hormone melatonin are important in the control of circadian rhythms in birds. Recent research has indicated the presence of high affinity melatonin-binding sites in a wide array of avian cerebral structures. In this study melatonin-binding sites were localized and characterized in the brains of 2-week-old chicks using in vitro autoradiography and image analysis of 2-[125I]iodomelatonin (IMEL) binding. The IMEL binding predominated in the major components of the chick's visual and auditory systems. These brain binding sites showed a daily variation in IMEL binding, with a higher density of binding during the daytime. A significant peak in IMEL binding was observed in the late afternoon, Zeitgeber time 10. This rhythm of IMEL binding continued in constant darkness, with the peak at circadian time 10. The amplitude of the peak was increased in constant darkness in all structures, with the exception of the ectostriatum and neostriatum. Scatchard analysis of the binding revealed an average increase of 45 +/- 5% in the number of binding sites in the daytime vs. nighttime samples, with little change in the binding affinities, indicating that the rhythm in binding is caused by an increase in the total number of binding sites available in the daytime tissue, rather than an increase in the affinity of the binding sites. The data suggest that a rhythm of melatonin sensitivity in a diverse set of cerebral structures may regulate a temporal control of their function.

Quantitative histochemistry of cytochrome oxidase in rat brain

Article

Mar 1991
NEUROSCI LETT

A quantitative analysis of cytochrome oxidase (CO) activity in histochemically stained sections of rat brain was developed using tissue standards and computerized image processing. Standards of brain paste containing known amounts of CO were cryosectioned and stained under the same conditions as brain sections. The gray levels of the stain were converted to units of CO activity using a calibration curve derived from densitometric analysis of the standards. The technique yields reproducible quantitative values, has the superior anatomical resolution of histochemistry, and is compatible with autoradiography.

Reassessing the mechanisms and origins of vocal learning in birds

Article

Jun 1991
TRENDS NEUROSCI

Fernando Nottebohm

The most widely accepted hypothesis of vocal imitation in birds pre-dates many recent studies on the behavior, anatomy, physiology and cell biology of this phenomenon. It states that vocal learning involves two steps: (1) an auditory memory is laid down, and then (2) vocal output is modified until the auditory feedback it generates matches the model. This black-box model of vocal imitation disregards circuitry. We now know that the brain pathways for vocal learning in birds include a series of well-defined nuclei and projections. Some of these nuclei and projections develop late in ontogeny, at the time when auditory models are first acquired and imitated. We also know that the pathways involved in song production respond to sound, an observation that blurs the demarcation between what is an auditory and what is a motor circuit. These and other recent discoveries call for a reassessment of the mechanisms and origins of vocal learning in birds and mammals.

Photoperiod as a Modifying and Limiting Factor in the Expression of Avian Circannual Rhythms

Article

Feb 1989

Eberhard Gwinner

In three species of birds that migrate long distances, the annual rhythms of gonadal activity, molt, and migratory restlessness (Zugunruhe) persist for more than 1 year under certain constant conditions. The most important zeitgeber for these circannual rhythms is the annual cycle of photoperiod, which adjusts the overall period of circannual rhythms to exactly 1 year and also provides for the appropriate adjustment of seasonal activities to the temporal structure of the environment. This is illustrated by results on garden warblers (Sylvia borin) indicating that the longer photoperiods experienced by individuals wintering far south in the African wintering area phase-advance spring migration and the accompanying gonadal development, relative to those of individuals wintering further north. The rate of acceleration is, however, slow enough to prevent a reproductive cycle during the Southern Hemisphere summer. Hence, endogenous circannual components and zeitgeber stimuli constitute a functional entity that provides as a whole for adaptive temporal programming. This idea is further supported by findings in the pied flycatcher (Ficedula hypoleuca), in which a circannual rhythmicity persists only if photoperiod in winter is at least as short as that normally encountered by the species in its wintering grounds slightly north of the equator. In collared flycatchers (Ficedula albicollis), in contrast, rhythmicity continues under much longer photoperiods, consistent with the fact that the wintering area of this species extends to latitudes far south of the equator. It is proposed that the adaptive function of circannual rhythms can be properly understood only if their interactions with environmental factors, particularly those that play a role as zeitgebers, are analyzed in sufficient detail. The biological significance of circannual rhythms may be more apparent in the context of the environmental constraints limiting their expression than in the often rather restricted set of conditions sustaining spontaneous annual cyclicity.

Seasonal changes in gonadal hormone levels of adult male Canaries and their relation to song

Article

Apr 1987
Behav Neural Biol

Samples of song and blood levels of three gonadal hormones, T, DHT, and E2, were taken at monthly intervals from six adult male canaries over a period of 1 year, as these birds went from 12 to 24 months of age. Song variability and addition of new syllable types were maximal during the summer and early fall, with a peak in September. A secondary peak in new syllable acquisition occurred in March. Blood T levels were particularly low during July-August and during February. Thus, a lowering of blood T levels preceded by about 1 month the two marked peaks in new syllable acquisition. Blood levels of the two other hormones were related less obviously to song learning peaks. It is hypothesized that a concurrence of hormonal, neural, and behavioral changes facilitates song learning in adulthood.

Changes in neuronal number, density and size account for increases in volume of song-control nuclei during song development in Zebra finches

Article

Jul 1986
NEUROSCI LETT

The caudal nucleus of the ventral hyperstriatum (HVc) and the robust nucleus of the archistriatum (RA) are two anatomically discrete brain regions that are known to be involved with song production in adult passerine birds. Both the HVc and RA increase greatly in volume during a restricted period of song development in male zebra finches, while brain regions not involved with song control show little or no increase in size. We report here that the increased volume of the HVc is attributable to an increase in the number of neurons during this period of song learning, whereas the growth of the RA is due to an increase in the somal size of neurons and a decrease in neuronal density. The pattern of results described is consistent with the idea that the HVc matures prior to the RA, and that the development of the RA may depend on the ingrowth of axons from the HVc and other song-control regions.

Photoperiodism in Birds

Article

Feb 1985
Ciba Found Symp

Birds show a circadian rhythm in melatonin secretion and, as expected, the pattern of output changes with photoperiod. Somewhat surprisingly then, in view of the mechanisms in mammals, birds do not seem to use this seasonal message in the photoperiodic control of reproduction. Some further experiments are needed, however, because in birds the pineal gland is not the only source of melatonin. Another difference from mammals is that birds detect the photoperiodic light not with the retina but by brain photoreceptors, which probably lie in the hypothalamus. An action spectrum for these receptors has now been obtained for the quail and this shows a peak absorption at 492 nm, suggesting that the photoreceptor is rhodopsin-based. The sensitivity of the brain receptors to 500 nm light was calculated at 2 X 10(4) photons mm-2s-1. For light to induce the photoperiodic response it must be interpreted by the bird's clock as a long day. This happens if the light falls 12-20 h after dawn and coincides with a rhythm of photosensitivity. The subsequent neuroendocrine response to the light signal is both precise and relatively long-term. A single 4 h light pulse initiates a wave of gonadotropin secretion lasting for 10 days. The light stimulus can be replaced by a brief (2 min) daily electrical stimulus given to the hypothalamus 10-12 h after dawn. Over the next few years it should be possible to disentangle further the neural processes involved.

Neuronal replacement in adulthood

Article

Feb 1985

F Nottebohm

Entrainment of Circadian Rhythms by Sound in Passer domesticus

Article

Jan 1967

The circadian locomotor rhythm of house sparrows was entrained by a sound stimulus. The birds were maintained at a constant temperature in, dim green light. The entraining agent was 4 (1/2) 12 hours of tape-recorded bird song ,played each day. Variations in the response to this stimulus have been correlated with individual variations in free-running period. This is the first clear demonstration that a biological clock can be influenced by sound stimuli.

Quantitative analysis of sex differences in hormone accumulation in the Zebra Finch brain: Methodological and theoretical issues

Article

Feb 1980

Arthur Arnold

The autoradiographic method was used to compare the numbers of hormone accumulating cells in several brain regions in male and female zebra finches (Poephila guttata) after injection of tritiated testosterone. The brain regions examined were the caudal nucleus of the hyperstriatum ventrale (HVc), magnocellular nucleus of the anterior neostriatum (MAN), robust nucleus of the archistriatum (RA), nucleus intercollicularis of the midbrain (ICo), the tracheosyringeal hypoglossal motor nucleus (nXIIts), and periventricular magnocellular nucleus of the anterior hypothalamus (PVM). All but the last of these regions are thought to be involved in the control of vocalizations in passerine song birds. Males have significantly more labelled cells in HVc and MAN. In RA, there is no difference in total percentage of labelled cells, but there is a sex difference in size distribution of labelled cells. No sex difference was detected in other brain regions. These differences are found when using a criterion for cell labelling which is based on the Poisson distribution, and the relative merits are evaluated of various quantitative criteria used in the analysis of steroid autoradiograms. The magnitude of the observed sex difference may be influenced by several biasing factors, yet the sex difference persists when corrections are applied to eliminate the biases, indicating that the sex difference is not an artifact of autoradiographic procedure. The magnitude of the sex difference in hormone accumulation has certain implications for the process of sexual differentiation of the brain.

Comparative Distribution of 2[125I]Iodomelatonin Binding in the Brains of Diurnal Birds: Outgroup Analysis with Turtles

Article

Feb 1995

The roles that the pineal gland and its hormone melatonin play in the regulation of circadian rhythmicity and photoperiodism vary among vertebrate species. Recently, putative sites of melatonin action have been elucidated in several avian and mammalian species by application of in vitro binding of a radioiodinated melatonin agonist, 2[125I]iodomelatonin (IMEL) and autoradioradiography. These studies in mammals, birds and reptiles have indicated profound differences in the distribution of IMEL binding between these diverse groups, suggesting that these large differences in binding may reflect differences in melatonin function. The present study was performed to determine systematically whether the variance in IMEL binding among avian species corresponds to changes in circadian organization and/or phylogenetic relationships. The distribution of specific IMEL binding was determined in the brains from birds belonging to 14 different species in 5 Orders (Psittaciformes, Passeriformes, Columbiformes, Galliformes and Anseriformes) using in vitro binding, autoradiography and computer-assisted image analysis. The distribution was compared to a similar study in 3 species of turtles as an outgroup. The data indicated IMEL binding in retinorecipient structures of the circadian, tectofugal, thalamofugal and accessory optic visual pathways in all avian species. Relay nuclei and integrative structures of the tectofugal, thalamofugal, accessory optic, and limbic systems, however, bound the hormone to varying degrees. In turtles, binding was observed in retinorecipient structures of the thalamofugal visual pathway and in retinorecipient and integrative areas of the tectofugal visual pathway. No binding was observed in the pineal gland, tuberal hypothalamus or adenohypophysis in any avian or testudine species. This distribution is drastically different from that observed in mammals, where binding predominates in the pars tuberalis of the adenohypophysis and in the suprachiasmatic nucleus, suggesting that the circadian system may influence a wide array of sensory and integrative functions in birds and reptiles through the circadian secretion of melatonin, but that this capacity has been lost in mammals.

Testosterone-induced changes in adult canary brain are reversible

Article

May 1993

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)

The density of melatonin receptors is dependent upon the prevailing photoperiod in the Japanese quail (Coturnix japonica)

Article

Jun 1994
NEUROSCI LETT

Two groups of Japanese quail (Coturnix japonica) were exposed to two different photoperiods (short and long days: LD 8:16 and LD 16:8, respectively), and their brains examined for the presence and distribution of melatonin receptors by means of quantitative in vitro autoradiography. Animals belonging to the LD 8:16 group expressed a significantly higher melatonin receptor density in the optic tectum and nucleus triangularis, while the LD 16:8 animals had a higher density of receptors in the hyperstriatum and nucleus preopticus dorsalis. These data demonstrate an apparent influence of the photoperiod on the density of melatonin receptors, especially in nuclei of the tectofugal pathway, related to the control of visual pattern and intensity discrimination, localization and orientation.

Combined gonadal and photic influences on 2-[125I]iodomelatonin-binding level changes in some brain areas of the quail

Article

Jul 1994

Quantitative receptor autoradiography was used to study the binding of 2-[125I] iodomelatonin in the brain of the castrated and gonadally intact male Japanese quail Coturnix japonica exposed to both long- and short-day photoperiod cycles. The distribution study displayed that these conditions were responsible for a heterogeneous binding pattern as shown by elevated receptor levels being located in visual brain centers, such as the stratum opticum, nucleus pretectalis, and nucleus geniculatus lateralis, pars ventralis, while lower values were found in the nucleus lateralis hypothalami and nucleus isthmi pars magnocellularis. Closer examination of the 2-[125I] iodomelatonin-binding pattern following the different gonadal and photic influences showed that combination of the gonadally intact condition and a 16L:8D (long-day) photoperiod cycle was required for the greater binding changes. These differences occurred in brain sites such as the area preoptica, paleostriatum primitivum, and nucleus ectomamillaris. Saturation binding studies, which were carried out only in some of the above areas, revealed that the combined gonadal- and photic-induced changes are basically due to the modifications of total number of binding sites. The importance of a gonadal steroid modulatory role in the photic-dependent melatonin binding activity suggests that other types of neuronal mechanisms might be involved in the regulation of neuroendocrine and socio-sexual behaviors in nonmammalian vertebrates.

Distribution and characterization of melatonin receptors in the brain of the Japanese quail, Coturnix japonica

Article

Mar 1993
NEUROSCI LETT

2-[125I]iodomelatonin was used to study the distribution and properties of the melatonin receptor in the Japanese quail brain. High receptor density was detected in the major targets of direct retinal input (optic tectum, nucleus of the optic basal rout, ventrolateral geniculate nucleus), as well as areas representing terminals in the visual pathways (nucleus rotundus, ectostriatum, thalamo-hyperstriatal pathway). Binding was also found in the piriform cortex, the hypophyseal pars tuberalis, the oculomotorius nucleus and the associated Edinger-Westphal nucleus, and in the nuclei of the third, fourth and sixth cranial nerves. A comparison of the receptor pharmacological profile to that of the mammalian brain demonstrated pharmacological identity of the two binding sites. In the saturation experiments, GPT gamma S decreased the binding affinity, numerical Kd values increasing from approximately 35 pM to approximately 150 pM.

Estrogen receptors in the avian brain: Survey reveals general distribution and forebrain areas unique to songbirds

Article

Feb 1993

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.

Immu-nocytochemical localizationof androgenreceptorsinthemalesong-bird and the quail brain The Clockwork Sparrow: Time, Clocks, and Calendars in Biological Organisms

J Balthazart
A Foidart
E M Wilson
G F Ball

Balthazart, J., Foidart, A., Wilson, E. M., and Ball, G. F. (1992). Immu-nocytochemical localizationof androgenreceptorsinthemalesong-bird and the quail brain. J. Comp. Neurol. 317, 407±420. r537 Melatonin and Avian Song System Binkley, S. (1990). The Clockwork Sparrow: Time, Clocks, and Calendars in Biological Organisms. Prentice±Hall, Englewood Cliffs, NJ

Exogenous melatonin entrains circa-AID H&B 1340

Jan 1992
30

S Heigl
E Gwinner

Heigl, S., and Gwinner, E. (1992). Exogenous melatonin entrains circa-AID H&B 1340 / 6807$$$404 12-31-96 06:12:30 haba AP: H & B

Neurogenesis in binding in the visual system of the house sparrow, Passer domesticus. adult canary telencephalon is independent of gonadal hormone

Jan 1993
2024-2032

S D Brown
F Johnson
S W Bottjer

Brown, S. D., Johnson, F., and Bottjer, S. W. (1993). Neurogenesis in binding in the visual system of the house sparrow, Passer domesticus. adult canary telencephalon is independent of gonadal hormone J. Comp. Physiol. A 173, 765 -774. levels. J. Neurosci. 13, 2024 -2032.

is dependent upon the prevailing photoperiod in the Japanese quail Estrogen re-(Coturnix japonica)

Jan 1993
111-114

London Pittman
M Gahr
H R Guttinger
D E Kroodsma

Pittman, London. is dependent upon the prevailing photoperiod in the Japanese quail Gahr, M., Guttinger, H. R., and Kroodsma, D. E. (1993). Estrogen re-(Coturnix japonica). Neurosci. Lett. 173, 111 – 114.

Photoperiodic controls in the secretion of gonadothe initial stage of photoperiodism in the Japanese quail. Biol. Retrophins in birds

Jan 1975
Am Zool
935-941

M Ohta
C Kadota
H Konishi

Ohta, M., Kadota, C., and Konishi, H. (1989). A role of melatonin in Farner, D. S. (1975). Photoperiodic controls in the secretion of gonadothe initial stage of photoperiodism in the Japanese quail. Biol. Retrophins in birds. Am. Zool. 15, 117 -135. prod. 40, 935 -941.

Avian daybreak and evening ogy 131, 1297-1304. song in relation to time and light intensity

Jan 1961
CONDOR
269-293

A Endocrinolleopold
A E Eynon

tion of 2-[ 125 I]iodomelatonin binding in the chick brain. EndocrinolLeopold, A., and Eynon, A. E. (1961). Avian daybreak and evening ogy 131, 1297-1304. song in relation to time and light intensity. Condor 63, 269-293.

Photoperiodism Panzica, The density of melatonin receptors and the Pineal

Jan 1985
93-103

B K Follett
R G Foster
T J G C Nicholls
F Fraschini
N Aste
V Lucini
C B Viglietti-Panzica

Follett, B. K., Foster, R. G., and Nicholls, T. J. (1985). Photoperiodism Panzica, G. C., Fraschini, F., Aste, N., Lucini, V., Viglietti-Panzica, C., in birds. In D. Evered and S. Clark (Eds.), Photoperiodism, Melatonin Cozzi, B., and Stankov, B. (1994). The density of melatonin receptors and the Pineal, pp. 93 – 103.

Survey reveals general distribution Circadian photo-forebrain areas unique to songbirds

Jan 1978
112-122

J S Takahashi
C Norris
M Menaker

ceptors in the avian brain: Survey reveals general distribution and Takahashi, J. S., Norris, C., and Menaker, M. (1978). Circadian photo-forebrain areas unique to songbirds. J. Comp. Neurol. 327, 112 – 122.

Distribution and (1987) Seasonal changes in gonadal hormone levels of adult male characterization of melatonin receptors in the brain of the Japanese canaries and their relation to song

Jan 1993
197-211

B Cozzi
B Stankov
C Vigletti-Panzica
S Capsomi
N Aste
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Melatonin Binding in the House Sparrow Song Control System: Sexual Dimorphism and the Effect of Photoperiod

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