Fig 7 - uploaded by Anton Reiner
Content may be subject to copyright.
A: Photomicrograph illustrating the SP' fiber labeling surrounding the subpallial cell islets. Medial is to the right. B: Photomicrograph of a Nissl-stained section illustrating the subpallial cell islets (indicated by arrows). Medial is to the left. C. Photomicrograph illustrating the dense SP+ fiber labeling at caudal ventrolateral levels of the subpallium. The subpallial islet (Is), though surrounded by labeled fibers, is itself free of
Source publication
The telencephalon of the African lungflsh, Protopterus annectens, was studied by immunohistochemical techniques in order to identify the major subdivisions of the telencephalon and determine the possible homologues of these subdivisions, if any, in other vertebrates. The distributions of four different neuropeptides (substance P, leucine-enkephalin...
Contexts in source publication
Context 1
... islets extend from this level to the very ventrolateral pole of the telencephalon. Immunohistochemically, the S1 clearly shows several of the major characteristics of the basal ganglia in amniotes (Figs. 2 4 , 7, 8). At intermediate and caudal levels, S1 contains a great abundance of SP+, LENK+, 5HTt, APP+, TH+, and LANTG+ fibers. ...
Context 2
... the telencephalon. Immunohistochemically, the S1 clearly shows several of the major characteristics of the basal ganglia in amniotes (Figs. 2 4 , 7, 8). At intermediate and caudal levels, S1 contains a great abundance of SP+, LENK+, 5HTt, APP+, TH+, and LANTG+ fibers. The SP+ fibers are particularly abundant and heavily labeled in these regions (Figs. 4, 7). At caudal levels, the labeled fibers of more superficial portions of S1 envelop the cell islets characteristic of caudal S1 (Fig. 7). In addition to labeled fibers, S1 contains SP+, LENK+, and LANTG+ neurons (Figs. 2,3). Neurons positive for LANTG (Fig. 7) were observed in greatest abundance in caudal S1 at the level of the ...
Context 3
... 2 4 , 7, 8). At intermediate and caudal levels, S1 contains a great abundance of SP+, LENK+, 5HTt, APP+, TH+, and LANTG+ fibers. The SP+ fibers are particularly abundant and heavily labeled in these regions (Figs. 4, 7). At caudal levels, the labeled fibers of more superficial portions of S1 envelop the cell islets characteristic of caudal S1 (Fig. 7). In addition to labeled fibers, S1 contains SP+, LENK+, and LANTG+ neurons (Figs. 2,3). Neurons positive for LANTG (Fig. 7) were observed in greatest abundance in caudal S1 at the level of the interventricular foramen. At these levels, the LANTG' neurons are found within a region that also contains a dense field of coarse SP+ and LENK+ ...
Context 4
... fibers. The SP+ fibers are particularly abundant and heavily labeled in these regions (Figs. 4, 7). At caudal levels, the labeled fibers of more superficial portions of S1 envelop the cell islets characteristic of caudal S1 (Fig. 7). In addition to labeled fibers, S1 contains SP+, LENK+, and LANTG+ neurons (Figs. 2,3). Neurons positive for LANTG (Fig. 7) were observed in greatest abundance in caudal S1 at the level of the interventricular foramen. At these levels, the LANTG' neurons are found within a region that also contains a dense field of coarse SP+ and LENK+ ...
Similar publications
Although the brains of the three extant lungfish genera have been previously described, the spatial relationship between the brain and the neurocranium has never before been fully described nor quantified. Through the application of virtual microtomography (μCT) and 3D rendering software, we describe aspects of the gross anatomy of the brain and la...
Social plasticity is a pervasive feature of animal behavior. Animals adjust the expression of their social behavior to the daily changes in social life and to transitions between life-history stages, and this ability has an impact in their Darwinian fitness. This behavioral plasticity may be achieved either by rewiring or by biochemically switching...
Citations
... There is thus potential that L. dimidiatus becomes a model organism for highly integrative behavioural research on wrasse. (Reiner and Northcutt, 1987) ...
As evidence for advanced cognitive abilities in fishes steadily increases, cytoarchitectonic studies of the Actinopterygian telencephalon receive increasing interest by neuro-ethologists. However, the amount of information concerning brain organization in this group is still rather small. Here, we present a cytoarchitectonic analysis of the telencephalon of Labroides dimidiatus, a species showing highly sophisticated interspecific social behavior in cleaning interactions with other reef fish species. Analysing cresyl violet-stained serial transverse sections, we designated cell regions and nuclei on the basis of characteristic size, shape and intensity of pericarion staining, density and distribution of cell bodies, cell-poor zones; congruence of cell groups with brain cellular structure identified in other species, consistent sequence of cell groups in subsequent sections and in corresponding centres of the opposite hemisphere. 27 telencephalic regions and nuclei, 9 in the ventral part and 18 in the dorsal part of the telencephalon were recognized and described.
... Some authors located also TH+ cells in Dc (Hornby et al., 1987;Roberts et al., 1989;Piñuela and Northcutt, 2007;O'Connell et al., 2013a), in Dp (Piñuela and Northcutt, 2007;), in Dl (O'Connell et al., 2011O'Connell et al., 2013a), and in Dm (Piñuela and Northcutt, 2007). TH+ cell populations in the telencephalon in addition to the IGL were also found in elasmobranchs (Meredith and Smeets, 1987), lampreys (Pierre et al., 1997;Pombal et al., 1997), and lungfish (Reiner and Northcutt, 1987) and seem to be basal vertebrate characteristic that was lost in tetrapods. ...
... Some authors located also TH+ cells in Dc (Hornby et al., 1987;Roberts et al., 1989;Piñuela and Northcutt, 2007;O'Connell et al., 2013a), in Dp (Piñuela and Northcutt, 2007;), in Dl (O'Connell et al., 2011O'Connell et al., 2013a), and in Dm (Piñuela and Northcutt, 2007). TH+ cell populations in the telencephalon in addition to the IGL were also found in elasmobranchs (Meredith and Smeets, 1987), lampreys (Pierre et al., 1997;Pombal et al., 1997), and lungfish (Reiner and Northcutt, 1987) and seem to be basal vertebrate characteristic that was lost in tetrapods. ...
Dopamine is present in all vertebrates and the functional roles of the subsystems are assumed to be similar. Whereas the effect of dopaminergic modulation is well investigated in different target systems, less is known about the factors that are causing the modulation of dopaminergic cells. Using the zebra mbuna, Pseudotropheus zebra, a cichlid fish from Lake Malawi as a model system, we investigated the activation of specific dopaminergic
cell populations detected by double-labeling with TH and pS6 antibodies while the animals were solving different learning tasks. Specifically, we compared an intense avoidance learning situation, an instrumental learning task, and a non-learning isolated group and found strong activation of different dopaminergic cell populations. Preoptic-hypothalamic cell populations respond to the stress component in the avoidance task, and the forced movement/locomotion may be responsible for activation in the posterior tubercle. The instrumental learning
task had little stress component, but the activation of the raphe superior in this group may be correlated with attention or arousal during the training sessions. At the same time, the weaker activation of the nucleus of the posterior commissure may be related to positive reward acting onto tectal circuits. Finally, we examined the coactivation patterns across all dopaminergic cell populations and recovered robust differences across experimental groups, largely driven by hypothalamic, posterior tubercle, and brain stem regions possibly encoding the valence
and salience associated with stressful stimuli. Taken together, our results offer some insights into the different functions of the dopaminergic cell populations in the brain of a non-mammalian vertebrate in correlation with different behavioral conditions, extending our knowledge for a more comprehensive view of the mechanisms of dopaminergic modulation in vertebrates.
... Some authors located also TH+ cells in Dc (Hornby et al., 1987;Roberts et al., 1989;Piñuela and Northcutt, 2007;O'Connell et al., 2013a), in Dp (Piñuela and Northcutt, 2007;), in Dl (O'Connell et al., 2011O'Connell et al., 2013a), and in Dm (Piñuela and Northcutt, 2007). TH+ cell populations in the telencephalon in addition to the IGL were also found in elasmobranchs (Meredith and Smeets, 1987), lampreys (Pierre et al., 1997;Pombal et al., 1997), and lungfish (Reiner and Northcutt, 1987) and seem to be basal vertebrate characteristic that was lost in tetrapods. ...
Dopamine is present in all vertebrates and the functional roles of the subsystems are assumed to be similar. Whereas the effect of dopaminergic modulation is well investigated in different target systems, less is known about the factors that are causing the modulation of dopaminergic cells. Using the zebra mbuna, Pseudotropheus zebra, a cichlid fish from Lake Malawi as a model system, we investigated the activation of specific dopaminergic cell populations detected by double-labeling with TH and pS6 antibodies while the animals were solving different learning tasks. Specifically, we compared an intense avoidance learning situation, an instrumental learning task, and a non-learning isolated group and found strong activation of different dopaminergic cell populations. Preoptic-hypothalamic cell populations respond to the stress component in the avoidance task, and the forced movement/locomotion may be responsible for activation in the posterior tubercle. The instrumental learning task had little stress component, but the activation of the raphe superior in this group may be correlated with attention or arousal during the training sessions. At the same time, the weaker activation of the nucleus of the posterior commissure may be related to positive reward acting onto tectal circuits. Finally, we examined the co-activation patterns across all dopaminergic cell populations and recovered robust differences across experimental groups, largely driven by hypothalamic, posterior tubercle, and brain stem regions possibly encoding the valence and salience associated with stressful stimuli. Taken together, our results offer some insights into the different functions of the dopaminergic cell populations in the brain of a non-mammalian vertebrate in correlation with different behavioral conditions, extending our knowledge for a more comprehensive view of the mechanisms of dopaminergic modulation in vertebrates.
... The location of a pallidal homolog is believed to either reside as an intermingled population among the striatal neurons of the Vd, as evidenced through nkx2.1 expression, or found in a ventral part of the ventral area (Vv), which also expresses nkx2.1 and is in the same relative topographical position of the mammalian MGE (Alunni et al., 2004). In lobe-finned fish, the presence of a striatum and GP in the ventrolateral telencephalon has been characterized by the presence of GABAergic MSNs, SP and ENK neurons, dopaminergic innervation from midbrain structures, and region-specific expression of dlx2 and nkx2.1 in the striatum and pallidum, respectively (Reiner & Northcutt, 1987, Vallarino et al., 1998. The ventrolateral telencephalon of amphibians also contains a striatal sector, containing SP and ENK neurons, GABAergic neurons (Inagaki et al., 1981;Taban & Cathieni, 1983), and dlx1/2 expression . ...
Striatal neurons within the basal ganglia play a central role in vertebrate action selection; however, their location in larval zebrafish is not well defined. We assayed for conserved striatal markers in the zebrafish subpallium using fluorescent in situ hybridization (FISH) and immunohistochemistry. Whole mount FISH revealed an inhibitory neuronal cluster rostral to the anterior commissure that expresses tac1, the gene that encodes the precursor peptide for substance P. This molecular profile is shared by mammalian striatal direct pathway neurons. A second partially overlapping population of inhibitory neurons was identified that expresses penka, the gene that encodes the precursor peptide for enkephalin. This molecular profile is shared by striatal indirect pathway neurons. Immunostaining for substance P and enkephalin confirmed the presence of these peptides in the subpallium as well as the presence of dopaminergic innervation. The tac1 and penka populations were both found to increase linearly across larval stages. Together, these findings support the existence of a striatal homologue in larval zebrafish that grows to match the development and increasing behavioural complexity of the organism.
... Pérez -Urzainqui et al., 2012, zebrafish: Rink & Wullimann, 2001, commentary by Wullimann, 2014. Additionally, in some chondrichthyes and lungfishes a mesencephalic dopaminergic cell group is reported, but detailed information about the connectivity is not available (Meredith & Smeets, 1987;Northcutt, Reiner, & Karten, 1988;Reiner & Northcutt, 1987). ...
... (5) The majority of dopaminergic cells innervating the caudateputamen of mammals are located in the ventral tier of the SNc (reviewed by Björklund & Dunnett, 2007), which is represented mostly by the ventral TPdm of anurans ( Figure 8). In lamprey, chondrichthyes, and teleosts, this nigrostriatal projection is represented by dopaminergic neurons in the posterior tubercle (Northcutt et al., 1988;Pérez-Fernández et al., 2014;Reiner & Northcutt, 1987;Rink & Wullimann, 2001;Wullimann, 2014). (Herkenham & Nauta, 1979;Kiss, Csáki, Bokor, Kocsis, & Kocsis, 2002) and cat (Araki et al., 1988), should be in compliance with VHb innervation of the Rm (Figure 7a). ...
Whereas our understanding of the dopaminergic system in mammals allows for a distinction between ventral tegmental area (VTA) and substantia nigra pars compacta (SNc), no clear evidence for separate structures in anamniotes has been presented to date. To broaden the insight into the organization and regulation of neuromodulatory systems in anuran amphibians, tracing and immunohistochemical investigations were performed in the Oriental fire-bellied toad, Bombina orientalis. Topographically organized catecholaminergic "nigrostriatal", "mesolimbic", "mesocortical", and spinal cord projections arising from the posterior tubercle and mesencephalic tegmentum were identified. We compared these results with published data from lampreys, chondrichthyes, teleosts, amphibians, reptiles, birds, and mammals. Based on the pattern of organization, as well as the differential innervation by the habenular nuclei, domains gradually comparable to the mammalian paranigral VTA, ventral tier of the SNc, interfascicular nucleus of the VTA, and supramamillary/retromamillary area were identified. Additionally, we could demonstrate topographic separate populations of habenula neurons projecting via a direct excitatory or indirect GABAergic pathway onto the catecholaminergic VTA/SNc homologs and serotonergic raphe nuclei. The indirect GABAergic habenula pathway derives from neurons in the superficial mamillary area, which in terms of its connectivity and chemoarchitecture resembles the mammalian rostromedial tegmental nucleus. These results demonstrate a much more elaborate interconnection principle of the anuran dopaminergic system than previously assumed. Based on the data presented it seems that most features of the dopaminergic system of amniotes had already evolved when the amphibian line of evolution diverged from that leading up to mammals, reptiles, and birds. This article is protected by copyright. All rights reserved.
... Studies on the neuroanatomy of lungfishes using modern methods such as immunohistochemistry, in situ hybridization, or tract-tracing techniques (see Morona, López, Northcutt, & González, 2018) are of special relevance because with classical staining techniques most regions of the brain that constitute clear divisions in the amniotes are not distinguished in lungfishes. This is due to the very limited cell migration from the ventricular zone, which leaves most neuron perikarya in a central layer where distinct brain structures can be recognized, at best, as local condensations Nieuwenhuys, 1998;Northcutt, 2011), Thus, the immunohistochemical detection of several markers, including neurotransmitters and other molecular markers, have revealed neuroanatomical features in the brain organization of lungfishes that allowed us to determine the extent to which it is comparable to that of tetrapods (see Morona et al., 2018;Reiner & Northcutt, 1987). ...
... Some researchers considered that most of the medial wall of the hemispheres of lungfishes was homologous to the septum in other vertebrates (reviewed by Nieuwenhuys, 1998) and this view was called the "restricted pallium hypothesis." However, our immunohistochemical analysis of Pax6 cells strongly supports the "extended pallium hypothesis," which considers that the medial telencephalic wall in lungfishes consists of a large, dorsal medial pallium, and a ventral septum (see González & Northcutt, 2009;Reiner & Northcutt, 1987) (Lindsay et al., 2005). The ventral pallial region, adjacent to the palliosubpallial boundary, which contains abundant Pax6 cells in the adult pallium of lungfishes has been proposed to include the lateral amygdala, as in amphibians (Brox, Puelles, Ferreiro, & Medina, 2004;González & Northcutt, 2009;Moreno & González, 2004 and it will be discussed below together with other amygdaloid complex. ...
The Pax6 gene encodes a regulatory transcription factor that is key in brain development. The molecular structure of Pax6, the roles it plays and its patterns of expression in the brain have been highly conserved during vertebrate evolution. As neurodevelopment proceeds, the Pax6 expression changes from the mitotic germinal zone in the ventricular zone to become distributed in cell groups in the adult brain. Studies in various vertebrates, from fish to mammals, found that Pax6 expression is maintained in adults in most regions that express it during development. Specifically, in amphibians Pax6 is widely expressed in the adult brain and its distribution pattern serves to highlight regional organization of the brain. In the present study we analyzed the detailed distribution of Pax6 cells in the adult central nervous system of lungfishes, the closest living relatives of all tetrapods. Immunohistochemistry was performed using double labeling techniques with several neuronal markers of known distribution patterns served to evaluate the actual location of Pax6 cells. Our results show that Pax6 expression is maintained in the adult brain of lungfishes, in distinct regions of the telencephalon (pallium and subpallium), diencephalon, mesencephalon, hindbrain, spinal cord and retina. The pattern of Pax6 expression is largely shared with amphibians and helps to understand the primitive condition that would have characterized the common ancestors to all sarcopterygians (lobe‐finned fishes and tetrapods), in which Pax6 would be needed to maintain specific entities of subpopulations of neurons. This article is protected by copyright. All rights reserved. Pax6 expression is maintained in the adult brain of lungfishes, in cells widely distributed in a stereotyped manner that allows the neuroanatomical identification of main brain regions, boundaries and distinct cell groups comparable to those of tetrapods, which evolved from an extinct close relative of lungfishes.
... Progenitors of the subpallium contribute inhibitory GABAergic neurons to the striatum and pallidum, highly conserved components of basal ganglia circuitry [21][22][23]. An extensive confluence of data from connections, cellular morphology, neurotransmitter expression, and developmental genetics indicates that a striatum and pallidum are found in all extant vertebrates in a similar topographical arrangement [24][25][26][27]. In addition, the subpallium generates GABAergic interneurons that disperse by tangential migration and then integrate into the circuits of the pallium ( Figure 1) [28,29]. ...
... Bullfrog adapted from [198] (DP, dorsal pallium; LP, lateral pallium; MP, medial pallium). Lungfish adapted from [24] and coelacanth from [199]. Ray-finned fishes adapted from [130] (DL, dorsolateral area; DM, dorsomedial area). ...
... Further studies of lungfishes, the closest living relatives of tetrapods, may help to address this possibility [128,129]. The African lungfish Protopterus annectens appears to possess a cortex-like structure segregated from the pallial ventricular grey matter, but little is known of its intrinsic organization ( Figure 5, Lungfish) [24,130]. ...
The dramatic evolutionary expansion of the neocortex, together with a proliferation of specialized cortical areas, is believed to underlie the emergence of human cognitive abilities. In a broader phylogenetic context, however, neocortex evolution in mammals, including humans, is remarkably conservative, characterized largely by size variations on a shared six-layered neuronal architecture. By contrast, the telencephalon in non-mammalian vertebrates, including reptiles, amphibians, bony and cartilaginous fishes, and cyclostomes, features a great variety of very different tissue structures. Our understanding of the evolutionary relationships of these telencephalic structures, especially those of basally branching vertebrates and invertebrate chordates, remains fragmentary and is impeded by conceptual obstacles. To make sense of highly divergent anatomies requires a hierarchical view of biological organization, one that permits the recognition of homologies at multiple levels beyond neuroanatomical structure. Here we review the origin and diversification of the telencephalon with a focus on key evolutionary innovations shaping the neocortex at multiple levels of organization.
... The telencephalic structures of the lungfish, Protopterus annectens, (a living species that represents an extinct member that gave rise to an amphibian), were immunohistochemically examined to study fish-amphibian transition [18,19]. A cluster of neurons positive for SP, ENK, TH [21], and NPY [22] were found in the basal telencephalon, revealing a primitive form of the basal ganglia composed of striatal and pallial subdivisions. A mosaic-like structure, however, was not described. ...
The intricate neuronal architecture of the striatum plays a pivotal role in the functioning of the basal ganglia circuits involved in the control of various aspects of motor, cognitive, and emotional functions. Unlike the cerebral cortex, which has a laminar structure, the striatum is primarily composed of two functional subdivisions (i.e., the striosome and matrix compartments) arranged in a mosaic fashion. This review addresses whether striatal compartmentalization is present in non-mammalian vertebrates, in which simple cognitive and behavioral functions are executed by primitive sensori-motor systems. Studies show that neuronal subpopulations that share neurochemical and connective properties with striosomal and matrix neurons are present in the striata of not only anamniotes (fishes and amphibians), but also amniotes (reptiles and birds). However, these neurons do not form clearly segregated compartments in these vertebrates, suggesting that such compartmentalization is unique to mammals. In the ontogeny of the mammalian forebrain, the later-born matrix neurons disperse the early-born striosome neurons into clusters to form the compartments in tandem with the development of striatal afferents from the cortex. We propose that striatal compartmentalization in mammals emerged in parallel with the evolution of the cortex and possibly enhanced complex processing of sensory information and behavioral flexibility phylogenetically.
... First, there are major differences in the hemispheres in Protopterus and Neoceratodus and the structures in the medial wall located ventral to the ependymal membrane in Neoceratodus, and most of the thick medial wall of Protopterus have been believed by some researchers to be homologous to the septum in other vertebrates, proposing therefore that the medial pallium (MP) of this animals is a very reduced structure (Nieuwenhuys and Meek, 1990;von Bartheld et al., 1990;Nieuwenhuys, 1998). In contrast to this ''restricted pallium hypothesis'' other authors proposed the ''extended pallium hypothesis'' in which the medial telencephalic wall in lungfishes is constituted by a dorsal MP and a ventral septum (Northcutt, 1984;Reiner and Northcutt, 1987) as in other vertebrates. This latter hypothesis has been particularly reinforced by different immunohistochemical studies (see López et al., 2017b), and the combination of Nkx2.1 and Isl1 that allow the septal identification from rostral to caudal levels supports it (present results). ...
... The connections of the basal ganglia in Pleurodeles suggested the presence of an actual pallidum ventrocaudal to the Marín et al. (1998b) confirmed by the Nklx2.1 expression (present results). In the case of lungfishes, the connections of the basal ganglia have not been studied, but the region here considered as pallidum coincides with that proposed in Protopterus based on the immunohistochemical demonstration of LANT6, a peptide specifically contained in pallidal neurons in amniotes (present results; Reiner and Northcutt, 1987;. ...
Expression patterns of Nkx2.1 and Islet-1 (Isl1), which encode transcription factors that are key in the regionalization of the forebrain, were analyzed by combined immunohistochemical methods in young adult specimens of two lungfishes (Neoceratodus forsteri and Protopterus dolloi) and a urodele amphibian (Pleurodeles waltl). We aimed to get insights into the possible organization of the forebrain in the common ancestor of all tetrapods because of the pivotal phylogenetic significance of these two groups, being lungfishes the closest living relatives of tetrapods, and representing urodeles a model of simple brain organization with most shared features with amniotes. These transcription factors display regionally restricted expression domains in adult (juvenile) brains that are best interpreted according to the current prosomeric model. The regional patterns observed serve to identify regions and compare between the three species studied, and with previous data reported mainly for amniotes. We corroborate that Nkx2.1 and Isl1 expressions have very similar topologies in the forebrain. Common features in all sarcopterygians (lungfishes and tetrapods) have been observed, such as the Isl1 expression in most striatal neurons, whereas Nkx2.1 is restricted to migrated interneurons that reach the ventral pallium (VP). In the pallidal derivatives, the combination of both markers allows the identification of the boundaries between the ventral septum, the bed nucleus of the stria terminalis (BST) and the preoptic commissural region. In addition, the high Isl1 expression in the central amygdala (CeA), its boundary with the lateral amygdala (LA), and the scattered Nkx2.1 expression in the medial amygdala (MeA) are also shared features. The alar and basal hypothalamic territories, and the prethalamus and posterior tubercle (TP) in the diencephalon, have maintained a common pattern of expression. This regional distribution of Isl1 and Nkx2.1 observed in the forebrain of urodeles and lungfishes contributes further to our understanding of the first terrestrial vertebrates and their ancestors.
