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![Development of larval zebrafish subpallium. Transverse sections show precommissural (a) and commissural (b) telencephalon, as well as medial amygdala and eminentia thalami in early mouse and zebrafish postcommissural telencephalon (c) with critical gene expression [modified from Gerlach and Wullimann, 2021; see there for more references on mouse and zebrafish gene expression]. Solid arrows designate radial migrations, dotted arrows designate tangential migrations. ac, anterior commissure; CGE, caudal ganglionic eminence; Dl, lateral zone of dorsal telencephalic area; Dm, medial zone of dorsal telencephalic area; DP, dorsal pallium (isocortex); DT, dorsal thalamus; ENv, ventral entopeduncular nucleus; EmT, eminentia thalami; Hy, hypothalamus; lfb, lateral forebrain bundle; LVe, lateral (telencephalic) ventricle; M3, early larval migration zone of eminentia thalami (= ENv); M4, early larval telencephalic migration zone (subpallial); MeA, medial amygdala; MP, medial pallium; Po, preoptic area (zebrafish); POA, anterior preoptic area (mouse); Pr, pretectum; Sd, larval dorsal part of subpallium; Sdd, dorsal subdivision of Sd (striatum homomog); Sdv, ventral subdivision of Sd (pallidum homolog); Sdp, posterior subdivision of Sd (subpallial amygdala homolog); SPV, supraopto-paraventricular region; Sv, larval ventral part of subpallium (septum homolog); TelCh, tela choroidea; Vi, intermediate nucleus of ventral telencephalon (medial amygdala homolog); VP, ventral pallium (pallial amygdala); VT, ventral thalamus (prethalamus). For gene names see text.](publication/361456476/figure/fig1/AS:11431281099881939@1669304294251/Development-of-larval-zebrafish-subpallium-Transverse-sections-show-precommissural-a.png)
Development of larval zebrafish subpallium. Transverse sections show precommissural (a) and commissural (b) telencephalon, as well as medial amygdala and eminentia thalami in early mouse and zebrafish postcommissural telencephalon (c) with critical gene expression [modified from Gerlach and Wullimann, 2021; see there for more references on mouse and zebrafish gene expression]. Solid arrows designate radial migrations, dotted arrows designate tangential migrations. ac, anterior commissure; CGE, caudal ganglionic eminence; Dl, lateral zone of dorsal telencephalic area; Dm, medial zone of dorsal telencephalic area; DP, dorsal pallium (isocortex); DT, dorsal thalamus; ENv, ventral entopeduncular nucleus; EmT, eminentia thalami; Hy, hypothalamus; lfb, lateral forebrain bundle; LVe, lateral (telencephalic) ventricle; M3, early larval migration zone of eminentia thalami (= ENv); M4, early larval telencephalic migration zone (subpallial); MeA, medial amygdala; MP, medial pallium; Po, preoptic area (zebrafish); POA, anterior preoptic area (mouse); Pr, pretectum; Sd, larval dorsal part of subpallium; Sdd, dorsal subdivision of Sd (striatum homomog); Sdv, ventral subdivision of Sd (pallidum homolog); Sdp, posterior subdivision of Sd (subpallial amygdala homolog); SPV, supraopto-paraventricular region; Sv, larval ventral part of subpallium (septum homolog); TelCh, tela choroidea; Vi, intermediate nucleus of ventral telencephalon (medial amygdala homolog); VP, ventral pallium (pallial amygdala); VT, ventral thalamus (prethalamus). For gene names see text.
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The neuromeric/prosomeric model has been rejuvenated by Puelles and Rubenstein (1993). Here, its application to the (teleostean) fish brain is detailed beginning with a historical account. The second part addresses three main issues with particular interest for fish neuroanatomy and looks at the impact of the neuromeric model on their understanding...
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... Helix-Loop-Helix (bHLH) and downstream expressed genes functionally related to neurogenesis and revealed great similarities to amniote telencephalic development (reviewed in [Mueller and Wullimann, 2016]). These zebrafish studies showed that bHLH genes Neurogenin1 (Ngn1) and NeuroD are expressed in developing neurons in the zebrafish pallium (Fig. 4c, right panel). In contrast, Zash1a (Ascl1a, formerly Mash1 in mouse) is complementarily expressed in the subpallium (review in [Gerlach and Wullimann, 2021]), as is the downstream subpallial marker gene Dlx2a (Fig. 4a, b). For the sake of simplicity, respective zebrafish pallial and subpallial expression domains of bHLH genes Ngn1/NeuroD and Ascl1a ...
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... studies showed that bHLH genes Neurogenin1 (Ngn1) and NeuroD are expressed in developing neurons in the zebrafish pallium (Fig. 4c, right panel). In contrast, Zash1a (Ascl1a, formerly Mash1 in mouse) is complementarily expressed in the subpallium (review in [Gerlach and Wullimann, 2021]), as is the downstream subpallial marker gene Dlx2a (Fig. 4a, b). For the sake of simplicity, respective zebrafish pallial and subpallial expression domains of bHLH genes Ngn1/NeuroD and Ascl1a are only shown in panel 4c but not in Figure 4a, b (see [Wullimann and Mueller, 2002] and Wullimann, 2002b, 2003] for full account). The LIM genes Lhx7 and Lhx6 are more restrictively expressed in the ...
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... contrast, Zash1a (Ascl1a, formerly Mash1 in mouse) is complementarily expressed in the subpallium (review in [Gerlach and Wullimann, 2021]), as is the downstream subpallial marker gene Dlx2a (Fig. 4a, b). For the sake of simplicity, respective zebrafish pallial and subpallial expression domains of bHLH genes Ngn1/NeuroD and Ascl1a are only shown in panel 4c but not in Figure 4a, b (see [Wullimann and Mueller, 2002] and Wullimann, 2002b, 2003] for full account). The LIM genes Lhx7 and Lhx6 are more restrictively expressed in the pallidal part of the subpallium (i.e., Sdv), and Lxh6 extends -like Dlx2a -laterally into peripherally migrated cell masses of M4 ( Fig. 3a1; Fig. 4 a, b). ...
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... are only shown in panel 4c but not in Figure 4a, b (see [Wullimann and Mueller, 2002] and Wullimann, 2002b, 2003] for full account). The LIM genes Lhx7 and Lhx6 are more restrictively expressed in the pallidal part of the subpallium (i.e., Sdv), and Lxh6 extends -like Dlx2a -laterally into peripherally migrated cell masses of M4 ( Fig. 3a1; Fig. 4 a, b). Furthermore, gad67 (gad1b), the gene coding for the synthetic enzyme leading to GABA, and the latter itself (both not shown) have fitting larval subpallial expression pattern (not shown; see [Mueller et al., 2006[Mueller et al., , 2008). Thus, the message regarding the identity of M4 could not be clearer: these larval migrated cell ...
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... further comment is necessary regarding the most caudal (postcommissural) telencephalic level (Fig. 4c). We had only recently discussed comparatively the larval zebrafish and embryonic mouse forebrain [Gerlach and Wullimann, 2021]. Briefly, the zebrafish subpallium includes septal (Sv = adult Vv), striatal (Sdd = adult Vdd), pallidal (Sdv = adult Vdd) and subpallial amygdalar (Sdp = adult Vs, Vp,Vi) divisions ( Fig. 2a, b; Fig. 3a-d, ...
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... [Turner et al., 2016]:). The most posterior subpallial area (i.e., the intermediate nucleus of ventral telencephalon, Vi, was most recently characterized in larval and adult zebrafish brains [Herget et al., 2014;Biechl et al., 2017] and recognized as the homolog of the amniote medial amygdala (Fig. 4c). This was based on kin recognition related behavior, vomeronasal-like peripheral input, higher-order neuronal connectivity, and neuronal activity (review by [Gerlach and Wullimann, ...
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... of the preoptic region (see Section 2). Second, it has been convincingly shown that the amniote medial amygdala (see citations and discussion in [Gerlach and Wullimann, 2021]) is a basically GABAergic division of the subpallial amygdala which receives unusual large contributions of glutamatergic cells from other regions via tangential migration ( Fig. 4c; dotted arrows in left panel). These include for example Lhx9 positive cells from the ventral pallium [García- López et al., 2008;Bupesh et al., 2011b] or -important for the argument here -Otp/Lhx5 positive cells from the supraopto-paraventricular (preoptic) region ( [García-Moreno et al., 2010]; see Section 2), plussomewhat ironically ...
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... involved in the GABAergic neurogenetic pathway, whereas the SPV expressess markers of glutamatergic cell development, such as the bHLH genes Ngn2 and NeuroD [Osório et al., 2010], the LIM homeodomain gene Lhx9 [Rétaux et al., 1999;García-López et al., 2008], and, importantly, the Orthopedia (Otp) gene is typically expressed in the SPV ( ; see Fig. 4c). The rodent SPV contains the adult paraventricular and supraoptic nuclei which represent the cellular loci of neuroendocrine neuropeptides including oxytocin (formerly isotocin in teleosts) and vasopressin (formerly arginin vasotocin in teleosts [Theofanopoulou et al., 2021] and various additional neurosecretory peptides (releasing ...
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... adjacent Dlx2a expression (similar to Dlx5 as described above), the SPV itself being glutamatergic as evidenced by expression of bHLH gene Neurogenin1. These authors furthermore divided the SPV molecularly into an anterior Sim1a/Foxg1 positive domain (overlapping with otp) and a posterior Sim1a-only expressing domain, as similarly seen in mouse ( Fig. 4c; [Morales et al., 2021]; reviewed in [Gerlach and Wullimann, ...
Citations
... The dopaminergic group of the posterior tubercle of actinopterygian fishes would correspond to the diencephalic component of the mesodiencephalic dopaminergic complex present in lungfishes and tetrapods (González et al., 1994;López et al., 2019;Lozano et al., 2019;Wullimann, 2022). The object of the present study is the expression of Isl1 in adult specimens, but nevertheless we cannot exclude the Isl1 expression in the posterior tubercle during brain development or its possible role in the acquisition of the dopaminergic phenotype in this region. ...
Islet-1 (Isl1) is one of the most conserved transcription factors in the evolution of vertebrates, due to its continuing involvement in such important functions as the differentiation of motoneurons, among other essential roles in cell fate in the forebrain. Although its functions are thought to be similar in all vertebrates, the knowledge about the conservation of its expression pattern in the central nervous system goes as far as teleosts, leaving the basal groups of actinopterygian fishes overlooked, despite their important phylogenetic position. In order to assess the extent of its conservation among vertebrates, we studied its expression pattern in the central nervous system of selected nonteleost actinopterygian fishes. By means of immunohistochemical techniques, we analyzed the Isl1 expression in the brain, spinal cord, and sensory ganglia of the cranial nerves of young adult specimens of the cladistian species Polypterus senegalus and Erpetoichthys calabaricus, the chondrostean Acipenser ruthenus, and the holostean Lepisosteus oculatus. We also detected the presence of the transcription factor Orthopedia and the enzymes tyrosine hydroxylase (TH) and choline acetyltransferase (ChAT) to better locate all the immunoreactive structures in the different brain areas and to reveal the possible coexpression with Isl1. Numerous conserved features in the expression pattern of Isl1 were observed in these groups of fishes, such as populations of cells in the subpallial nuclei, preoptic area, subparaventricular and tuberal hypothalamic regions, prethalamus, epiphysis, cranial motor nuclei and sensory ganglia of the cranial nerves, and the ventral horn of the spinal cord. Double labeling of TH and Isl1 was observed in cells of the preoptic area, the subparaventricular and tuberal hypothalamic regions, and the prethalamus, while virtually all motoneurons in the hindbrain and the spinal cord coexpressed ChAT and Isl1. Altogether, these results show the high degree of conservation of the expression pattern of the transcription factor Isl1, not only among fish, but in the subsequent evolution of vertebrates.
The telencephalon of ray‐finned fishes undergoes eversion, which is very different to the evagination that occurs in most other vertebrates. Ventricle morphogenesis is key to build an everted telencephalon. Thus, here we use the apical marker zona occludens 1 to understand ventricle morphology, extension of the tela choroidea and the eversion process during early telencephalon development of four teleost species: giant danio ( Devario aequipinnatus ), blind cavefish ( Astyanax mexicanus ), medaka ( Oryzias latipes ), and paradise fish ( Macroposus opercularis ). In addition, by using immunohistochemistry against tubulin and calcium‐binding proteins, we analyze the general morphology of the telencephalon, showing changes in the location and extension of the olfactory bulb and other telencephalic regions from 2 to 5 days of development. We also analyze the impact of abnormal eye and telencephalon morphogenesis on eversion, showing that cyclops mutants do undergo eversion despite very dramatic abnormal eye morphology. We discuss how the formation of the telencephalic ventricle in teleost fish, with its characteristic shape, is a crucial event during eversion.
The brain is spatially organized into subdivisions, nuclei and areas, which often correspond to functional and developmental units. A segmentation of brain regions in the form of a consensus atlas facilitates mechanistic studies and is a prerequisite for sharing information among neuroanatomists. Gene expression patterns objectively delineate boundaries between brain regions and provide information about their developmental and evolutionary histories. To generate a detailed molecular map of the larval zebrafish diencephalon, we took advantage of the Max Planck Zebrafish Brain (mapzebrain) atlas, which aligns hundreds of transcript and transgene expression patterns in a shared coordinate system. Inspection and co‐visualization of close to 50 marker genes have allowed us to resolve the tripartite prosomeric scaffold of the diencephalon at unprecedented resolution. This approach clarified the genoarchitectonic partitioning of the alar diencephalon into pretectum (alar part of prosomere P1), thalamus (alar part of prosomere P2, with habenula and pineal complex), and prethalamus (alar part of prosomere P3). We further identified the region of the nucleus of the medial longitudinal fasciculus, as well as the posterior and anterior parts of the posterior tuberculum, as molecularly distinct basal parts of prosomeres 1, 2, and 3, respectively. Some of the markers examined allowed us to locate glutamatergic, GABAergic, dopaminergic, serotoninergic, and various neuropeptidergic domains in the larval zebrafish diencephalon. Our molecular neuroanatomical approach has thus (1) yielded an objective and internally consistent interpretation of the prosomere boundaries within the zebrafish forebrain; has (2) produced a list of markers, which in sparse combinations label the subdivisions of the diencephalon; and is (3) setting the stage for further functional and developmental studies in this vertebrate brain.
Gamma-aminobutyric acid (GABA) functions as the primary inhibitory neurotransmitter within the central nervous system (CNS) of vertebrates. In this study, we examined the distribution pattern of GABA immunoreactive (GABA-ir) cells and fibres in the CNS of the viviparous teleost Poecilia sphenops using immunofluorescence and immunocytochemical methods. GABA immunoreactivity was seen in the glomerular, mitral, and granular layers of the olfactory bulbs, as well as in most parts of the dorsal and ventral telencephalon. The preoptic area consisted of a small cluster of GABA-ir cells, whereas extensively labelled GABA-ir neurons were observed in the hypothalamic areas, including the paraventricular organ, tuberal hypothalamus, nucleus recessus lateralis, nucleus recessus posterioris, and inferior lobes. In the thalamus, GABA-positive neurons were only found in the ventral thalamic and central posterior thalamic nuclei, whereas the dorsal part of the nucleus pretectalis periventricularis consisted of a few GABA-ir cells. GABA-immunoreactivity was extensively seen in the alar and basal subdivisions of the midbrain, whereas in the rhombencephalon, GABA-ir cells and fibres were found in the cerebellum, nucleus of glossopharyngeal and vagal nerves, nucleus commissuralis of Cajal, and reticular formation. In the spinal cord, GABA-ir cells and fibres were observed in the dorsal horn, ventral horn, and around the central canal. Overall, the extensive distribution of GABA-ir cells and fibres throughout the CNS suggests several roles for GABA, including neuroendocrine, viscerosensory, and somatosensory functions, for the first time in a viviparous teleost.
The amygdala is a central node in functional networks regulating emotions, social behavior and social cognition. It develops in the telencephalon and includes pallial and subpallial parts, but these are extremely complex with multiple subdivisions, cell types and connections. The homology of the amygdala in non-mammals is highly controversial, especially for the pallial part, and we are still far from understanding general principles on its organization that are common to different groups. Here we review data on the adult functional architecture and developmental genoarchitecture of the amygdala in different amniotes (mammals and sauropsids), which are helping to disentangle and to better understand this complex structure. The use of an evolutionary developmental biology (evodevo) approach has helped to distinguish three major divisions in the amygdala, derived from the pallium, the subpallium and from a newly identified division called telencephalon-opto-hypothalamic domain (TOH). This approach has also helped to identify homologous cell populations with identical embryonic origins and molecular profiles in the amygdala of different amniotes. While subpallial cells produce different subtypes of GABAergic neurons, the pallium and TOH are major sources of glutamatergic cells. Available data point to a development-based molecular code that contributes to shape distinct functional subsystems in the amygdala, and comparative genoarchitecture is helping to delineate the cells involved in same subsystems in non-mammals. Thus, the evodevo approach can provide crucial information to understand common organizing principles of the amygdalar cells and networks that control behavior, emotions and cognition in amniotes.
