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Diagrams showing the telencephalic divisions and subdivisions in tetrapods (A) or fish (B). As shown in (A), each telencephalic division/subdivision shows expression of a unique combination of developmental regulatory genes. Many of the genes represented have been analyzed in mouse, chick and Xenopus ( Dlx/Dll , Nkx 2.1, Sonic hedgehog or Shh , Pax 6, Tbr 1 / 2, and Emx 1). Some of these have also been analyzed in turtle ( Dlx , Pax 6, Emx 1). Their expression patterns in the different species, in combination with other anatomical and molecular data, suggest that all tetrapods show the same (field homologous) molecularly distinct divisions and subdivisions in the telencephalon. Some of the genes shown in (A) have only been analyzed in mouse ( Dbx 1, Lmo 2, Lmo 3) and more studies are needed in non-mammalian species. Based on expression of Distal-less ( Dll ) and Pax 6, it appears that the major telencephalic divisions (pallium and subpallium) are present in fish (including jawed fish, such as the teleost zebrafish, as well as some jawless fish, such as the lamprey). Based on expression of Nkx 2.1, zebrafish appears to have striatal and pallidal subdivisions in the subpallium, but the lamprey apparently lacks such subpallial subdivisions. In the pallium, the expression pattern of Emx 1 suggests the existence of a ventral pallial subdivision in fish (including the lamprey). The existence of a medial pallium has also been proposed in teleosts based on other criteria (topological position, connections, function). However, the existence of other pallial subdivisions is at present unclear. See text for more details. Abbreviations : AEP, anterior entopeduncular area; DP, dorsal pallium; LP, lateral pallium; MP, medial pallium; PA, pallidum; ST, striatum; VP, ventral pallium.
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In this study, we review data on the existence of comparable divisions and subdivisions in the telencephalon of different groups of tetrapods based on expression of some developmental regulatory genes, having a particular focus in the comparison of the anuran amphibian Xenopus and the mouse. The available data on Xenopus, mouse, chick and turtle in...
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... Furthermore, the presence of a homologous domain giving rise to the neocortex within the pallium territory in non-mammalian vertebrates is equally debated and little consensus exists to this day (Northcutt, 1995;Wullimann and Mueller, 2004;Medina and Abellán, 2009;Nieuwenhuys, 2009). Nevertheless, the basic core of orderly molecular and cellular processes governing anatomical and functional compartmentalization (bauplan) of the forebrain and fundamental principle of neurogenesis are conserved within the vertebrate lineage (Bachy et al., 2002;Puelles and Rubenstein, 2003;Wilson and Houart, 2004;Medina et al., 2005). Interestingly, specific cortical high-order cognitive abilities have also been mapped in teleosts (Portavella et al., 2002;Salas et al., 2003;von Trotha et al., 2014;Messina et al., 2022) and ancestral features can also be found in invertebrates (Williams et al., 2004;Cavallin et al., 2018). ...
... The genetic and molecular paradigms of the ground patterning and regionalization of the forebrain are conserved within various vertebrates (Puelles et al., 2000;Wilson and Houart, 2004;Medina et al., 2005;Murakami et al., 2005) and even in more distantly amniotes vertebrates, i.e., teleost fish (Heisenberg et al., 1996;Fernandez et al., 1998;Shinya et al., 2001;Puelles and Rubenstein, 2003;Kitagawa et al., 2004;Ganz et al., 2012). These processes have deep roots in evolution such that the molecular topography of a "paleopallium" can be traced back even to basal Bilateria (Medina and Abellán, 2009;Tomer et al., 2010). ...
The variety in the display of animals’ cognition, emotions, and behaviors, typical of humans, has its roots within the anterior-most part of the brain: the forebrain, giving rise to the neocortex in mammals. Our understanding of cellular and molecular events instructing the development of this domain and its multiple adaptations within the vertebrate lineage has progressed in the last decade. Expanding and detailing the available knowledge on regionalization, progenitors’ behavior and functional sophistication of the forebrain derivatives is also key to generating informative models to improve our characterization of heterogeneous and mechanistically unexplored cortical malformations. Classical and emerging mammalian models are irreplaceable to accurately elucidate mechanisms of stem cells expansion and impairments of cortex development. Nevertheless, alternative systems, allowing a considerable reduction of the burden associated with animal experimentation, are gaining popularity to dissect basic strategies of neural stem cells biology and morphogenesis in health and disease and to speed up preclinical drug testing. Teleost vertebrates such as zebrafish, showing conserved core programs of forebrain development, together with patients-derived in vitro 2D and 3D models, recapitulating more accurately human neurogenesis, are now accepted within translational workflows spanning from genetic analysis to functional investigation. Here, we review the current knowledge of common and divergent mechanisms shaping the forebrain in vertebrates, and causing cortical malformations in humans. We next address the utility, benefits and limitations of whole-brain/organism-based fish models or neuronal ensembles in vitro for translational research to unravel key genes and pathological mechanisms involved in neurodevelopmental diseases.
... The term " amygdala" was first used by Burdach in the early 19th century because of its almond shape in the human brain. Although its identification in other vertebrates is a challenge due to differences in shape, size, or cellular composition, homologous territories have been identified in many vertebrates [Puelles et al., 2000;Martínez-García et al., 2002;Medina et al., 2005;Reiner et al., 2005;González, 2006, 2007b;García-López et al., 2008;Martínez-García et al., 2008;Bupesh et al., 2011a, b;Medina et al., 2011;Abellán et al., 2013;Maximino et al., 2013;Biechl et al., 2017;Medina et al., 2019;Puelles et al., 2019;Porter and Mueller, 2020;Gerlach and Wullimann, an update of the tetrapartite pallial model, making this a key moment in the re-evaluation of the vertebrate pallium [Puelles, 2017], especially affecting the ventropallial derivatives and the origin of the pallial amygdala (reviewed in ). An additional proposal of hexapartite pallial organization suggests that the ventrocaudal pallium gives rise to the posterior pole of the pallial amygdala [Desfilis et al., 2018] (reviewed in Medina et al. [2021]). ...
The amygdaloid complex plays a crucial role in socio-emotional conduct, learning, survival, and reproductive behaviors. It is constituted by a set of nuclei presenting a great cellular heterogeneity and embryonic origin diversity (pallial, subpallial and even extra-telencephalic). In the last two decades, the tetrapartite pallial paradigm defined the pallial portion of the amygdala as a derivative of the lateroventral pallium. However, the pallial conception is currently being reanalyzed and one of these new proposals is to consider the mouse pallial amygdala as a radial histogenetic domain independent from the rest of the pallial subdomains. In anamniotes, and particularly in amphibian anurans, the amygdaloid complex was described as a region with pallial and subpallial components similar to those described in amniotes. In the present study carried out in Xenopus laevis, after a detailed analysis of the orientation of the amygdalar radial glia, we propose an additional amygdala derived from the pallial region. It is independent of the vomeronasal/olfactory amygdaloid nuclei described in anurans, expresses markers such as Lhx9 present in the mammalian pallial amygdala, and lacks Otp-expressing cells, detected in the adjacent medial amygdala. Further studies are needed to clarify the functional involvement of this area, and whether it is a derivative of the adjacent ventral pallium or an independent pallial domain.
... (4) The medial pallium (MP), the hippocampal primordium is indicatively identified by Lef1 and Lhx2/9 expression (Abellán et al., 2014). This tetrapartite model has been successfully applied to study pallial development in a wide range of vertebrates, including various tetrapod species (Medina et al., 2005;Puelles, 2017). Recent evidence in lacertids has proposed the existence of two additional domains, the dorsolateral and ventrocaudal pallia (Desfilis et al., 2018). ...
The telencephalon develops from the alar plate of the secondary prosencephalon and is subdivided into two distinct divisions, the pallium, which derives solely from prosomere hp1, and the subpallium which derives from both hp1 and hp2 prosomeres. In this first systematic analysis of the feline telencephalon genoarchitecture, we apply the prosomeric model to compare the expression of a battery of genes, including Tbr1, Tbr2, Pax6, Mash1, Dlx2, Nkx2-1, Lhx6, Lhx7, Lhx2 , and Emx1 , the orthologs of which alone or in combination, demarcate molecularly distinct territories in other species. We characterize, within the pallium and the subpallium, domains and subdomains topologically equivalent to those previously described in other vertebrate species and we show that the overall genoarchitectural map of the E26/27 feline brain is highly similar to that of the E13.5/E14 mouse. In addition, using the same approach at the earlier (E22/23 and E24/25) or later (E28/29 and E34/35) stages we further analyze neurogenesis, define the timing and duration of several developmental events, and compare our data with those from similar mouse studies; our results point to a complex pattern of heterochronies and show that, compared with the mouse, developmental events in the feline telencephalon span over extended periods suggesting that cats may provide a useful animal model to study brain patterning in ontogenesis and evolution.
... This is a very difficult question to answer, even after a thorough review of the bibliography, since the interspecific variations that can be found are as many as the models described. In rodents it has been reported that local inhibitory cortical interneurons represent approximately 20-30% of total neurons, and only the aspiny (or sparsely spiny) non-pyramidal cells are GABAergic neurons (Kepecs and Fishell 2014), located in all layers (Dirksen et al. 1993;Brox et al. 2003;Medina et al. 2005;Bachy and Rétaux 2006;Moreno et al. 2008a, b) and turtle (Connors and Kriegstein 1986;Blanton et al. 1987;Métin et al. 2007;Moreno et al. 2010;Tanaka and Nakajima 2012). In addition, GABAergic neurons were also observed in the pallium of other gnathostomes (Franzoni and Morino 1989;Medina et al. 1994;Veenman and Reiner 1994;Carrera et al. 2008;Mueller et al. 2008;Mueller and Guo 2009). ...
The organization of the pallial derivatives across vertebrates follows a comparable elementary arrangement, although not all of them possess a layered cortical structure as sophisticated as the cerebral cortex of mammals. However, its expansion along evolution has only been possible by the development and coevolution of the cellular networks formed by excitatory neurons and inhibitory interneurons. Thus, the comparative analysis of interneuron types in vertebrate models of key evolutionary significance will provide important information, due to the extraordinary anatomical sophistication of their interneuron systems with simpler behavioral implications. Particularly in mammals, the main consensus for classifying interneuron types is based on non-overlapping markers, which do not form a single population, but consist of several distinct classes of inhibitory cells showing co-expression of other markers. In our study, we analyzed immunohistochemically the expression of the main markers like somatostatin (SOM), parvalbumin (PV), calretinin (CR), calbindin (CB), neuropeptide Y (NPY) and/or nitric oxide synthase (NOS) at the pallial regions of three different models of Osteichthyes. First, we selected two tetrapods, one amniote from the genus Pseudemys belonging to the order Testudine, at the base of the amniote diversification and with a three-layered simple cortex, and the Anuran Xenopus laevis, an anamniote tetrapod with a non-layered evaginated pallium, and finally the order Polypteriform, a small fish group at the base of the actinopterygian diversification with an everted telencephalon. SOM was the most conserved interneuron type in terms of its distribution and co-expression with other markers such as CR, in contrast to PV, which showed a different pattern between the models analyzed. In addition, the SOM expression supports a homological relationship between the medial pallial derivatives in all the models. CR and CB expressions in the tetrapods were observed, particularly, CR expressing cells were detected in the medial and the dorsal pallial derivatives, in contrast to CB, which appeared only in discrete scattered populations. However, the pallium of Polypteriforms fishes was almost devoid of CR cells, in contrast to the important number of CB cells observed in all the pallial regions. The NPY immunoreactivity was detected in all the pallial domains of all the models, as well as cells coexpressing CR. Finally, the pallial nitrergic expression was also conserved, which allows to postulate the homological relationships between the ventropallial and the amygdaloid derivatives. In summary, even in basal pallial models the neurochemically characterized interneurons indicate that their first appearance took place before the common ancestor of amniotes. Thus, our results suggest a shared pattern of interneuron types in the pallium of all Osteichthyes.
... Regionally, there are three forebrain Dlx expression domains, shared by all four Dlx paralog genes at least transiently (Akimenko, Ekker, Wegner, Lin, & Westerfield, 1994;Brox, Puelles, Ferreiro, & Medina, 2003;Bulfone et al., 1993;Eisenstat et al., 1999;Ellies et al., 1997;Hauptmann & Gerster, 2000;Liu et al., 1997;Medina, Brox, Legaz, García-López, & Puelles, 2005;Mueller, Wullimann, & Guo, 2008;Myojin et al., 2001;Neidert, Virupannavar, Hooker, & Langeland, 2001;Papalopulu & Kintner, 1993;Puelles et al., 2000;Puelles, Martinez, Martinez-de-la-Torre, & Rubenstein, 2004;Simeone et al., 1994;Smith-Fernandez, Pieau, Repérant, Boncinelli, & Wassef, 1998). The earliest expression domain appears around E10 in a welldelimited longitudinal sector of the rostral alar forebrain, which encompasses a ventral part of the prospective alar prethalamus and extends rostralward into the subparaventricular alar hypothalamic area (Puelles, Martinez-de-la-Torre, Bardet, et al., 2012). ...
We present here a thorough and complete analysis of mouse P0‐P140 prethalamic histogenetic subdivisions and corresponding nuclear derivatives, in the context of local tract landmarks. The study used as fundamental material brains from a transgenic mouse line that expresses LacZ under the control of an intragenic enhancer of Dlx5 and Dlx6 (Dlx5/6‐LacZ). Subtle shadings of LacZ signal, jointly with pan‐DLX immunoreaction, and several other ancillary protein or RNA markers, including Calb2 and Nkx2.2 ISH (for the prethalamic eminence, and derivatives of the rostral zona limitans shell domain, respectively) were mapped across the prethalamus. The resulting model of the prethalamic region postulates tetrapartite rostrocaudal and dorsoventral subdivisions, as well as a tripartite radial stratification, each cell population showing a characteristic molecular profile. Some novel nuclei are proposed, and some instances of potential tangential cell migration were noted.
... These results suggest that different regulatory elements used by the full length Grg family members have independently of the coding sequences evolved; this may correlate with the development of spe- cific cell types or structures of the brain. Grg1, Grg2 and Grg4 expression has also been studied in the developing telencephalon of Xenopus tropicalis [51] while in Xenopus laevis only Grg4 expression has been analysed [57,58]; in these studies and at equivalent developmental stages, the expression of the Xenopus tropicalis Grg1 was broadly detected in all telencephalic areas while the expression of Xenopus tropicalis Grg2 was detected in the ventral telencephalon [51]. However, the expression of these genes was not confined in a specific zone of the telencephalon as we observe in our experiments in the mouse embryo in which Grg1 expression is restricted in the VZ and Grg2 in the SVZ and mantle zone [51]. ...
... In the developing telencephalon of Xenopus and at equivalent stages Grg4 was broadly expressed, in our experiments however, we do not observe broad distribution of the Grg4 mRNA analysed [57]. Several studies based on the analy- sis of the expression of sets of regulatory genes have established that the tetrapod telencephalon is organized into specific, comparable and molecularly distinct divisions and subdivisions [58][59][60]; however differences, such as the differences we observe in the Grg expression patterns, have been described between Xenopus and mouse for several genes and are considered to reflect modifications related to the anamniote to amniote transition [60][61][62][63]. ...
The full-length members of the Groucho/Transducin-like Enhancer of split gene family, namely Grg1-4, encode nuclear corepressors that act either directly, via interaction with transcription factors, or indirectly by modifying histone acetylation or chromatin structure. In this work we describe a detailed expression analysis of Grg1-4 family members during embryonic neurogenesis in the developing murine telencephalon. Grg1-4 presented a unique, complex yet overlapping expression pattern; Grg1 and Grg3 were mainly detected in the proliferative zones of the telencephalon, Grg2 mainly in the subpallium and finally, Grg4 mainly in the subpallial post mitotic neurons. In addition, comparative analysis of the expression of Grg1-4 revealed that, at these stages, distinct telencephalic progenitor domains or structures are characterized by the presence of different combinations of Grg repressors, thus forming a “Grg-mediated repression map”.
... Most importantly, Alu's are enriched and well-conserved within introns of CNS and developmental regulatory (DevReg) genes, suggesting they have played integral roles in primate-specific encephalization and minicolumnar expansion (although evidence is currently circumstantial and in need of further research) (Lippman et al., 2004;Polak and Domany, 2006;Casanova et al., 2017). Some of the CNS and many of the DevReg genes in question are expressed within the brain during symmetric division of radial glia, which implies that evolutionary changes to the forces that regulate their expression likewise alter radial glial number and thus minicolumn expansion and overall brain size (Buxhoeveden and Casanova, 2005b;Medina et al., 2005;Richardson et al., 2014;Pollen et al., 2015;Spocter et al., 2015). Alu elements are therefore prime candidates for effecting genetic changes within a relatively short period of time, in contrast to the more constant rate of point mutations that are the basis of the "molecular clock" (Shankar et al., 2004;Oei et al., 2004;Drake et al., 1998). ...
... An enhanced atlas of individual gene expression and regional gene signatures across the developing ectoderm Next, we provided a comprehensive quantitative atlas of individual gene expression in the single ectoderm germ layer, enhanced by NMF deconvolution. We anticipate that this repertoire will be of broad use in vertebrate embryos, given the high conservation of developmental mechanisms and gene expression patterns in vertebrates, in general, and in tetrapods, in particular [93]. We have compared the usual averaging strategies (i.e., averaging expression level between biological replicates for a given dissected region) to an unsupervised approach using NMF, designed to define homogeneous domains in the neurula ectoderm, independently of potential variations between replicate samples for a given dissected region, especially in the case of closely located regions. ...
During vertebrate neurulation, the embryonic ectoderm is patterned into lineage progenitors for neural plate, neural crest, placodes and epidermis. Here, we use Xenopus laevis embryos to analyze the spatial and temporal transcriptome of distinct ectodermal domains in the course of neurulation, during the establishment of cell lineages. In order to define the transcriptome of small groups of cells from a single germ layer and to retain spatial information, dorsal and ventral ectoderm was subdivided along the anterior-posterior and medial-lateral axes by microdissections. Principal component analysis on the transcriptomes of these ectoderm fragments primarily identifies embryonic axes and temporal dynamics. This provides a genetic code to define positional information of any ectoderm sample along the anterior-posterior and dorsal-ventral axes directly from its transcriptome. In parallel, we use nonnegative matrix factorization to predict enhanced gene expression maps onto early and mid-neurula embryos, and specific signatures for each ectoderm area. The clustering of spatial and temporal datasets allowed detection of multiple biologically relevant groups (e.g., Wnt signaling, neural crest development, sensory placode specification, ciliogenesis, germ layer specification). We provide an interactive network interface, EctoMap, for exploring synexpression relationships among genes expressed in the neurula, and suggest several strategies to use this comprehensive dataset to address questions in developmental biology as well as stem cell or cancer research.
... In general, Dlx1/2 are expressed transiently, as the postmitotic neurons pass from the ventricular to the subventricular zones, whereas Dlx5/6 are expressed in more mature neuronal differentiation stages in the overlying mantle zone, showing a protracted signal which disappears at postnatal stages (Liu et al., 1997;Eisenstat et al., 1999;Stühmer et al., 2002). Comparable Dlx expression patterns, as regards regional topography, have been described in several vertebrates [chick, turtle, Xenopus frog, zebrafish and lamprey (Dirksen et al., 1993;Papalopolu and Kintner, 1993;Akimenko et al., 1994;Smith-Fernández et al., 1998;Hauptmann and Gerster, 2000;Neidert et al., 2001;Myojin et al., 2001;Brox et al., 2003;Medina et al., 2005;Mueller et al., 2008;Kuraku et al., 2010)]. ...
... The Dlx-positive subpallium therefore includes septal, striatal, pallidal, diagonal (innominate or pallidopeduncular) and preoptic subregions. These regions stretch along the oblique (diagonal) septo-amygdaloid dimension between a septal pole and an amygdaloid pole; at the back of the telencephalon they contribute in addition to the subpallial part of the amygdala (Swanson and Petrovich, 1998;Puelles et al., 2000;Medina et al., 2005;Flames et al., 2007;García-López et al., 2008). Morphological analysis of the telencephalic subpallium in lampreys is handicapped by the apparent lack of significant cyto-or chemoarchitectonic differences across the relevant anatomical neighbourhoods, which led previous authors to be satisfied, at least provisionally, with the tentative topographic identification of only three subpallial parts: "septum," "striatum," and "preoptic area" (Heier, 1948;Schöber, 1964;Pombal et al., 1997a,b;Nieuwenhuys and Nicholson, 1998). ...
... Subpallial neurons entering the pallium differentiate as GABAergic inhibitory interneurons (Anderson et al., 1997a(Anderson et al., ,b, 1999(Anderson et al., , 2001Stühmer et al., 2002;Marín and Rubenstein, 2003), with a variety of subtypes supposed to derive from specific subpallial progenitor domains (Flames et al., 2007). Such a tangential migration of prospective pallial inhibitory interneurons now seems generally present in vertebrates, since Dlx-positive neurons co-localized with GABA-immunoreactive or GAD-67-expressing cells were observed in the frog pallium and olfactory bulb (Dirksen et al., 1993;Brox et al., 2003;Medina et al., 2005) and GABAergic neurons are widely observed in the pallium of gnathostomes (Franzoni and Morino, 1989;Medina et al., 1994;Veenman and Reiner, 1994;Brox et al., 2003;Carrera et al., 2008;Mueller et al., 2008;Mueller and Guo, 2009). GABA-ir neurons are also present in the lamprey olfactory bulb , the dorsal and ventral parts of the lateral pallium (Pombal et al., 1997a;Meléndez-Ferro et al., 2002), and other pallial areas such as the classical medial pallium, both at larval and adult stages (Pombal and Puelles, 1999;Pombal, unpublished observations; see also Meléndez-Ferro, 2001;Robertson et al., 2007). ...
... Montiel and Molnár (2013) assert that some constitutive genes (such as the 21 glutamate receptor genes) are very likely overrepresented in the sample and may not refer to developmental patterning processes. Furthermore, Chen et al. (2013) did not use any early markers that distinguish between different pallial regions in several species (Brox et al., 2004;Medina et al., 2005Medina et al., , 2011, which makes it difficult to assess homologies of the distinct pallial components in other vertebrates. Thus, Montiel and Molnár (2013) highlight the differences with other gene mapping and cell migration studies (Fernández et al., 1998;Redies et al., 2001;Nomura et al., 2008;Medina and Abellán, 2009;Medina et al., 2011; see also Puelles et al., 1999Puelles et al., , 2000, and propose that similarity in gene expression profiles between say, the nidopallium and parts of the hyperpallium, could more easily be explained by the parallel or convergent recruitment of similar developmental programs in these regions (see also Aboitiz, 2011;Medina et al., 2013). ...
The anatomical organization of the mammalian neocortex stands out among vertebrates for its laminar and columnar arrangement, featuring vertically oriented, excitatory pyramidal neurons. The evolutionary origin of this structure is discussed here in relation to the brain organization of other amniotes, i.e., the sauropsids (reptiles and birds). Specifically, we address the developmental modifications that had to take place to generate the neocortex, and to what extent these modifications were shared by other amniote lineages or can be considered unique to mammals. In this article, we propose a hypothesis that combines the control of proliferation in neural progenitor pools with the specification of regional morphogenetic gradients, yielding different anatomical results by virtue of the differential modulation of these processes in each lineage. Thus, there is a highly conserved genetic and developmental battery that becomes modulated in different directions according to specific selective pressures. In the case of early mammals, ecological conditions like nocturnal habits and reproductive strategies are considered to have played a key role in the selection of the particular brain patterning mechanisms that led to the origin of the neocortex.
