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Patterns of neuronal migration in the developing mammalian and avian pallium. (A, A′) Radial migration of cortical neurons labeled by electroporation of green fluorescent protein (GFP)-expression vector in E17.5 mouse cortex display a bipolar shape. (B, B′) Migrating neurons in E9 quail dorsal pallium display a multi-polar shape. (C) Schematic illustration showing morphological differences of radial glial cells (RG) and migrating neurons (N) in the absence (left) or the presence (right) of Reelin-positive cells. (D, D′) The straight projection of radial fibers and a bipolar-shape migrating neurons in Dbx1-overexpressed pallium, where a large number of Reelin-positive cells are induced (Nomura et al. 2008).
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The mammalian cerebral cortex has a remarkable laminated structure, which is derived from the pallium, the dorsal part of the embryonic telencephalon. Recent studies indicate that the pallium is developed as a homologous structure in all vertebrate species. However, the cellular and molecular mechanism for making architectural diversity of the pall...
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During embryonic development of brain laminated structures, the protein Reelin, secreted into the extracellular matrix of the cortex and hippocampus by Cajal-Retzius (CR) cells located in the marginal zone, contributes to the regulation of migration and positioning of cortical and hippocampal neurons that do not synthesize Reelin. Soon after birth,...
Citations
... We have previously shown species-specific patterns of neuronal migration in the developing amniote pallium, among which the sequential production of excitatory neuron subtypes and the locomotive mode of neuronal migration are unique characteristics of the developing mammalian neocortex 37 . It has also been reported that NICD controls the radial migration of cortical neurons downstream of Reelin signaling 39 , which is greatly amplified in the developing mammalian neocortex 50 . Thus, we suggest that the temperature robustness of Notch . ...
Ambient temperature significantly affects developmental timing in animals. The temperature sensitivity of embryogenesis is generally believed to be a consequence of the thermal dependency of cellular metabolism. However, the adaptive molecular mechanisms that respond to variations in temperature remain unclear. Here, we report species-specific thermal sensitivity of Notch signaling in the developing amniote brain. Transient hypothermic conditions increase canonical Notch activity and reduce neurogenesis in chick neural progenitors. Increased biosynthesis of phosphatidylethanolamine, a major glycerophospholipid components of the plasma membrane, mediates hypothermia-induced Notch activation. Furthermore, the species-specific thermal dependency of Notch signaling is associated with developmental robustness to altered Notch signaling. Our results reveal unique regulatory mechanisms for temperature-dependent neurogenic potentials that underlie developmental and evolutionary adaptations to a range of ambient temperatures in amniotes.
... Functionally, CR cells have been defined as the first generated and essential pioneering cortical neurons that control neuronal migration, cell positioning, layer formation, and arealization in the cortex of mammals Barber et al., 2015]. Although evolutionarily they have often been related to cortical origin [Nomura et al., 2008[Nomura et al., , 2009Montiel et al., 2016;Goffinet, 2017], it has not been shown how. And, in those models in which there are no stratified cortical structures, the exact function of these cells remains a mystery, though it seems that their number and morphological complexity increases parallel to that of the neocortex [Villar-Cerviño et al., 2013]. ...
... DOI: 10.1159/000519025 (present results). However, an in-depth and detailed analysis of a cohort of CR markers and their putative areas of origin in the brain was not available, despite the fact that there has been much discussion about the participation of these cells in the evolution of the mammalian cortex [Nomura et al., 2008[Nomura et al., , 2009Puelles, 2011;Goffinet, 2017]. From an evolutionary perspective, several questions immediately arise with regard to CR cells, such as: Can CR cells be defined in species without layered cortical organization? ...
... Based on gene expression analysis in birds and reptiles, it has been proposed that at least a hippocampal precursor was present in the cortical bauplan of early amniotes [Puelles et al., 2001;Pombal et al., 2009;Abellán et al., 2014;Hevner, 2016] and therefore, it should probably include a cortical hem signaling center. In both birds and reptiles, a hem has been described as rudimentary and very tiny [Cabrera-Socorro et al., 2007;Medina and Abellán, 2009], and cortical hem specific markers, such as Wnt5 [Nomura et al., 2020], cWnt8b [Abellán et al., 2014;Nomura et al., 2020], and p73 [Cabrera-Socorro et al., 2007] have been detected, as well as Reln+ cells scattered in the pallium Goffinet et al., 1999;Bar et al., 2000;Bernier, 2000;Tissir et al., 2003;Cabrera-Socorro et al., 2007;Nomura et al., 2008Nomura et al., , 2009Nomura et al., , 2013Medina and Abellán, 2009]. In this context, in an-Brain Behav Evol DOI: 10.1159/000519025 urans, similarly as described in mammals [Godbole et al., 2017], the Lhx2 [Moreno et al., 2004] and Pax6 [Moreno et al., 2008a] expressions resemble the medial versus ventral pattern implicated in the notion of dorsoventral patterning of the pallium. ...
Cajal-Retzius cells are essential for cortical development in mammals, and their involvement in the evolution of this structure has been widely postulated, but very little is known about their progenitor domains in non-mammalian vertebrates. Using in situhybridization and immunofluorescence techniques we analyzed the expression of some of the main Cajal-Retzius cell markers such as Dbx1, Ebf3, ER81, Lhx1, Lhx5, p73, Reelin, Wnt3a, Zic1, and Zic2 in the forebrain of the anuran Xenopus laevis, because amphibians are the only class of anamniote tetrapods and show a tetrapartite evaginated pallium, but no layered or nuclear organization. Our results suggested that the Cajal-Retzius cell progenitor domains were comparable to those previously described in amniotes. Thus, at dorsomedial telencephalic portions a region comparable to the cortical hem was defined in Xenopus based on the expression of Wnt3a, p73, Reelin, Zic1, and Zic2. In the septum, two different domains were observed: a periventricular dorsal septum, at the limit between the pallium and the subpallium, expressing Reelin, Zic1, and Zic2, and a related septal domain, expressing Ebf3, Zic1, and Zic2. In the lateral telencephalon, the ventral pallium next to the pallio-subpallial boundary, the lack of Dbx1 and the unique expression of Reelin during development defined this territory as the most divergent with respect to mammals. Finally, we also analyzed the expression of these markers at the prethalamic eminence region, suggested as Cajal-Retzius progenitor domain in amniotes, observing there Zic1, Zic2, ER81, and Lhx1 expression. Our data show that in anurans there are different subtypes and progenitor domains of Cajal-Retzius cells, which probably contribute to the cortical regional specification and territory-specific properties. This supports the notion that the basic organization of pallial derivatives in vertebrates follows a comparable fundamental arrangement, even in those that do not have a sophisticated stratified cortical structure like the mammalian cerebral cortex.
... This reduced Reelin expression apparently results from the lack of CR cells originated from the cortical hem or ventral pallium (Bielle et al., 2005;Cabrera-Socorro et al., 2007). It has been shown that the increase of Reelin expressing cells in the avian dorsal cortex through experimental manipulation modifies the RGC fibers organization and the patterns of neuronal migration, suggesting that the increase of Reelin signaling was a key step in the evolution of the mammalian neocortex (Nomura et al., 2008(Nomura et al., , 2009. ...
The remarkable sensory, motor, and cognitive abilities of mammals mainly depend on the neocortex. Thus, the emergence of the six-layered neocortex in reptilian ancestors of mammals constitutes a fundamental evolutionary landmark. The mammalian cortex is a columnar epithelium of densely packed cells organized in layers where neurons are generated mainly in the subventricular zone in successive waves throughout development. Newborn cells move away from their site of neurogenesis through radial or tangential migration to reach their specific destination closer to the pial surface of the same or different cortical area. Interestingly, the genetic programs underlying neocortical development diversified in different mammalian lineages. In this work, I will review several recent studies that characterized how distinct transcriptional programs relate to the development and functional organization of the neocortex across diverse mammalian lineages. In some primates such as the anthropoids, the neocortex became extremely large, especially in humans where it comprises around 80% of the brain. It has been hypothesized that the massive expansion of the cortical surface and elaboration of its connections in the human lineage, has enabled our unique cognitive capacities including abstract thinking, long-term planning, verbal language and elaborated tool making capabilities. I will also analyze the lineage-specific genetic changes that could have led to the modification of key neurodevelopmental events, including regulation of cell number, neuronal migration, and differentiation into specific phenotypes, in order to shed light on the evolutionary mechanisms underlying the diversity of mammalian brains including the human brain.
... However, the appearance of the six-layered neocortex cannot be accounted for by just one single change at the level of expression of any molecule. As shown by avian in ovo experiments, an indirect experimental increase of reelin signaling in quail embryos did not modify the neurogenic distribution of pallial neurons (Nomura et al., 2008a;. No glial-aided locomotion was found, and pallial neurons remained located following the usual outside-in gradient of distribution. ...
Most neurons in the central nervous system assemble to circuits and function in a location that is different from their site of origin. Neuronal migration has strong implications in brain development, and the way the migratory patterns evolved brought major consequences on brain evolution. Here, we review the impact that the two main modes neuronal migration had on vertebrate brain diversity and function. First, radial migration enabled a more efficient production of neurons from the limited proliferative sector and promoted the efficient rearrangement of internal circuits. And second, tangential migration influenced brain evolution at several levels, such as diversifying neuronal types, enhancing network computational capabilities, shifting developmental programs on distant regions, and promoting novel wiring scenarios. We review the evolving modes of neuronal migration that sculpted and diversified vertebrate brains and how they substantially increased brain complexity over vertebrate evolution.
... CSF is free to diffuse across the CSF-brain interface into the ventricular zone and stimulate the stem and progenitor cells directly. Subarachnoid CSF stimulates migration and this is probably through stimulation of pial meningeal and Cajal-Retzius cells and the associated Reelin pathway involved in migration [130][131][132][133]. Unrestricted diffusion of CSF into the brain would likely produce abnormal migration with the mix of signal molecules produced. ...
The central nervous system develops around a fluid filled space which persists in the adult within the ventricles, spinal canal and around the outside of the brain and spinal cord. Ventricular fluid is known to act as a growth medium and stimulator of proliferation and differentiation to neural stem cells but the role of CSF in the subarachnoid space has not been fully investigated except for its role in the recently described "glymphatic" system. Fundamental changes occur in the control and coordination of CNS development upon completion of brain stem and spinal cord development and initiation of cortical development. These include changes in gene expression, changes in fluid and fluid source from neural tube fluid to cerebrospinal fluid (CSF), changes in fluid volume, composition and fluid flow pathway, with exit of high volume CSF into the subarachnoid space and the critical need for fluid drainage. We used a number of experimental approaches to test a predicted critical role for CSF in development of the cerebral cortex in rodents and humans. Data from fetuses affected by spina bifida and/or hydrocephalus are correlated with experimental evidence on proliferation and migration of cortical cells from the germinal epithelium in rodent neural tube defects, as well as embryonic brain slice experiments demonstrating a requirement for CSF to contact both ventricular and pial surfaces of the developing cortex for normal proliferation and migration. We discuss the possibility that complications with the fluid system are likely to underlie developmental disorders affecting the cerebral cortex as well as function and integrity of the cortex throughout life.
... 28,83 The TeO of the chicken brain is particularly interesting to study the role of THs in the process of neuro-and gliogenesis, since it displays several features of cortical development and shares a similar cytoarchitecture, such as the occurrence of layers, expression of the TH-responsive gene RELN (encoding reelin) and an inside-out developmental gradient. 84 Furthermore, both neurons and glial cells arise from a common progenitor during embryonic TeO development, giving rise to a structure that is essentially mature prior to hatching at E20. [85][86][87] KD of MCT8 in TeO neural progenitors as early as E3 reduced intracellular TH signalling, decreased NSC proliferation, and caused a premature depletion of the progenitor cell pool, resulting in cellular hypoplasia at later stages. Consequently, glutamatergic and GABAergic neuronal populations were smaller, possibly disrupting the TeO visual processing function. ...
In the vertebrate brain, neural stem cells (NSCs) generate both neuronal and glial cells throughout life. However, their neuro‐ and gliogenic capacity changes as a function of the developmental context. Despite the growing body of evidence on the variety of intrinsic and extrinsic factors regulating NSC physiology, their precise cellular and molecular actions are not fully determined. Our review focuses on thyroid hormone (TH), a vital component for both development and adult brain function that regulates NSC biology at all stages. First, we review comparative data to analyse how TH modulates neuro‐ and gliogenesis during vertebrate brain development. Second, as the mammalian brain is the most studied, we highlight the molecular mechanisms underlying TH action in this context. Lastly, we explore how the interplay between TH signalling and cell metabolism governs both neurodevelopmental and adult neurogenesis. We conclude that, together, TH and cellular metabolism regulate optimal brain formation, maturation and function from early foetal life to adult in vertebrate species.
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... Another marker, PCP4, showed intense labeling of subregions in chicken and zebra finch that correspond to AD and AId in our study. However, PCP4 and ER81 are also expressed in the basolateral amygdala of mammals, a pallial derivative, and not exclusively in layer V neurons (Jarvis et al., 2013;Nomura, Hattori, & Osumi, 2009). One explanation for this could be that the pallial amygdala is an extension of cortex layers V and VI, and therefore shares the expression of the same marker genes (Swanson, 2000). ...
Abstract
At the beginning of the 20th century it was suggested that a complex group of nuclei in the avian posterior ventral telencephalon is comparable to the mammalian amygdala. Subsequent findings,
however, revealed that most of these structures share premotor characteristics, while some indeed constitute the avian amygdala. These developments resulted in 2004 in a change of nomenclature
of these nuclei, which from then on were named arcopallial or amygdala nuclei and referred to as the arcopallium/amygdala complex. The structural basis for the similarities between avian and
mammalian arcopallial and amygdala subregions is poorly understood. Therefore, we analyzed binding site densities for glutamatergic AMPA, NMDA and kainate, GABAergic GABAA, muscarinic M1, M2 and nicotinic acetylcholine (nACh; a4b2 subtype), noradrenergic a1 and a2, serotonergic 5-HT1A and dopaminergic D1/5 receptors using quantitative in vitro receptor autoradiography combined with a detailed analysis of the cyto- and myelo-architecture. Our approach supports a segregation of the pigeon’s arcopallium/amygdala complex into the following subregions: the arcopallium anterius (AA), the arcopallium ventrale (AV), the arcopallium dorsale (AD), the arcopallium intermedium (AI), the arcopallium mediale (AM), the arcopallium posterius (AP), the nucleus posterioris amygdalopallii pars basalis (PoAb) and pars compacta (PoAc), the nucleus taeniae amgygdalae (TnA) and the area subpallialis amygdalae (SpA). Some of these subregions showed further subnuclei and each region of the arcopallium/amygdala complex are characterized by a distinct multireceptor density expression. Here we provide a new detailed map of the pigeon’s arcopallium/amygdala complex and compare the receptor architecture of the subregions to their possible mammalian
counterparts.
KEYWORDS
amygdala, arcopallium, avian, autoradiography, receptor
... Electroporation of an pRFP-MCT8-RNAi vector has also been used to target neural progenitors of the chicken optic tectum (Fig. 3), a mesencephalic layered structure which serves as a model for the mammalian cerebral cortex (LaVail and Cowan, 1971;Lever et al., 2014;Nomura et al., 2009). The rationale behind a possible early role of MCT8 in corticogenesis was dual. ...
Monocarboxylate transporter 8 (MCT8) facilitates transmembrane transport of thyroid hormones (THs) ensuring their action on gene expression during vertebrate neurodevelopment. A loss of MCT8 in humans results in severe psychomotor deficits associated with the Allan-Herndon-Dudley Syndrome (AHDS). However, where and when exactly a lack of MCT8 causes the neurological manifestations remains unclear because of the varying expression pattern of MCT8 between specific brain regions and cells. Here, we elaborate on the animal models that have been generated to elucidate the mechanisms underlying MCT8-deficient brain development. The absence of a clear neurological phenotype in Mct8 knockout mice made it clear that a single species would not suffice. The evolutionary conservation of TH action on neurodevelopment as well as the components regulating TH signalling however offers the opportunity to answer different aspects of MCT8 function in brain development using different vertebrate species. Moreover, the plethora of tools for genome editing available today facilitates gene silencing in these animals as well. Studies in the recently generated mct8-deficient zebrafish and Mct8/Oatp1c1 double knockout mice have put forward the current paradigm of impaired TH uptake at the level of the blood-brain barrier during peri- and postnatal development as being the main pathophysiological mechanism of AHDS. RNAi vector-based, cell-specific induction of MCT8 knockdown in the chicken embryo points to an additional function of MCT8 at the level of the neural progenitors during early brain development. Future studies including also additional in vivo models like Xenopus or in vitro approaches such as induced pluripotent stem cells will continue to help unravelling the exact role of MCT8 in developmental events. In the end, this multispecies approach will lead to a unifying thesis regarding the cellular and molecular mechanisms responsible for the neurological phenotype in AHDS patients.
... Another marker, PCP4, showed intense labeling of subregions in chicken and zebra finch that correspond to AD and AId in our study. However, PCP4 and ER81 are also expressed in the basolateral amygdala of mammals, a pallial derivative, and not exclusively in layer V neurons (Jarvis et al., 2013;Nomura, Hattori, & Osumi, 2009). One explanation for this could be that the pallial amygdala is an extension of cortex layers V and VI, and therefore shares the expression of the same marker genes (Swanson, 2000). ...
At the beginning of the 20th century it was suggested that a complex group of nuclei in the avian posterior ventral telencephalon is comparable to the mammalian amygdala. Subsequent findings, however, revealed that most of these structures share premotor characteristics, while some indeed constitute the avian amygdala. These developments resulted in 2004 in a change of nomenclature of these nuclei, which from then on were named arcopallial or amygdala nuclei and referred to as the arcopallium/amygdala complex. The structural basis for the similarities between avian and mammalian arcopallial and amygdala subregions is poorly understood. Therefore, we analyzed binding site densities for glutamatergic AMPA, NMDA and kainate, GABAergic GABAA, muscarinic M1, M2 and nicotinic acetylcholine (nACh; α4β2 subtype), noradrenergic α1 and α2, serotonergic 5-HT1A and dopaminergic D1/5 receptors using quantitative in vitro receptor autoradiography combined with a detailed analysis of the cyto- and myeloarchitecture. Our approach supports a segregation of the pigeon's arcopallium/amygdala complex into the following subregions: the arcopallium anterius (AA), the arcopallium ventrale (AV), the arcopallium dorsale (AD), the arcopallium intermedium (AI), the arcopallium mediale (AM), the arcopallium posterius (AP), the nucleus posterioris amygdalopallii pars basalis (PoAb) and pars compacta (PoAc), the nucleus taeniae amgygdalae (TnA) and the area subpallialis amygdalae (SpA). Some of these subregions showed further subnuclei and each region of the arcopallium/amygdala complex is characterized by a distinct multi-receptor density expression. Here we provide a new detailed map of the pigeon's arcopallium/amygdala complex and compare the receptor architecture of the subregions to their possible mammalian counterparts. This article is protected by copyright. All rights reserved.
... However, during adulthood, HD and mesopallium only expressed FOXP1, while HA of the Wulst expressed PPAPDC1A and SEMA6A. ROR-β was only expressed in certain thalamorecipient nuclei (IHA of the Wulst, entopallium, and Field L) of the adult bird brain Nomura, Hattori, & Osumi, 2009). Thus, gene expression has supplied much detail regarding homologies of avian brain structures, but it should be noted that across species and developmental stages of the avian brain, gene expression in HD was not consistent. ...
