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Neural progenitors, patterning and ecology in neocortical origins.

Aboitiz F, Zamorano F - Front Neuroanat (2013)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Departamento de Psiquiatría, Facultad de Medicina y Centro Interdisciplinario de Neurociencia, Pontificia Universidad Católica de Chile Santiago, Chile.

ABSTRACT
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.

No MeSH data available.


Related in: MedlinePlus

Neocortical development. The deep ventricular zone (VZ) and the subventricular zone (SVZ) are the compartments where cell proliferation takes place. (A) In early cortical development, primary neural progenitors or radial glia (RG) in the VZ divide and give rise to early neurons that migrate to the preplate (PP), and then make up the embryonic subplate (SPl). (B, C) Later in development, radial glia generate intermediate progenitors (IP), that keep dividing and producing neurons into the emerging cortical plate (CP, future layers VI–II of the neocortex), in an inside-out gradient where deep layers (VI–V) are formed first and mostly derive from progenitors in the VZ, and superficial layers (IV–II) are formed later, deriving from progenitors in the SVZ. The more superficial layer (Layer I) is the remnant of the embryonic marginal zone (MZ), in which Reelin-producing Cajal-Retzius neurons are located.
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Figure 1: Neocortical development. The deep ventricular zone (VZ) and the subventricular zone (SVZ) are the compartments where cell proliferation takes place. (A) In early cortical development, primary neural progenitors or radial glia (RG) in the VZ divide and give rise to early neurons that migrate to the preplate (PP), and then make up the embryonic subplate (SPl). (B, C) Later in development, radial glia generate intermediate progenitors (IP), that keep dividing and producing neurons into the emerging cortical plate (CP, future layers VI–II of the neocortex), in an inside-out gradient where deep layers (VI–V) are formed first and mostly derive from progenitors in the VZ, and superficial layers (IV–II) are formed later, deriving from progenitors in the SVZ. The more superficial layer (Layer I) is the remnant of the embryonic marginal zone (MZ), in which Reelin-producing Cajal-Retzius neurons are located.

Mentions: The cortical plate that grows between the marginal zone and the subplate, making up the future cortical layers II–VI, develops in the already described inside-out sequence, with deep layer VI forming first, then layer V above it, then layer IV and finally the superficial layers III and II (layer I, the marginal zone, remains largely free of neurons after Cajal-Retzius cells disappear in late development, together with the subplate; for reviews, see Aboitiz et al., 2003; Rakic, 2009). Radial glia, once beleived to represent only a scaffolding for neuronal migration, have been recognized in the last years as the main neural stem and progenitor cells in development, differentiating into many cortical cell types, including excitatory neurons, astrocytes and oligodendrocytes (Malatesta and Götz, 2013). On the other hand, most inhibitory neurons originate in the subpallium and populate the developing cortex via tangential migration (Anderson et al., 1997). Radial glia has shown to be highly diverse, some producing both glia and neurons, others only glia and others only neurons (Malatesta and Götz, 2013). A recent study identified a population of radial glia that is committed to produce only neurons to the superficial layers IV-III-II (Franco et al., 2012). In the deepest ventricular zone (VZ) of the hemisphere, early progenitors divide symmetrically, increasing their number, but also make up asymmetrical divisions that give rise to a self-renewing progenitor and to a cell that differentiates into a neuron, making up the earliest radial components of the subplate and the cortical plate (deep layers). Later in development, these asymmetric divisions generate one intermediate progenitor that may remain in the VZ and migrate contributing to deep neocortical layers; or may remain above the VZ, in the subventricular zone (SVZ), and keeps dividing for one or more cell cycles, producing mostly late-born, superficial cortical neurons (see Figure 1; Tarabykin et al., 2001; Farkas and Huttner, 2008; Pontious et al., 2008). The growth of the SVZ has been associated with neocortical expansion both in development and across species (Farkas and Huttner, 2008; Pontious et al., 2008), and appears to underly the developing neocortex of all mammals, including marsupials and monotremes. On the other hand, a SVZ containing intermediate progenitors is still lacking or is minimal in most reptiles, but appears in the subpallium of crocodiles (phylogenetically close to birds) and is maximally expressed in the embryonic avian nidopallium. The SVZ is also present in the hyperpallium of some birds who have developed this structure, possibly associated to binocularity (see below; Charvet et al., 2009; Cheung et al., 2010; Heesy and Hall, 2010; Aboitiz, 2011; Ashwell and Hardman, 2012).


Neural progenitors, patterning and ecology in neocortical origins.

Aboitiz F, Zamorano F - Front Neuroanat (2013)

Neocortical development. The deep ventricular zone (VZ) and the subventricular zone (SVZ) are the compartments where cell proliferation takes place. (A) In early cortical development, primary neural progenitors or radial glia (RG) in the VZ divide and give rise to early neurons that migrate to the preplate (PP), and then make up the embryonic subplate (SPl). (B, C) Later in development, radial glia generate intermediate progenitors (IP), that keep dividing and producing neurons into the emerging cortical plate (CP, future layers VI–II of the neocortex), in an inside-out gradient where deep layers (VI–V) are formed first and mostly derive from progenitors in the VZ, and superficial layers (IV–II) are formed later, deriving from progenitors in the SVZ. The more superficial layer (Layer I) is the remnant of the embryonic marginal zone (MZ), in which Reelin-producing Cajal-Retzius neurons are located.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3824149&req=5

Figure 1: Neocortical development. The deep ventricular zone (VZ) and the subventricular zone (SVZ) are the compartments where cell proliferation takes place. (A) In early cortical development, primary neural progenitors or radial glia (RG) in the VZ divide and give rise to early neurons that migrate to the preplate (PP), and then make up the embryonic subplate (SPl). (B, C) Later in development, radial glia generate intermediate progenitors (IP), that keep dividing and producing neurons into the emerging cortical plate (CP, future layers VI–II of the neocortex), in an inside-out gradient where deep layers (VI–V) are formed first and mostly derive from progenitors in the VZ, and superficial layers (IV–II) are formed later, deriving from progenitors in the SVZ. The more superficial layer (Layer I) is the remnant of the embryonic marginal zone (MZ), in which Reelin-producing Cajal-Retzius neurons are located.
Mentions: The cortical plate that grows between the marginal zone and the subplate, making up the future cortical layers II–VI, develops in the already described inside-out sequence, with deep layer VI forming first, then layer V above it, then layer IV and finally the superficial layers III and II (layer I, the marginal zone, remains largely free of neurons after Cajal-Retzius cells disappear in late development, together with the subplate; for reviews, see Aboitiz et al., 2003; Rakic, 2009). Radial glia, once beleived to represent only a scaffolding for neuronal migration, have been recognized in the last years as the main neural stem and progenitor cells in development, differentiating into many cortical cell types, including excitatory neurons, astrocytes and oligodendrocytes (Malatesta and Götz, 2013). On the other hand, most inhibitory neurons originate in the subpallium and populate the developing cortex via tangential migration (Anderson et al., 1997). Radial glia has shown to be highly diverse, some producing both glia and neurons, others only glia and others only neurons (Malatesta and Götz, 2013). A recent study identified a population of radial glia that is committed to produce only neurons to the superficial layers IV-III-II (Franco et al., 2012). In the deepest ventricular zone (VZ) of the hemisphere, early progenitors divide symmetrically, increasing their number, but also make up asymmetrical divisions that give rise to a self-renewing progenitor and to a cell that differentiates into a neuron, making up the earliest radial components of the subplate and the cortical plate (deep layers). Later in development, these asymmetric divisions generate one intermediate progenitor that may remain in the VZ and migrate contributing to deep neocortical layers; or may remain above the VZ, in the subventricular zone (SVZ), and keeps dividing for one or more cell cycles, producing mostly late-born, superficial cortical neurons (see Figure 1; Tarabykin et al., 2001; Farkas and Huttner, 2008; Pontious et al., 2008). The growth of the SVZ has been associated with neocortical expansion both in development and across species (Farkas and Huttner, 2008; Pontious et al., 2008), and appears to underly the developing neocortex of all mammals, including marsupials and monotremes. On the other hand, a SVZ containing intermediate progenitors is still lacking or is minimal in most reptiles, but appears in the subpallium of crocodiles (phylogenetically close to birds) and is maximally expressed in the embryonic avian nidopallium. The SVZ is also present in the hyperpallium of some birds who have developed this structure, possibly associated to binocularity (see below; Charvet et al., 2009; Cheung et al., 2010; Heesy and Hall, 2010; Aboitiz, 2011; Ashwell and Hardman, 2012).

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Departamento de Psiquiatría, Facultad de Medicina y Centro Interdisciplinario de Neurociencia, Pontificia Universidad Católica de Chile Santiago, Chile.

ABSTRACT
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.

No MeSH data available.


Related in: MedlinePlus