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Patterns of neurogenesis and amplitude of Reelin expression are essential for making a mammalian-type cortex.

Nomura T, Takahashi M, Hara Y, Osumi N - PLoS ONE (2008)

Bottom Line: We compared the neurogenesis in mammalian and avian pallium, focusing on subtype-specific gene expression, and found that the avian pallium generates distinct types of neurons in a spatially restricted manner.Furthermore, expression of Reelin gene is hardly detected in the developing avian pallium, and an experimental increase in Reelin-positive cells in the avian pallium modified radial fiber organization, which resulted in dramatic changes in the morphology of migrating neurons.Our results demonstrate that distinct mechanisms govern the patterns of neuronal specification in mammalian and avian pallial development, and that Reelin-dependent neuronal migration plays a critical role in mammalian type corticogenesis.

View Article: PubMed Central - PubMed

Affiliation: Division of Developmental Neuroscience, Center for Translational and Advanced Animal Research (CTTAR), Tohoku University School of Medicine, Sendai, Japan.

ABSTRACT
The mammalian neocortex is characterized as a six-layered laminar structure, in which distinct types of pyramidal neurons are distributed coordinately during embryogenesis. In contrast, no other vertebrate class possesses a brain region that is strictly analogous to the neocortical structure. Although it is widely accepted that the pallium, a dorsal forebrain region, is specified in all vertebrate species, little is known of the differential mechanisms underlying laminated or non-laminated structures in the pallium. Here we show that differences in patterns of neuronal specification and migration provide the pallial architectonic diversity. We compared the neurogenesis in mammalian and avian pallium, focusing on subtype-specific gene expression, and found that the avian pallium generates distinct types of neurons in a spatially restricted manner. Furthermore, expression of Reelin gene is hardly detected in the developing avian pallium, and an experimental increase in Reelin-positive cells in the avian pallium modified radial fiber organization, which resulted in dramatic changes in the morphology of migrating neurons. Our results demonstrate that distinct mechanisms govern the patterns of neuronal specification in mammalian and avian pallial development, and that Reelin-dependent neuronal migration plays a critical role in mammalian type corticogenesis. These lines of evidence shed light on the developmental programs underlying the evolution of the mammalian specific laminated cortex.

Show MeSH
Schematic illustration of differences in neuronal specification and migration patterns between the mammalian and avian pallium.In the developing mammalian telencephalon, Reelin-positive neurons are derived from several origins including ventral pallium, and Er81 and Brn2-positive neurons are isotopically generated from entire pallial regions in a temporal manner. In contrast, in the developing avian telencephalon, Reelin-positive neurons are not derived from the ventral pallium, and Er81 and Brn2-positive neurons are generated from distinct pallial regions in a spatially regulated manner.
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pone-0001454-g004: Schematic illustration of differences in neuronal specification and migration patterns between the mammalian and avian pallium.In the developing mammalian telencephalon, Reelin-positive neurons are derived from several origins including ventral pallium, and Er81 and Brn2-positive neurons are isotopically generated from entire pallial regions in a temporal manner. In contrast, in the developing avian telencephalon, Reelin-positive neurons are not derived from the ventral pallium, and Er81 and Brn2-positive neurons are generated from distinct pallial regions in a spatially regulated manner.

Mentions: These data indicate that in the developing avian pallium, 1) Reelin-positive cells are few in number, and not derived from the ventral pallium, and that 2) Er81 and Brn2-positive neurons are generated from distinct pallial regions in spatially restricted manner (Fig. 4). These features are markedly different from those in the mammalian cortex, in which a large number of Reelin-positive Cajal-Retzius cells is originated from several telencephalic regions, and Er81 and Brn2-positive cortical neurons are isotopically generated from the entire cortical ventricular zone in a temporally regulated manner (Fig. 4). Thus, patterns of neuronal subtype specification in the avian pallium are largely different from those in the mammalian cortex.


Patterns of neurogenesis and amplitude of Reelin expression are essential for making a mammalian-type cortex.

Nomura T, Takahashi M, Hara Y, Osumi N - PLoS ONE (2008)

Schematic illustration of differences in neuronal specification and migration patterns between the mammalian and avian pallium.In the developing mammalian telencephalon, Reelin-positive neurons are derived from several origins including ventral pallium, and Er81 and Brn2-positive neurons are isotopically generated from entire pallial regions in a temporal manner. In contrast, in the developing avian telencephalon, Reelin-positive neurons are not derived from the ventral pallium, and Er81 and Brn2-positive neurons are generated from distinct pallial regions in a spatially regulated manner.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2175532&req=5

pone-0001454-g004: Schematic illustration of differences in neuronal specification and migration patterns between the mammalian and avian pallium.In the developing mammalian telencephalon, Reelin-positive neurons are derived from several origins including ventral pallium, and Er81 and Brn2-positive neurons are isotopically generated from entire pallial regions in a temporal manner. In contrast, in the developing avian telencephalon, Reelin-positive neurons are not derived from the ventral pallium, and Er81 and Brn2-positive neurons are generated from distinct pallial regions in a spatially regulated manner.
Mentions: These data indicate that in the developing avian pallium, 1) Reelin-positive cells are few in number, and not derived from the ventral pallium, and that 2) Er81 and Brn2-positive neurons are generated from distinct pallial regions in spatially restricted manner (Fig. 4). These features are markedly different from those in the mammalian cortex, in which a large number of Reelin-positive Cajal-Retzius cells is originated from several telencephalic regions, and Er81 and Brn2-positive cortical neurons are isotopically generated from the entire cortical ventricular zone in a temporally regulated manner (Fig. 4). Thus, patterns of neuronal subtype specification in the avian pallium are largely different from those in the mammalian cortex.

Bottom Line: We compared the neurogenesis in mammalian and avian pallium, focusing on subtype-specific gene expression, and found that the avian pallium generates distinct types of neurons in a spatially restricted manner.Furthermore, expression of Reelin gene is hardly detected in the developing avian pallium, and an experimental increase in Reelin-positive cells in the avian pallium modified radial fiber organization, which resulted in dramatic changes in the morphology of migrating neurons.Our results demonstrate that distinct mechanisms govern the patterns of neuronal specification in mammalian and avian pallial development, and that Reelin-dependent neuronal migration plays a critical role in mammalian type corticogenesis.

View Article: PubMed Central - PubMed

Affiliation: Division of Developmental Neuroscience, Center for Translational and Advanced Animal Research (CTTAR), Tohoku University School of Medicine, Sendai, Japan.

ABSTRACT
The mammalian neocortex is characterized as a six-layered laminar structure, in which distinct types of pyramidal neurons are distributed coordinately during embryogenesis. In contrast, no other vertebrate class possesses a brain region that is strictly analogous to the neocortical structure. Although it is widely accepted that the pallium, a dorsal forebrain region, is specified in all vertebrate species, little is known of the differential mechanisms underlying laminated or non-laminated structures in the pallium. Here we show that differences in patterns of neuronal specification and migration provide the pallial architectonic diversity. We compared the neurogenesis in mammalian and avian pallium, focusing on subtype-specific gene expression, and found that the avian pallium generates distinct types of neurons in a spatially restricted manner. Furthermore, expression of Reelin gene is hardly detected in the developing avian pallium, and an experimental increase in Reelin-positive cells in the avian pallium modified radial fiber organization, which resulted in dramatic changes in the morphology of migrating neurons. Our results demonstrate that distinct mechanisms govern the patterns of neuronal specification in mammalian and avian pallial development, and that Reelin-dependent neuronal migration plays a critical role in mammalian type corticogenesis. These lines of evidence shed light on the developmental programs underlying the evolution of the mammalian specific laminated cortex.

Show MeSH