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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.

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Origins of Brn2 and Er81-positive cells in the quail telencephalon.(A and B) Whole-mount (A) and coronal section (B) of E6 embryos in which GFP-expression vector were electroporated into the lateral pallium (LP). Arrow indicates the electroporated site. (C-C″) Immunohistochemistry indicates the LP-derived GFP-labeled cells express Brn2. (D–F) Whole-mount (D) and coronal sections (E and F) of the E7 telencephalon in which GFP was electroporated into the medial pallium (MP). The MP-derived GFP-positive cells (arrows) contribute to the Er81-positive region. Scale bars, 100 µm and 10 µm in whole mount and sections, respectively.
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pone-0001454-g003: Origins of Brn2 and Er81-positive cells in the quail telencephalon.(A and B) Whole-mount (A) and coronal section (B) of E6 embryos in which GFP-expression vector were electroporated into the lateral pallium (LP). Arrow indicates the electroporated site. (C-C″) Immunohistochemistry indicates the LP-derived GFP-labeled cells express Brn2. (D–F) Whole-mount (D) and coronal sections (E and F) of the E7 telencephalon in which GFP was electroporated into the medial pallium (MP). The MP-derived GFP-positive cells (arrows) contribute to the Er81-positive region. Scale bars, 100 µm and 10 µm in whole mount and sections, respectively.

Mentions: Next, we examined the origin of Er81 and Brn-2 positive neurons in the developing quail pallium. Focal electroporation of GFP gene into the distinct pallial regions at E4 revealed that the nidopallial Brn2-positive neurons were derived from the lateral pallium (Fig. 3A–C), whereas the hippocampal and arcopallial Er81-positive neurons were originated from the medial and caudal parts of the ventral pallium, respectively (Fig. 3D–F, Figure S3 and data not shown). In contrast to labeling the hem and septum, tangential neuronal migration was rarely observed in the case of labeling dorsal, lateral and ventral pallium at this stage.


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)

Origins of Brn2 and Er81-positive cells in the quail telencephalon.(A and B) Whole-mount (A) and coronal section (B) of E6 embryos in which GFP-expression vector were electroporated into the lateral pallium (LP). Arrow indicates the electroporated site. (C-C″) Immunohistochemistry indicates the LP-derived GFP-labeled cells express Brn2. (D–F) Whole-mount (D) and coronal sections (E and F) of the E7 telencephalon in which GFP was electroporated into the medial pallium (MP). The MP-derived GFP-positive cells (arrows) contribute to the Er81-positive region. Scale bars, 100 µm and 10 µm in whole mount and sections, respectively.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0001454-g003: Origins of Brn2 and Er81-positive cells in the quail telencephalon.(A and B) Whole-mount (A) and coronal section (B) of E6 embryos in which GFP-expression vector were electroporated into the lateral pallium (LP). Arrow indicates the electroporated site. (C-C″) Immunohistochemistry indicates the LP-derived GFP-labeled cells express Brn2. (D–F) Whole-mount (D) and coronal sections (E and F) of the E7 telencephalon in which GFP was electroporated into the medial pallium (MP). The MP-derived GFP-positive cells (arrows) contribute to the Er81-positive region. Scale bars, 100 µm and 10 µm in whole mount and sections, respectively.
Mentions: Next, we examined the origin of Er81 and Brn-2 positive neurons in the developing quail pallium. Focal electroporation of GFP gene into the distinct pallial regions at E4 revealed that the nidopallial Brn2-positive neurons were derived from the lateral pallium (Fig. 3A–C), whereas the hippocampal and arcopallial Er81-positive neurons were originated from the medial and caudal parts of the ventral pallium, respectively (Fig. 3D–F, Figure S3 and data not shown). In contrast to labeling the hem and septum, tangential neuronal migration was rarely observed in the case of labeling dorsal, lateral and ventral pallium at this stage.

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