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Evolutionary conservation of neocortical neurogenetic program in the mammals and birds.

Suzuki IK, Hirata T - Bioarchitecture (2012)

Bottom Line: In our recent study, we found the evidence showing that the evolutionary origin of the neocortical neuron subtypes predates the actual emergence of layer structure.We further demonstrated that the neocortical layer-specific neuron subtypes are arranged as mediolaterally separated domains in the chick, but not as layers in the mammalian neocortex.These animal group-specific neuronal arrangements are accomplished by spatial modulation of the neurogenetic program, suggesting an evolutionary hypothesis that the regulatory changes in the neurogenetic program innovated the mammalian specific layered neocortex.

View Article: PubMed Central - PubMed

Affiliation: Division of Brain Function; National Institute of Genetics; Graduate University for Advanced Studies (Sokendai); Mishima, Japan.

ABSTRACT
The unique innovation of the layered neocortex in mammalian evolution is believed to facilitate adaptive radiation of mammalian species to various ecological environments by furnishing high information processing ability. There are no transitional states from the non-mammalian simple brain to the mammalian multilayered neocortex, and thus it is totally a mystery so far how this brain structure has been acquired during evolution. In our recent study, we found the evidence showing that the evolutionary origin of the neocortical neuron subtypes predates the actual emergence of layer structure. Our comparative developmental analysis of the chick pallium, homologous to the mammalian neocortex, revealed that mammals and avians fundamentally share the neocortical neuron subtypes and their production mechanisms, suggesting that their common ancestor already possessed a similar neuronal repertory. We further demonstrated that the neocortical layer-specific neuron subtypes are arranged as mediolaterally separated domains in the chick, but not as layers in the mammalian neocortex. These animal group-specific neuronal arrangements are accomplished by spatial modulation of the neurogenetic program, suggesting an evolutionary hypothesis that the regulatory changes in the neurogenetic program innovated the mammalian specific layered neocortex.

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Figure 2. Animal group-specific neurogenesis in the pallium and the potential evolutionary history of pallial bioarchitecture during the evolution. (A and B) Comparison of the pallial neurogenesis between mammals and birds. The gray, green and magenta circles indicate the neural progenitor, DL and UL subtypes, respectively. The arrows indicate the neurogenetic process. (A) Spatially unbiased progression of neurogenesis constructs homogeneous layers of neuron subtypes across the mammalian neocortex. (B) The spatially biased neurogenesis constructs the mediolaterally separated subtype arrangement in the avian pallium. (C) Hypothetical evolutionary scenario of the emergence of the neocortical layer architecture. Neocortical layer-specific neuron subtypes originated from the common ancestor of the mammals and birds (purple filled star). The layered arrangement of neuron subtypes newly emerged (white star) in the mammalian lineage before the branch leading to the monotremes. Illustrations in (A and B) are reproduced with permission from reference 22.
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Figure 2: Figure 2. Animal group-specific neurogenesis in the pallium and the potential evolutionary history of pallial bioarchitecture during the evolution. (A and B) Comparison of the pallial neurogenesis between mammals and birds. The gray, green and magenta circles indicate the neural progenitor, DL and UL subtypes, respectively. The arrows indicate the neurogenetic process. (A) Spatially unbiased progression of neurogenesis constructs homogeneous layers of neuron subtypes across the mammalian neocortex. (B) The spatially biased neurogenesis constructs the mediolaterally separated subtype arrangement in the avian pallium. (C) Hypothetical evolutionary scenario of the emergence of the neocortical layer architecture. Neocortical layer-specific neuron subtypes originated from the common ancestor of the mammals and birds (purple filled star). The layered arrangement of neuron subtypes newly emerged (white star) in the mammalian lineage before the branch leading to the monotremes. Illustrations in (A and B) are reproduced with permission from reference 22.

Mentions: The neural progenitors reside in the ventricular zone surrounding the ventricle in all vertebrate brain regions. In the whole mammalian neocortex, the neuron subtypes sequentially generated from progenitors radially migrate from the ventricular zone toward the brain surface and are piled up chronologically in an inside-out fashion (Fig. 2A). Consequently, the neuronal layers are constructed in parallel with the ventricular zone over the entire neocortex. In the chick pallium, neuronal subtypes are also generated from the progenitors in the ventricular zone and migrate radially.2,24 How then is this irregular mediolateral arrangement of DL and UL subtypes achieved?


Evolutionary conservation of neocortical neurogenetic program in the mammals and birds.

Suzuki IK, Hirata T - Bioarchitecture (2012)

Figure 2. Animal group-specific neurogenesis in the pallium and the potential evolutionary history of pallial bioarchitecture during the evolution. (A and B) Comparison of the pallial neurogenesis between mammals and birds. The gray, green and magenta circles indicate the neural progenitor, DL and UL subtypes, respectively. The arrows indicate the neurogenetic process. (A) Spatially unbiased progression of neurogenesis constructs homogeneous layers of neuron subtypes across the mammalian neocortex. (B) The spatially biased neurogenesis constructs the mediolaterally separated subtype arrangement in the avian pallium. (C) Hypothetical evolutionary scenario of the emergence of the neocortical layer architecture. Neocortical layer-specific neuron subtypes originated from the common ancestor of the mammals and birds (purple filled star). The layered arrangement of neuron subtypes newly emerged (white star) in the mammalian lineage before the branch leading to the monotremes. Illustrations in (A and B) are reproduced with permission from reference 22.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3675072&req=5

Figure 2: Figure 2. Animal group-specific neurogenesis in the pallium and the potential evolutionary history of pallial bioarchitecture during the evolution. (A and B) Comparison of the pallial neurogenesis between mammals and birds. The gray, green and magenta circles indicate the neural progenitor, DL and UL subtypes, respectively. The arrows indicate the neurogenetic process. (A) Spatially unbiased progression of neurogenesis constructs homogeneous layers of neuron subtypes across the mammalian neocortex. (B) The spatially biased neurogenesis constructs the mediolaterally separated subtype arrangement in the avian pallium. (C) Hypothetical evolutionary scenario of the emergence of the neocortical layer architecture. Neocortical layer-specific neuron subtypes originated from the common ancestor of the mammals and birds (purple filled star). The layered arrangement of neuron subtypes newly emerged (white star) in the mammalian lineage before the branch leading to the monotremes. Illustrations in (A and B) are reproduced with permission from reference 22.
Mentions: The neural progenitors reside in the ventricular zone surrounding the ventricle in all vertebrate brain regions. In the whole mammalian neocortex, the neuron subtypes sequentially generated from progenitors radially migrate from the ventricular zone toward the brain surface and are piled up chronologically in an inside-out fashion (Fig. 2A). Consequently, the neuronal layers are constructed in parallel with the ventricular zone over the entire neocortex. In the chick pallium, neuronal subtypes are also generated from the progenitors in the ventricular zone and migrate radially.2,24 How then is this irregular mediolateral arrangement of DL and UL subtypes achieved?

Bottom Line: In our recent study, we found the evidence showing that the evolutionary origin of the neocortical neuron subtypes predates the actual emergence of layer structure.We further demonstrated that the neocortical layer-specific neuron subtypes are arranged as mediolaterally separated domains in the chick, but not as layers in the mammalian neocortex.These animal group-specific neuronal arrangements are accomplished by spatial modulation of the neurogenetic program, suggesting an evolutionary hypothesis that the regulatory changes in the neurogenetic program innovated the mammalian specific layered neocortex.

View Article: PubMed Central - PubMed

Affiliation: Division of Brain Function; National Institute of Genetics; Graduate University for Advanced Studies (Sokendai); Mishima, Japan.

ABSTRACT
The unique innovation of the layered neocortex in mammalian evolution is believed to facilitate adaptive radiation of mammalian species to various ecological environments by furnishing high information processing ability. There are no transitional states from the non-mammalian simple brain to the mammalian multilayered neocortex, and thus it is totally a mystery so far how this brain structure has been acquired during evolution. In our recent study, we found the evidence showing that the evolutionary origin of the neocortical neuron subtypes predates the actual emergence of layer structure. Our comparative developmental analysis of the chick pallium, homologous to the mammalian neocortex, revealed that mammals and avians fundamentally share the neocortical neuron subtypes and their production mechanisms, suggesting that their common ancestor already possessed a similar neuronal repertory. We further demonstrated that the neocortical layer-specific neuron subtypes are arranged as mediolaterally separated domains in the chick, but not as layers in the mammalian neocortex. These animal group-specific neuronal arrangements are accomplished by spatial modulation of the neurogenetic program, suggesting an evolutionary hypothesis that the regulatory changes in the neurogenetic program innovated the mammalian specific layered neocortex.

Show MeSH
Related in: MedlinePlus