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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

Above, dorsal and ventral patterning centers in the cerebral hemispheres, and presumed ancestral condition. The dorsally located cortical hem (CH) expresses dorsalizing factors like Wnts and Emxs and patterns the embryonic medial pallium (MP, hippocampal formation and homologous structures) and the dorsal pallium (DP, neocortex in mammals; dorsal cortex/hyperpallium in sauropsids). On the other hand, the antihem, induced by Pax6 activity, specifies the ventral pallium (pallial amygdala in mammals, DVR/nidopallium in sauropsids). Pax 6 is expressed in a anteroventral-to-caudodorsal gradient that counteracts with the dorsalizing factors, and contributes also to neocortical and hippocampal patterning in mammals. In the common ancestor, perhaps similar of present-day amphibians, there was possibly a relatively large dorsal pallium, at the expense of the development of other pallial regions (Northcutt, 2013). Below, hypothetical scenario of developmental evolution in the pallium of amniotes. Pax6 is proposed here as a candidate to drive the amplification of progenitor proliferation in the brains of different amniotes, but there may be other or additional factors contributing to this process. Pax6 expression is proposed to have been upregulated in both sauropsids and mammals. In reptiles, this event produced a modest amplification of the antihem (AH) and the ventral pallium (VP), giving rise to the dorsal ventricular ridge. In birds, Pax6 amplification reached higher levels, expanding the nidopallium and mesopallium, and also reaching the DP, contributing to generate the hyperpallium. Conversely, in mammals, in addition to Pax6 enhancement there was a concomitant upregulation of dorsal signals (illustrated by an increase in Wnt and Emx activities), which antagonized Pax6 signaling, restricting the expansion of the antihem. Furthermore, in mammals, upregulation of Pax6 and dorsal signals show a significant overlap, allowing Pax6 to influence the expansion of the DP, giving rise to the neocortex. Not shown for simplicity is the anterior forebrain, patterned by the action of FGFs, which may have also contributed to brain expansion particularly in mammals. Note that the subpallium also increased in size in all amniotes. SP, subpallium, marked by the expression of markers like Dlx1/2.
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Figure 3: Above, dorsal and ventral patterning centers in the cerebral hemispheres, and presumed ancestral condition. The dorsally located cortical hem (CH) expresses dorsalizing factors like Wnts and Emxs and patterns the embryonic medial pallium (MP, hippocampal formation and homologous structures) and the dorsal pallium (DP, neocortex in mammals; dorsal cortex/hyperpallium in sauropsids). On the other hand, the antihem, induced by Pax6 activity, specifies the ventral pallium (pallial amygdala in mammals, DVR/nidopallium in sauropsids). Pax 6 is expressed in a anteroventral-to-caudodorsal gradient that counteracts with the dorsalizing factors, and contributes also to neocortical and hippocampal patterning in mammals. In the common ancestor, perhaps similar of present-day amphibians, there was possibly a relatively large dorsal pallium, at the expense of the development of other pallial regions (Northcutt, 2013). Below, hypothetical scenario of developmental evolution in the pallium of amniotes. Pax6 is proposed here as a candidate to drive the amplification of progenitor proliferation in the brains of different amniotes, but there may be other or additional factors contributing to this process. Pax6 expression is proposed to have been upregulated in both sauropsids and mammals. In reptiles, this event produced a modest amplification of the antihem (AH) and the ventral pallium (VP), giving rise to the dorsal ventricular ridge. In birds, Pax6 amplification reached higher levels, expanding the nidopallium and mesopallium, and also reaching the DP, contributing to generate the hyperpallium. Conversely, in mammals, in addition to Pax6 enhancement there was a concomitant upregulation of dorsal signals (illustrated by an increase in Wnt and Emx activities), which antagonized Pax6 signaling, restricting the expansion of the antihem. Furthermore, in mammals, upregulation of Pax6 and dorsal signals show a significant overlap, allowing Pax6 to influence the expansion of the DP, giving rise to the neocortex. Not shown for simplicity is the anterior forebrain, patterned by the action of FGFs, which may have also contributed to brain expansion particularly in mammals. Note that the subpallium also increased in size in all amniotes. SP, subpallium, marked by the expression of markers like Dlx1/2.

Mentions: Attempting to interpret some of the apparently discrepant evidences shown above, we proposed a neuro-developmental model of the amniote brain, taking into account the recent evidence of the patterning effect of distinct and evolutionarily conserved morphogenetic centers, located in the dorsomedial hemisphere (the cortical hem), the anterior and ventral forebrain (anterior neural ridge-related to olfactory placodes, and septal region in later stages), and the lateral hemisphere (the antihem; Figure 3; Hoch et al., 2009; Medina and Abellán, 2009; Aboitiz, 2011; Alfano and Studer, 2013). As most of the evidence on these signaling centers and their activity has been collected in the mouse neocortex, we will make a brief summary of these studies in order to provide the appropriate context. When referring to other brain regions or to nonmammalian specie it will be clearly stated.


Neural progenitors, patterning and ecology in neocortical origins.

Aboitiz F, Zamorano F - Front Neuroanat (2013)

Above, dorsal and ventral patterning centers in the cerebral hemispheres, and presumed ancestral condition. The dorsally located cortical hem (CH) expresses dorsalizing factors like Wnts and Emxs and patterns the embryonic medial pallium (MP, hippocampal formation and homologous structures) and the dorsal pallium (DP, neocortex in mammals; dorsal cortex/hyperpallium in sauropsids). On the other hand, the antihem, induced by Pax6 activity, specifies the ventral pallium (pallial amygdala in mammals, DVR/nidopallium in sauropsids). Pax 6 is expressed in a anteroventral-to-caudodorsal gradient that counteracts with the dorsalizing factors, and contributes also to neocortical and hippocampal patterning in mammals. In the common ancestor, perhaps similar of present-day amphibians, there was possibly a relatively large dorsal pallium, at the expense of the development of other pallial regions (Northcutt, 2013). Below, hypothetical scenario of developmental evolution in the pallium of amniotes. Pax6 is proposed here as a candidate to drive the amplification of progenitor proliferation in the brains of different amniotes, but there may be other or additional factors contributing to this process. Pax6 expression is proposed to have been upregulated in both sauropsids and mammals. In reptiles, this event produced a modest amplification of the antihem (AH) and the ventral pallium (VP), giving rise to the dorsal ventricular ridge. In birds, Pax6 amplification reached higher levels, expanding the nidopallium and mesopallium, and also reaching the DP, contributing to generate the hyperpallium. Conversely, in mammals, in addition to Pax6 enhancement there was a concomitant upregulation of dorsal signals (illustrated by an increase in Wnt and Emx activities), which antagonized Pax6 signaling, restricting the expansion of the antihem. Furthermore, in mammals, upregulation of Pax6 and dorsal signals show a significant overlap, allowing Pax6 to influence the expansion of the DP, giving rise to the neocortex. Not shown for simplicity is the anterior forebrain, patterned by the action of FGFs, which may have also contributed to brain expansion particularly in mammals. Note that the subpallium also increased in size in all amniotes. SP, subpallium, marked by the expression of markers like Dlx1/2.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: Above, dorsal and ventral patterning centers in the cerebral hemispheres, and presumed ancestral condition. The dorsally located cortical hem (CH) expresses dorsalizing factors like Wnts and Emxs and patterns the embryonic medial pallium (MP, hippocampal formation and homologous structures) and the dorsal pallium (DP, neocortex in mammals; dorsal cortex/hyperpallium in sauropsids). On the other hand, the antihem, induced by Pax6 activity, specifies the ventral pallium (pallial amygdala in mammals, DVR/nidopallium in sauropsids). Pax 6 is expressed in a anteroventral-to-caudodorsal gradient that counteracts with the dorsalizing factors, and contributes also to neocortical and hippocampal patterning in mammals. In the common ancestor, perhaps similar of present-day amphibians, there was possibly a relatively large dorsal pallium, at the expense of the development of other pallial regions (Northcutt, 2013). Below, hypothetical scenario of developmental evolution in the pallium of amniotes. Pax6 is proposed here as a candidate to drive the amplification of progenitor proliferation in the brains of different amniotes, but there may be other or additional factors contributing to this process. Pax6 expression is proposed to have been upregulated in both sauropsids and mammals. In reptiles, this event produced a modest amplification of the antihem (AH) and the ventral pallium (VP), giving rise to the dorsal ventricular ridge. In birds, Pax6 amplification reached higher levels, expanding the nidopallium and mesopallium, and also reaching the DP, contributing to generate the hyperpallium. Conversely, in mammals, in addition to Pax6 enhancement there was a concomitant upregulation of dorsal signals (illustrated by an increase in Wnt and Emx activities), which antagonized Pax6 signaling, restricting the expansion of the antihem. Furthermore, in mammals, upregulation of Pax6 and dorsal signals show a significant overlap, allowing Pax6 to influence the expansion of the DP, giving rise to the neocortex. Not shown for simplicity is the anterior forebrain, patterned by the action of FGFs, which may have also contributed to brain expansion particularly in mammals. Note that the subpallium also increased in size in all amniotes. SP, subpallium, marked by the expression of markers like Dlx1/2.
Mentions: Attempting to interpret some of the apparently discrepant evidences shown above, we proposed a neuro-developmental model of the amniote brain, taking into account the recent evidence of the patterning effect of distinct and evolutionarily conserved morphogenetic centers, located in the dorsomedial hemisphere (the cortical hem), the anterior and ventral forebrain (anterior neural ridge-related to olfactory placodes, and septal region in later stages), and the lateral hemisphere (the antihem; Figure 3; Hoch et al., 2009; Medina and Abellán, 2009; Aboitiz, 2011; Alfano and Studer, 2013). As most of the evidence on these signaling centers and their activity has been collected in the mouse neocortex, we will make a brief summary of these studies in order to provide the appropriate context. When referring to other brain regions or to nonmammalian specie it will be clearly stated.

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