Limits...
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
Origins of Reelin-positive cells in the developing quail telencephalon.(A and B) GFP-labeled cells in E4.5 quail telencephalon, in which GFP-expression vector was electroporated into the hem (A) or septum (Spt; B) at E3.5. Arrows indicate migrating GFP-positive cells. r: rostral, c: caudal. (C and C′) Expression of Reelin in the GFP-positive, hem-derived cells. (D) Coronal sections of the telencephalon in which GFP-plasmid was electroporated into the ventral pallium (VP). (E) The VP-derived GFP-positive cells (arrows) do not express Reelin. Arrowheads indicate Reelin-positive cells, which might be derived from the hem region. Scale bars, 200 µm (A, B, D), 50 µm (C, E).
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC2175532&req=5

pone-0001454-g002: Origins of Reelin-positive cells in the developing quail telencephalon.(A and B) GFP-labeled cells in E4.5 quail telencephalon, in which GFP-expression vector was electroporated into the hem (A) or septum (Spt; B) at E3.5. Arrows indicate migrating GFP-positive cells. r: rostral, c: caudal. (C and C′) Expression of Reelin in the GFP-positive, hem-derived cells. (D) Coronal sections of the telencephalon in which GFP-plasmid was electroporated into the ventral pallium (VP). (E) The VP-derived GFP-positive cells (arrows) do not express Reelin. Arrowheads indicate Reelin-positive cells, which might be derived from the hem region. Scale bars, 200 µm (A, B, D), 50 µm (C, E).

Mentions: To examine the developmental origins of Reelin, Er81 and Brn2-positive neurons in the quail telencephalon, we performed cell-tracing analysis by focal electroporation of green fluorescent protein (GFP)-expression vectors. In the developing mammalian telencephalon, Reelin-positive Cajal-Retzius cells are originated from various telencephalic regions including the cortical hem [25], [26], septum [27], ventral pallium [27] and retrobulber regions [28]. Based on these lines of evidence, we focused on the quail hem, septum and ventral pallium, and examined whether these regions generate Reelin-positive cells. When we introduce the GFP gene into the E3 and E4 quail hem or septum, a large number of GFP-positive cells migrated on the surface of the quail telencephalon from electroporated regions (hem: n = 3, septum: n = 2, Fig. 2A and 2B). Immunohistochemical studies indicated that a subset of these GFP-labeled cells expressed Reelin (Fig. 2C). The migration patterns of these GFP/Reelin-positive cells were similar to those of mammalian Cajal-Retzius cells [25]–[27]; they migrate from medial to lateral regions of the telencephalon. However, when we labeled the quail ventral pallim by electroporation, generation of Reelin-positive cells was not detected from the labeled area (n = 3, Fig. 2D and 2E). To further confirm the results of in vivo tracing, we performed explant culture of distinct brain regions and examined Reelin expression. When we isolated E3 chicken cortical hem and cultured them for 48 hours, a large number of Reelin-positive cells differentiated in the explants (n = 8, Figure S2A, S2C and S2D). In contrast, we rarely detected Reelin-positive cells in explants taken from the ventral pallium (n = 8, Figure S2B, C and D).


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 Reelin-positive cells in the developing quail telencephalon.(A and B) GFP-labeled cells in E4.5 quail telencephalon, in which GFP-expression vector was electroporated into the hem (A) or septum (Spt; B) at E3.5. Arrows indicate migrating GFP-positive cells. r: rostral, c: caudal. (C and C′) Expression of Reelin in the GFP-positive, hem-derived cells. (D) Coronal sections of the telencephalon in which GFP-plasmid was electroporated into the ventral pallium (VP). (E) The VP-derived GFP-positive cells (arrows) do not express Reelin. Arrowheads indicate Reelin-positive cells, which might be derived from the hem region. Scale bars, 200 µm (A, B, D), 50 µm (C, E).
© Copyright Policy
Related In: Results  -  Collection

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

pone-0001454-g002: Origins of Reelin-positive cells in the developing quail telencephalon.(A and B) GFP-labeled cells in E4.5 quail telencephalon, in which GFP-expression vector was electroporated into the hem (A) or septum (Spt; B) at E3.5. Arrows indicate migrating GFP-positive cells. r: rostral, c: caudal. (C and C′) Expression of Reelin in the GFP-positive, hem-derived cells. (D) Coronal sections of the telencephalon in which GFP-plasmid was electroporated into the ventral pallium (VP). (E) The VP-derived GFP-positive cells (arrows) do not express Reelin. Arrowheads indicate Reelin-positive cells, which might be derived from the hem region. Scale bars, 200 µm (A, B, D), 50 µm (C, E).
Mentions: To examine the developmental origins of Reelin, Er81 and Brn2-positive neurons in the quail telencephalon, we performed cell-tracing analysis by focal electroporation of green fluorescent protein (GFP)-expression vectors. In the developing mammalian telencephalon, Reelin-positive Cajal-Retzius cells are originated from various telencephalic regions including the cortical hem [25], [26], septum [27], ventral pallium [27] and retrobulber regions [28]. Based on these lines of evidence, we focused on the quail hem, septum and ventral pallium, and examined whether these regions generate Reelin-positive cells. When we introduce the GFP gene into the E3 and E4 quail hem or septum, a large number of GFP-positive cells migrated on the surface of the quail telencephalon from electroporated regions (hem: n = 3, septum: n = 2, Fig. 2A and 2B). Immunohistochemical studies indicated that a subset of these GFP-labeled cells expressed Reelin (Fig. 2C). The migration patterns of these GFP/Reelin-positive cells were similar to those of mammalian Cajal-Retzius cells [25]–[27]; they migrate from medial to lateral regions of the telencephalon. However, when we labeled the quail ventral pallim by electroporation, generation of Reelin-positive cells was not detected from the labeled area (n = 3, Fig. 2D and 2E). To further confirm the results of in vivo tracing, we performed explant culture of distinct brain regions and examined Reelin expression. When we isolated E3 chicken cortical hem and cultured them for 48 hours, a large number of Reelin-positive cells differentiated in the explants (n = 8, Figure S2A, S2C and S2D). In contrast, we rarely detected Reelin-positive cells in explants taken from the ventral pallium (n = 8, Figure S2B, C and D).

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