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Identification of distinct telencephalic progenitor pools for neuronal diversity in the amygdala.

Hirata T, Li P, Lanuza GM, Cocas LA, Huntsman MM, Corbin JG - Nat. Neurosci. (2009)

Bottom Line: We found that Dbx1-positive cells of the ventral pallium generate the excitatory neurons of the basolateral complex and cortical amygdala nuclei.The Dbx1-positive, POA-derived population migrated specifically to the amygdala and, as defined by both immunochemical and electrophysiological criteria, generated a unique subclass of inhibitory neurons in the medial amygdala nucleus.Thus, this POA-derived population represents a previously unknown progenitor pool dedicated to the limbic system.

View Article: PubMed Central - PubMed

Affiliation: Center for Neuroscience Research, Children's National Medical Center, 111 Michigan Avenue, NW, Suite 645, Washington, DC 20010, USA.

ABSTRACT
The development of the amygdala, a central structure of the limbic system, remains poorly understood. We found that two spatially distinct and early-specified telencephalic progenitor pools marked by the homeodomain transcription factor Dbx1 are major sources of neuronal cell diversity in the mature mouse amygdala. We found that Dbx1-positive cells of the ventral pallium generate the excitatory neurons of the basolateral complex and cortical amygdala nuclei. Moreover, Dbx1-derived cells comprise a previously unknown migratory stream that emanates from the preoptic area (POA), a ventral telencephalic domain adjacent to the diencephalic border. The Dbx1-positive, POA-derived population migrated specifically to the amygdala and, as defined by both immunochemical and electrophysiological criteria, generated a unique subclass of inhibitory neurons in the medial amygdala nucleus. Thus, this POA-derived population represents a previously unknown progenitor pool dedicated to the limbic system.

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Migration from the PSB and POADiI crystals (red) were placed in either the PSB in coronal slices (a, b, n=2) or in the POA (f, g, n=4) in horizontal slices at E13.5 in Dbx1+/CreERT2;R26RYFP embryos treated with tamoxifen at E10.5. After two days in vitro (DIV), DiI labeled cells (red) from both the PSB and the POA migrate to the basal telencephalon (b, g). Boxed regions show that migratory streams from both the PSB (arrows, c-e) and POA (arrows, h-j) comprise Dbx1-derived cells as revealed by co-expression of DiI (red) and YFP (green). DiI and YFP co-expressing cells are also shown from another brain slice (arrows, k-m). β-galactosidase stained horizontal sections from E12.5 Dlx2+/tauLacZ embryos (n) and Lhx2 mRNA expression (o) also mark the PAS migratory route (double arrows, asterisk marks the POA in (o)). Scale bar in (a) for (a, b, f, g); 250 µm. Scale bar in (c) for (c-e, h-m); 50 µm. Scale bar in (n) for (n, o); 250 µm.
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Figure 5: Migration from the PSB and POADiI crystals (red) were placed in either the PSB in coronal slices (a, b, n=2) or in the POA (f, g, n=4) in horizontal slices at E13.5 in Dbx1+/CreERT2;R26RYFP embryos treated with tamoxifen at E10.5. After two days in vitro (DIV), DiI labeled cells (red) from both the PSB and the POA migrate to the basal telencephalon (b, g). Boxed regions show that migratory streams from both the PSB (arrows, c-e) and POA (arrows, h-j) comprise Dbx1-derived cells as revealed by co-expression of DiI (red) and YFP (green). DiI and YFP co-expressing cells are also shown from another brain slice (arrows, k-m). β-galactosidase stained horizontal sections from E12.5 Dlx2+/tauLacZ embryos (n) and Lhx2 mRNA expression (o) also mark the PAS migratory route (double arrows, asterisk marks the POA in (o)). Scale bar in (a) for (a, b, f, g); 250 µm. Scale bar in (c) for (c-e, h-m); 50 µm. Scale bar in (n) for (n, o); 250 µm.

Mentions: Second, we also carried out a series of DiI experiments in telencephalic slices from Dbx1+/CreERT2;R26RYFP embryos at E13.5 (Fig. 5). After two days in vitro, numerous DiI+ cells from the POA and PSB migrate toward the region of the developing amygdala (Fig. 5a,b,f,g). Many DiI+ cells from both the PSB and POA also express YFP (Fig. 5c–e, h–m), revealing that these migratory streams were comprised, at least in part, of Dbx1-derived cells. Interestingly, the PAS is also marked by expression of Dlx2+/tauLacZ and Lhx2, suggesting that this novel migratory route is comprised of a heterogeneously marked population of cells (Fig. 5n–o). Although their mode of migration remains to be fully elucidated, Dbx1-derived cells of the POA also intermingle with RC2+ radial glia, suggesting that these cells may migrate along radial glia (Supplementary Fig. 4).


Identification of distinct telencephalic progenitor pools for neuronal diversity in the amygdala.

Hirata T, Li P, Lanuza GM, Cocas LA, Huntsman MM, Corbin JG - Nat. Neurosci. (2009)

Migration from the PSB and POADiI crystals (red) were placed in either the PSB in coronal slices (a, b, n=2) or in the POA (f, g, n=4) in horizontal slices at E13.5 in Dbx1+/CreERT2;R26RYFP embryos treated with tamoxifen at E10.5. After two days in vitro (DIV), DiI labeled cells (red) from both the PSB and the POA migrate to the basal telencephalon (b, g). Boxed regions show that migratory streams from both the PSB (arrows, c-e) and POA (arrows, h-j) comprise Dbx1-derived cells as revealed by co-expression of DiI (red) and YFP (green). DiI and YFP co-expressing cells are also shown from another brain slice (arrows, k-m). β-galactosidase stained horizontal sections from E12.5 Dlx2+/tauLacZ embryos (n) and Lhx2 mRNA expression (o) also mark the PAS migratory route (double arrows, asterisk marks the POA in (o)). Scale bar in (a) for (a, b, f, g); 250 µm. Scale bar in (c) for (c-e, h-m); 50 µm. Scale bar in (n) for (n, o); 250 µm.
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Figure 5: Migration from the PSB and POADiI crystals (red) were placed in either the PSB in coronal slices (a, b, n=2) or in the POA (f, g, n=4) in horizontal slices at E13.5 in Dbx1+/CreERT2;R26RYFP embryos treated with tamoxifen at E10.5. After two days in vitro (DIV), DiI labeled cells (red) from both the PSB and the POA migrate to the basal telencephalon (b, g). Boxed regions show that migratory streams from both the PSB (arrows, c-e) and POA (arrows, h-j) comprise Dbx1-derived cells as revealed by co-expression of DiI (red) and YFP (green). DiI and YFP co-expressing cells are also shown from another brain slice (arrows, k-m). β-galactosidase stained horizontal sections from E12.5 Dlx2+/tauLacZ embryos (n) and Lhx2 mRNA expression (o) also mark the PAS migratory route (double arrows, asterisk marks the POA in (o)). Scale bar in (a) for (a, b, f, g); 250 µm. Scale bar in (c) for (c-e, h-m); 50 µm. Scale bar in (n) for (n, o); 250 µm.
Mentions: Second, we also carried out a series of DiI experiments in telencephalic slices from Dbx1+/CreERT2;R26RYFP embryos at E13.5 (Fig. 5). After two days in vitro, numerous DiI+ cells from the POA and PSB migrate toward the region of the developing amygdala (Fig. 5a,b,f,g). Many DiI+ cells from both the PSB and POA also express YFP (Fig. 5c–e, h–m), revealing that these migratory streams were comprised, at least in part, of Dbx1-derived cells. Interestingly, the PAS is also marked by expression of Dlx2+/tauLacZ and Lhx2, suggesting that this novel migratory route is comprised of a heterogeneously marked population of cells (Fig. 5n–o). Although their mode of migration remains to be fully elucidated, Dbx1-derived cells of the POA also intermingle with RC2+ radial glia, suggesting that these cells may migrate along radial glia (Supplementary Fig. 4).

Bottom Line: We found that Dbx1-positive cells of the ventral pallium generate the excitatory neurons of the basolateral complex and cortical amygdala nuclei.The Dbx1-positive, POA-derived population migrated specifically to the amygdala and, as defined by both immunochemical and electrophysiological criteria, generated a unique subclass of inhibitory neurons in the medial amygdala nucleus.Thus, this POA-derived population represents a previously unknown progenitor pool dedicated to the limbic system.

View Article: PubMed Central - PubMed

Affiliation: Center for Neuroscience Research, Children's National Medical Center, 111 Michigan Avenue, NW, Suite 645, Washington, DC 20010, USA.

ABSTRACT
The development of the amygdala, a central structure of the limbic system, remains poorly understood. We found that two spatially distinct and early-specified telencephalic progenitor pools marked by the homeodomain transcription factor Dbx1 are major sources of neuronal cell diversity in the mature mouse amygdala. We found that Dbx1-positive cells of the ventral pallium generate the excitatory neurons of the basolateral complex and cortical amygdala nuclei. Moreover, Dbx1-derived cells comprise a previously unknown migratory stream that emanates from the preoptic area (POA), a ventral telencephalic domain adjacent to the diencephalic border. The Dbx1-positive, POA-derived population migrated specifically to the amygdala and, as defined by both immunochemical and electrophysiological criteria, generated a unique subclass of inhibitory neurons in the medial amygdala nucleus. Thus, this POA-derived population represents a previously unknown progenitor pool dedicated to the limbic system.

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