Selective Requirement of Pax6, But Not Emx2, in the Specification and Development of Several Nuclei of the Amygdaloid Complex

Tole, Shubha; Remedios, Ryan; Saha, Bhaskar; Stoykova, Anastassia

doi:10.1523/jneurosci.3014-04.2005

Cited by 97 publications

(211 citation statements)

References 38 publications

(73 reference statements)

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“…Although it has been suggested that the LCS provides cells to the ventrolateral neocortex, piriform cortex, endopiriform nucleus, claustrum (Bayer and Altman, 1991), and the dense cell layer of the olfactory tubercle (Tamamaki et al, 2001), little is known regarding the developmental profile of this migratory stream and the genetic factors governing its development. Here, consistent with previous studies (Stoykova et al, 1996;Puelles et al, 2000;Hirata et al, 2002;Tole et al, 2005), we show that the LCS is a heterogeneous population comprised of separate pallial Pax6 ϩ -derived and subpallial Dlx2 ϩ -derived cells. Our data also interestingly indicate that the LCS is comprised of an additional population of progenitor cells that coexpress both pallial (Pax6) and subpallial (Dlx2) markers.…”

Section: Discussionsupporting

confidence: 93%

“…Our observations in the present study are also consistent with this model, because the LCS appears to be a major source of both pallial-and subpallialderived cells of the amygdala. Furthermore, although LCS cells migrate to numerous other ventral telencephalic structures, in agreement with previous studies (Stoykova et al, 1996;Tole et al, 2005), we observe Pax6 ϩ and Dlx2 ϩ cells populating distinct subsets of developing amygdala nuclei such as the basolateral complex and basomedial and cortical nuclei. Furthermore, colocalization of both Pax6 ϩ and Dlx2 ϩ cells with the early neuronal marker TUJ1 indicates that at least some of these cells will differentiate into neurons.…”

Section: Discussionsupporting

confidence: 93%

“…This observation has lead to a model proposed by Swanson and Petrovich (1998), which hypothesized that the amygdala is comprised of both pallial-and subpallial-derived cells. Genetic and transplantation-based fate mapping of both pallial-derived (Gorski et al, 2002) and subpallial-derived (Nery et al, 2002;Stenman et al, 2003a) progenitor cells, as well as gene expression studies (Fernandez et al, 1998;Puelles et al, 1999Puelles et al, , 2000Zirlinger et al, 2001;Medina et al, 2004;Remedios et al, 2004;Tole et al, 2005), have lent significant credence to this model. Our observations in the present study are also consistent with this model, because the LCS appears to be a major source of both pallial-and subpallialderived cells of the amygdala.…”

Section: Discussionmentioning

confidence: 98%

“…This "molecular" CSB (herein referred to as CSB) is po-sitioned just ventral to the corticostriatal sulcus and also is the site of expression of a variety of specific intrinsic [e.g., Dbx1 (developing brain homeobox 1), Er81 (Ets transcription factor ER81), Sp8 (a member of the Sp1 zinc finger transcription factor gene family), and Tsh1 (Teashirt 1)] and extrinsic [e.g., Sfrp2 (secreted frizzled-related protein 2), Tgf-␣, and Fgf7] factors (Lu et al, 1996;Kim et al, 2001;Assimacopoulos et al, 2003;Stenman et al, 2003a;Caubit et al, 2005;Waclaw et al, 2006). Furthermore, gene expression studies have indicated that the LCS consists of at least two progenitor populations that arise from both the pallial and subpallial compartments (Stoykova et al, 1996;Puelles et al, 2000;Toresson et al, 2000;Yun et al, 2001;Medina et al, 2004;Tole et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

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Cell Migration along the Lateral Cortical Stream to the Developing Basal Telencephalic Limbic System

Carney¹,

Alfonso²,

Cohen³

et al. 2006

J. Neurosci.

113

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During embryogenesis, the lateral cortical stream (LCS) emerges from the corticostriatal border (CSB), the boundary between the developing cerebral cortex and striatum. The LCS is comprised of a mix of pallial-and subpallial-derived neural progenitor cells that migrate to the developing structures of the basal telencephalon, most notably the piriform cortex and amygdala. Using a combination of in vitro and in vivo approaches, we analyzed the timing, composition, migratory modes, origin, and requirement of the homeodomaincontaining transcription factor Gsh2 (genomic screened homeobox 2) in the development of this prominent migratory stream. We reveal that Pax6 (paired box gene 6)-positive pallial-derived and Dlx2 (distal-less homeobox 2)-positive subpallial-derived subpopulations of LCS cells are generated in distinct temporal windows during embryogenesis. Furthermore, our data indicate the CSB border not only is comprised of separate populations of pallial-and subpallial-derived progenitors that contribute to the LCS but also a subpopulation of cells coexpressing Pax6 and Dlx2. Moreover, despite migrating along a route outlined by a cascade of radial glia, the Dlx2-positive population appears to migrate primarily in an apparent chain-like manner, with LCS migratory cells being generated locally at the CSB with little contribution from other subpallial structures such as the medial, lateral, or caudal ganglionic eminences. We further demonstrate that the generation of the LCS is dependent on the homeodomain-containing gene Gsh2, revealing a novel requirement for Gsh2 in telencephalic development.

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Section: Discussionsupporting

confidence: 93%

Section: Discussionsupporting

confidence: 93%

Section: Discussionmentioning

confidence: 98%

Section: Introductionmentioning

confidence: 99%

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Cell Migration along the Lateral Cortical Stream to the Developing Basal Telencephalic Limbic System

Carney¹,

Alfonso²,

Cohen³

et al. 2006

J. Neurosci.

113

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“…8). Previous studies indicated that COUP-TFII is also highly expressed in the amygdaloid nucleus, which some of the CGE cells are destined to populate (Lopes da Silva et al, 1995;Nery et al, 2002;Ló pez-Bendito et al, 2004;Tole et al, 2005). We also observed that some of the calretinin-positive cells in the hippocampus are COUP-TFII positive (data not shown).…”

Section: Characteristics Of Coup-tfii-positive Interneuronssupporting

confidence: 62%

COUP-TFII Is Preferentially Expressed in the Caudal Ganglionic Eminence and Is Involved in the Caudal Migratory Stream

Kanatani¹,

Yozu²,

Tabata³

et al. 2008

J. Neurosci.

149

184

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While the cortical interneurons derived from the medial ganglionic eminence (MGE) migrate rather diffusely into the cortex, interneurons that migrate out from the caudal ganglionic eminence (CGE) mainly move caudally into the caudal cerebral cortex and the hippocampus in the form of the caudal migratory stream (CMS) (Yozu et al., 2005). Although transplantation experiments at embryonic day 13.5 had revealed that the migrating cells in these two populations are already intrinsically different in regard to their ability to respond to the CGE environment (Yozu et al., 2005), it is not known how the CGE cells are specified and how their migratory behavior is determined.In this study we showed that, although CGE and lateral ganglionic eminence (LGE) express almost the same marker molecules, LGE cells do not migrate caudally when transplanted into the CGE, suggesting that LGE cells are intrinsically different from CGE cells. We therefore compared the transcriptomes of the CGE, MGE, and LGE, and the results showed that COUP-TFII was expressed preferentially in the CGE as well as in the migrating interneurons in the CMS. Transplantation experiments revealed that COUP-TFII is sufficient to change the direction of MGE cell migration to caudal when transplanted into the CGE environment, and knockdown of COUP-TFII inhibited the caudal migration of the CGE cells. These results suggest that COUP-TFII is both required and sufficient for the CGE-cellspecific migratory behavior in the caudal direction. Thus, a locally expressed transcription factor determines the migratory direction of the cortical interneurons in a region-specific manner.

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The Olfactory Amygdala in Amniotes: An Evo‐Devo Approach

Abellán

Desfilis

Medina

2013

The Anatomical Record

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In tetrapods, the medial amygdala is a forebrain center that integrates olfactory and/or vomeronasal signals with the endocrine and autonomic systems, playing a key role in different social behaviors. The vomeronasal system has undergone important changes during evolution, which may be behind some interspecies differences in chemosensorymediated social behavior. These evolutionary changes are associated with variations in vomeronasal-recipient brain structures, including the medial amygdala. Herein, we employed an evolutionary developmental biology approach for trying to understand the function and evolution of the medial amygdala. For that purpose, we reviewed published data on fate mapping in mouse, and the expression of orthologous developmental regulatory genes (Nkx2.1, Lhx6, Shh, Tbr1, Lhx9, Lhx5, Otp, and Pax6) in embryos of mouse, chicken, emydid turtles, and a pipid frog. We also analyzed novel data on Lhx9 and Otp in a lacertid lizard. Based on distinct Abbreviations used: AAv 5 anterior amygdala, ventral part; ACo 5 anterior cortical amygdalar area; AHN 5 anterior hypothalamic nucleus; AOB 5 accessory olfactory bulb; AON 5 anterior olfactory nucleus; APH 5 parahippocampal area (chicken); Arc 5 arcopallium (part of the pallial amygdala in chicken); AStr 5 amygdalo-striatal transition area; BAOT 5 bed nucleus of the accessory olfactory bulb; Bas 5 basal nucleus (Meynert); BC 5 basal amygdalar complex; BL 5 basolateral amygdalar nucleus; BLA 5 basolateral amygdalar nucleus, anterior part; BLV 5 basolateral amygdalar nucleus, ventral part; BM 5 basomedial amygdalar nucleus; BMA 5 basomedial amygdalar nucleus, anterior part; BSTia 5 bed nucleus of the stria terminalis, intraamygdaloid part; BSTM 5 bed nucleus of the stria terminalis, medial part; BSTM1 5 dorsolateral subnucleus of BSTM (chicken); BSTM2 5 ventromedial subnucleus of BSTM (chicken); CDL 5 dorsolateral corticoid area (chicken); Ce 5 central amygdala (central amygdalar nucleus); Co 5 cortical amygdalar area (chicken, comparable to ACo of mammals); CPu 5 caudate-putamen; CxA 5 cortico-amygdalar transition area; DC 5 dorsal cortex (reptile); DEn 5 dorsal endopiriform nucleus; EMT 5 prethalamic (or thalamic) eminence; Ent 5 entorhinal cortex; Gaba1 5 g-aminobutyric acid (GABA)-ergic cells; Glu1 5 glutamatergic cells; GP 5 globus pallidus; GPL 5 globus pallidus, lateral part; GPM 5 globus pallidus, medial part; Hb 5 basal hypothalamus; Hip 5 hippocampal formation, rostral olfacto-recipient part; I 5 intercalated cell groups of the amygdale; ic 5 internal capsule; IM 5 intercalated cell groups of the amygdala, main division; L 5 lateral amygdalar nucleus; LC 5 lateral cortex (reptile); LGE 5 lateral ganglionic eminence; LOT 5 nucleus of the lateral olfactory tract; LOT1 5 nucleus of the lateral olfactory tract, layer 1; MC 5 medial cortex (reptile); Me 5 medial amygdala in nonmammals; MeA 5 medial amygdala, anterior part; MeAV 5 medial amygdala, anteroventral part; MePD 5 medial amygdala, posterodorsal part; MePV 5 medial amygdala, posteroven...

show abstract

Selective Requirement of Pax6, But Not Emx2, in the Specification and Development of Several Nuclei of the Amygdaloid Complex

Cited by 97 publications

References 38 publications

Cell Migration along the Lateral Cortical Stream to the Developing Basal Telencephalic Limbic System

Cell Migration along the Lateral Cortical Stream to the Developing Basal Telencephalic Limbic System

COUP-TFII Is Preferentially Expressed in the Caudal Ganglionic Eminence and Is Involved in the Caudal Migratory Stream

The Olfactory Amygdala in Amniotes: An Evo‐Devo Approach

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