Expression ofDbx1,Neurogenin 2,Semaphorin 5A,Cadherin 8, andEmx1distinguish ventral and lateral pallial histogenetic divisions in the developing mouse claustroamygdaloid complex

Abstract

We studied the lateral and ventral pallial divisions of the claustroamygdaloid complex by means of analysis of expression patterns of the developmental regulatory genes Tbr1, Dbx1, Neurogenin 2, Emx1, Cadherin 8, and Semaphorin 5A in mouse developing telencephalon, from embryonic day 12.5 until birth. Our results indicate that these genes help to distinguish distinct lateral and ventral pallial histogenetic divisions in the embryonic telencephalon. Tbr1 is broadly expressed in both lateral and ventral pallial histogenetic divisions (the lateroventral migratory stream plus the mantle) during early and intermediate embryonic development; its signal becomes weak in parts of the mantle during late embryonic development. Dbx1 is strongly and specifically expressed in progenitor cells (ventricular zone) of the ventral pallium during early embryonic development, but there is no signal of this gene in the rest of the pallium nor the subpallium. Neurogenin 2 and Semaphorin 5A are both expressed in a ventral subdivision of the lateroventral migratory stream (called by us the ventral migratory stream). Further, specific nuclei of the claustral complex and pallial amygdala show strong expression of Neurogenin 2 and/or Semaphorin 5A, including the ventromedial claustrum and endopiriform nuclei, the lateral and basomedial amygdalar nuclei, the anterior and posteromedial cortical amygdalar areas, plus the amygdalo-hippocampal area. We interpret these nuclei or areas of the claustroamygdaloid complex as possible derivatives of the ventral pallium. In contrast, during embryonic development the dorsolateral claustrum, the basolateral amygdalar nucleus, and the posterolateral cortical amygdalar area do not express or show weak expression of Neurogenin 2 or Semaphorin 5A, but express selectively and strongly Cadherin 8 plus Emx1, and may be derivatives of the lateral pallium. The lateral pallial and ventral pallial divisions of the claustroamygdaloid complex appear to have some different sets of connections, although this requires further investigation.

A Novel Transient Glutamatergic Population Migrating from the Pallial–Subpallial Boundary Contributes to Neocortical Development

“…7 I, J; supplemental Fig. 4, available at www.jneurosci.org as supplemental material), as expected from the dynamic of Dbx1 expression (Yun et al, 2001;Medina et al, 2004;Bielle et al, 2005). No cell death was observed in the cortex dorsally to the PSB at any embryonic stages tested (E11.5, E12.5, E14.5, E16.5, and E18.5) ( Fig.…”

“…Glutamatergic Dbx1-derived CP neurons are generated by progenitors at the PSB The Dbx1 gene was shown to be specifically expressed in the ventricular zone of the ventral pallium (VP) at the PSB with a caudal high rostral low gradient, in the septum and in the preoptic area (POA)/anterior entopenduncular area (AEP) (Yun et al, 2001;Medina et al, 2004;Bielle et al, 2005;Hirata et al, 2009). We previously reported that Dbx1-expressing progenitors at the PSB generate Reln ϩ CajalRetzius neurons between E10.5 and E11.5 (Bielle et al, 2005).…”

“…The PSB has been the center of debate in studies on cortical evolution and the acquisition of a new progenitor domain in the VP at the PSB or of migration trajectories from this domain have been proposed to play a crucial role in the "complexification" of the claustro-amygdaloid complex and of the lateral pallium (LP) in mammals (Molnár and Butler, 2002;Medina et al, 2004). …”

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

“…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.…”

“…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).…”