Development of the mouse amygdala as revealed by enhanced green fluorescent protein gene transfer by means of in utero electroporation

Abstract

The amygdala is located in the caudal part of the ventral telencephalon. It is composed of many subdivisions and is involved in the control of emotion. It is important to know the mechanisms of amygdalar development in order to analyze the pathogenesis of emotional disorders, but they are still not adequately understood. In the present study the migration, differentiation, and distribution of amygdalar neurons in the mouse embryo were investigated by means of in utero electroporation. Ventricular zone cells in restricted regions, that is, the caudal ganglionic eminence (CGE), the ventral pallium, the lateral pallium, and the diencephalon, were labeled with an expression vector of the enhanced green fluorescent protein (EGFP) gene. Labeling at embryonic day (E)10 revealed that the central nucleus originates from the neuroepithelium in the ganglionic eminence and the labeling at E11 and E12 revealed that the basolateral complex originates from the neuroepithelium of the ventral and lateral pallia. The introduction of the EGFP gene into the neuroepithelium of the third ventricle at E11 showed that the medial nucleus originates, at least in part, from the neuroepithelium of the diencephalon and migrates over the diencephalo-telencephalic boundary. The radial glial arrangement corresponded well with the initial migration of amygdalar neurons, and the radial processes later formed the boundary demarcating the basolateral complex. These findings indicate that the neurons originating from the temporally and spatially restricted neuroepithelium in both the telencephalon and diencephalon migrate and differentiate to form the mosaic of amygdalar subdivisions. J.

The COUP-TFII/Neuropilin-2 is a molecular switch steering diencephalon-derived GABAergic neurons in the developing mouse brain

“…The present findings show that the POa-derived cells that were migrating to the neocortex and the amygdala initially shared the migratory stream and then took separate paths controlled by the dynamic expression of COUP-TFII and Nrp2. A previous study by Soma et al shows a sharp, bundle-like migratory stream from the third ventricle; however, it was reported without characterizing the origin of this stream (29). Our present findings, which are based on focal electroporation into specific regions of the hypothalamus, demonstrate that the bundle-like migratory stream originates mainly from the POa2 domain.…”

Global view of the functional molecular organization of the avian cerebrum: mirror images and functional columns

“…For example, the ER81 gene expression pattern used to support the hypothesis of homology between the avian arcopallium and mammalian layer V cortical neurons Dugas-Ford et al, 2012) is also expressed in the basal lateral amygdala (Nomura et al, 2009). In turn, the basal lateral amygdala and other pallial amygdala regions have been proposed to developmentally derive from pallial cells that are similar to the cortex (Swanson, 2000;Deussing and Wurst, 2007;Remedios et al, 2007;Soma et al, 2009). Conversely, the EMX1 gene expression pattern used to support the hypothesis of homology of the ventral pallial region of birds (hyperstriatum ventrale; our MD) and mammalian ventral claustrum (Smith-Fernandez et al, 1998;Puelles et al, 2000; Aboitiz, 2011) is also expressed in the mammalian cortex, and is also high in both avian MV and MD, where just like for GRIA1, FOXP1, and other mesopallium marker genes, the LMI boundary is not always seen with mesopallium enriched genes.…”

“…The mammalian cortical columns extend across layers of cells that predominantly arrive in their locations by radial migration from the same sector of the ventricle zone during development, whereas the avian pallial columns extend across larger clusters of cells that may predominantly arrive in their location by tangential migration from different sectors of the ventricle zone (Medina and Abellan, 2009). The pallial portions of the mammalian amygdala and claustrum develop by diverse mechanisms, including both local radial and long-distance tangential migration of cells from the dorsal pallium, the thalamus and preoptic area (Carney et al, 2006;Deussing and Wurst, 2007;Hirata et al, 2009;Soma et al, 2009;Garcia-Moreno et al, 2010;Bupesh et al, 2011). Nevertheless, regardless of how the pallial and subpallial cells arrive to their final destination in mammals and birds, the final outcome is similar: columns across different cell populations organized as layers (cortex in mammals) or thick nuclear slabs (pallium in birds and claustrum/ amygdala in mammals).…”

Contribution of Genoarchitecture to Understanding Forebrain Evolution and Development, with Particular Emphasis on the Amygdala

“…However, its location and extension in sauropsids has remained highly controversial [reviewed in Striedter, 1997;Puelles, 2001b;Jarvis et al, 2005;Martínez-García et al, 2007;Medina and Abellán, 2009]. A large amount of developmental data published in recent years has provided highly interesting information on the embryonic and molecular identity of amygdalar components in mammals [Puelles et al, 2000;Medina et al, 2004;Remedios et al, 2004;Tole et al, 2005;Hirata et al, 2009;Soma et al, 2009;García-Moreno et al, 2010;Waclaw et al, 2010;Bupesh et al, 2011a, b]. Little by little, similar information is being collected in other vertebrates, and these data are becoming essential for understanding the development and evolution of this structure.…”

“…Therefore, using single genes or combinations of genes for identifying homologous structures disregarding the topological framework of the neural tube often leads to erroneous interpretations. We will focus on the amygdala, a telencephalic center involved in the control of emotions and social behavior that has been found at least in all tetrapods [reviews by Moreno and González, 2006;Martínez-García et al, 2007]; its development has been investigated in depth using genetic and fate map tools in recent years [Puelles et al, 2000;Medina et al, 2004;Remedios et al, 2004Remedios et al, , 2007Tole et al, 2005;Moreno and González, 2007a, b;Medina, 2008, 2009;García-López et al, 2008;Moreno et al, 2008aMoreno et al, , b, 2009Abellán et al, , 2010Hirata et al, 2009;Soma et al, 2009;García-Moreno et al, 2010;Waclaw et al, 2010;Bupesh et al, 2011a, b]. Since the amygdala in different tetrapods also appears to include neurons derived from extratelencephalic domains [Bardet et al, 2008;Abellán et al, 2010;García-Moreno et al, 2010], we will start with a brief summary of some aspects of forebrain development that help to understand its basic divisions and organization.…”