Neurogenesis and widespread forebrain migration of distinct GABAergic neurons from the postnatal subventricular zone

Abstract

Most forebrain GABAergic interneurons in rodents are born during embryonic development in the ganglionic eminences (GE) and migrate tangentially into the cortical plate. A subset, however, continues to be generated postnatally in the subventricular zone (SVZ). These interneurons populate the olfactory bulb (OB) reached via migration in the rostral migratory stream (RMS). Employing transgenic mice expressing EGFP in 5-HT 3-positive neurons, we identified additional migratory pathways in the early postnatal brain. Time-lapse imaging experiments revealed massive migration of EGFP-positive cells from the SVZ into numerous forebrain regions, including cortex, striatum, and nucleus accumbens. The neuronal fate of the migratory EGFP-labeled cells was indicated by their doublecortin (DCX) expression. Birthdating experiments, by using 5-bromo-2-deoxyuridine (BrdU) and retrovirus-based experiments, provided evidence that migrating neuroblasts were born in the SVZ postnatally and developed a distinct GABAergic phenotype. Our results demonstrate that the SVZ is a reservoir of GABAergic interneurons not only for the OB, but also for other cortical and subcortical areas.calretinin ͉ EGFP ͉ 5-HT3A receptor ͉ inhibitory interneurons ͉ neuroblast migration

5-HT3AReceptor-Bearing White Matter Interstitial GABAergic Interneurons Are Functionally Integrated into Cortical and Subcortical Networks

“…In 5-HT 3A -EGFP mice the expression of the fluorescent protein was detected in a subset of mature GABAergic interneurons and in postnatally generated neurons derived from the subventricular zone (Inta et al, 2008). The latter eventually populate the olfactory bulb and the cortex.…”

“…The main hindrance for the identification of WMICs in acute slices is their scarcity. We identified distinct WMICs by taking recourse to transgenic mice in which 5-HT 3A receptor-bearing interneurons express enhanced green fluorescence protein (EGFP) (Inta et al, 2008). These mice were originally generated to identify a subgroup of forebrain GABAergic interneurons that feature the expression of the ionotropic serotonin receptor type 5-HT 3A receptors (Tecott et al, 1993;Morales and Bloom, 1997).…”

The N-terminal region of reelin regulates postnatal dendritic maturation of cortical pyramidal neurons

“…There are no reports on the expression of serotonin receptors on Cajal-Retzius cells, although it has been suggested that they may express 5-HT 1A and/or 5-HT 3 receptors (17,20). In this study, we made use of a transgenic mouse line which expresses enhanced green fluorescent protein (EGFP) under the control of the 5-HT 3A promotor (21) to show that Cajal-Retzius cells indeed express functional 5-HT 3 receptors. Because Cajal-Retzius cells are strategically located in layer I of the cortex, where the apical dendrites of pyramidal neurons develop and branch after birth, we tested the hypothesis that serotonergic input on Cajal-Retzius cells controls the postnatal maturation of the apical dendritic trees.…”

Tangential migration and proliferation of intermediate progenitors of GABAergic neurons in the mouse telencephalon

“…As the neocortex grows, the neurogenic intermediate progenitors (nIPs) (Kriegstein and Alvarez-Buylla, 2009) of principal excitatory neurons (Noctor et al, 2004;Miyata et al, 2004;Haubensak et al, 2004;Wu et al, 2005;Hansen et al, 2010) and GABAergic inhibitory neurons (Letinic et al, 2002;Inta et al, 2008) appear in the subventricular zone (SVZ). Unlike the neural precursors of the VZ, the nIPs are multipolar as well as bipolar, and they are not fixed to a given position as are, for example, radial glia, which are anchored by their radial processes.…”