Tangential migration of glutamatergic neurons and cortical patterning during development: Lessons from Cajal‐Retzius cells

Abstract

Tangential migration is a mode of cell movement, which in the developing cerebral cortex, is defined by displacement parallel to the ventricular surface and orthogonal to the radial glial fibers. This mode of long-range migration is a strategy by which distinct neuronal classes generated from spatially and molecularly distinct origins can integrate to form appropriate neural circuits within the cortical plate. While it was previously believed that only GABAergic cortical interneurons migrate tangentially from their origins in the subpallial ganglionic eminences to integrate in the cortical plate, it is now known that transient populations of glutamatergic neurons also adopt this mode of migration. These include Cajal-Retzius cells (CRs), subplate neurons (SPs), and cortical plate transient neurons (CPTs), which have crucial roles in orchestrating the radial and tangential development of the embryonic cerebral cortex in a noncell-autonomous manner. While CRs have been extensively studied, it is only in the last decade that the molecular mechanisms governing their tangential migration have begun to be elucidated. To date, the mechanisms of SPs and CPTs tangential migration remain unknown. We therefore review the known signaling pathways, which regulate parameters of CRs migration including their motility, contact-redistribution and adhesion to the pial surface, and discuss this in the context of how CR migration may regulate their signaling activity in a spatial and temporal manner. © 2015 Wiley Periodicals, Inc. Develop Neurobiol 76: 847-881, 2016.

In Vitro, Ex Vivo and In Vivo Techniques to Study Neuronal Migration in the Developing Cerebral Cortex

“…Inhibitory GABAergic neurons are born in the ventral regions of the brain and they have to migrate long distances to reach the cortex using a mode of migration called tangential migration (Figure 1) [3,10]. Although the distinction in radially migrating glutamatergic neurons and tangentially migrating interneurons is particularly helpful for discussion purposes, it is important to note that several classes of glutamatergic neurons, such as Cajal Retzius cells, a subpopulation of subplate neurons and transient cortical neurons also migrate tangentially to disperse along the medio-lateral axis [11]. …”

Sculpting Cerebral Cortex with Serotonin in Rodent and Primate

“…They will both participate in regulating neurogenesis [69]. The first generated neurons, Cajal-Retzius (C-R) cells and subplate cells (SP; from E10 in mice, GW5-7 in human), constitute transient and heterogeneous populations of cells that originate from both pallial and subpallial territories and form the preplate (PP; Boulder Committee; [66,70,71]). SP and reelin-secreting C-R cells provide positioning cues and instructions to developing cortical neurons and afferents [71][72][73][74].…”

“…The first generated neurons, Cajal-Retzius (C-R) cells and subplate cells (SP; from E10 in mice, GW5-7 in human), constitute transient and heterogeneous populations of cells that originate from both pallial and subpallial territories and form the preplate (PP; Boulder Committee; [66,70,71]). SP and reelin-secreting C-R cells provide positioning cues and instructions to developing cortical neurons and afferents [71][72][73][74]. The cortical plate, is formed from E13-E17 in mice and GW7-20 in human by post-mitotic excitatory pyramidal neurons migrated along radial glial (RG) fibres in an inside out gradient of development from layer VIa to layer II [13].…”

The Onecut Transcription Factors Regulate Differentiation and Distribution of Dorsal Interneurons during Spinal Cord Development

“…The genetic programs that support the generation and the diversification of spinal interneurons have been extensively investigated (Lu et al, 2015). However, in contrast to cortical interneurons whose migration mechanisms have been largely deciphered (Guo and Anton, 2014; Barber and Pierani, 2016), the molecular determinants that regulate the distribution of interneuron populations in the developing spinal cord remain elusive.…”