Abstract
The orderly radial migration of cortical neurons from their birthplace in the germinal zones to their final destination in the cortical plate is a prerequisite for the functional assembly of microcircuits in the neocortex. Rodent and primate corticogenesis differ both quantitatively and qualitatively, particularly with respect to the generation of neurons of the supragranular layers. Marked area differences in the outer subventricular zone progenitor cell density impact the radial glia scaffold compactness which is likely to induce area differences in radial migration strategy. Here, we describe specific features of radial migration in the non-human primate, including the absence of the premigratory multipolar stage found in rodents. Ex vivo approaches in the embryonic macaque monkey visual cortex, show that migrating neurons destined for supragranular and infragranular layers exhibit significant differences in morphology and velocity. Migrating neurons destined for the supragranular layers show a more complex bipolar morphology and higher motility rates than do infragranular neurons. There are area differences in the gross morphology and membrane growth behavior of the tip of the leading process. In the subplate compartment migrating neurons destined for the supragranular layers of presumptive area 17 exhibit radial constrained trajectories and leading processes with filopodia, which contrast with the meandering trajectories and leading processes capped by lamellipodia observed in the migrating neurons destined for presumptive area 18. Together these results present evidence that migrating neurons may exhibit autonomy and in addition show marked area-specific differences. We hypothesize that the low motility and high radial trajectory of area 17 migrating neurons contribute to the unique structural features of this area.
Highlights
Radial migration of glutamatergic neurons from their birthplace in the germinal zones (GZ) to their final destination in the cortical plate (CP) is a complex process requiring a series of highly coordinated cellular events
The present study focuses on two developmental stages: E65 and E78 (Figure 1A) that correspond, respectively to the generation of the bulk of IG (E55–E71) and SG layer neurons (E72–E90) in the occipital cortex of the macaque monkey (Rakic, 1972; Dehay et al, 1993; Lukaszewicz et al, 2005; Betizeau et al, 2013)
Embryonic organotypic cortical slices provide an unrivaled ex vivo non-human primate model of early corticogenesis, where morphology, proliferation, differentiation and migration can be explored in an intact cytoarchitecture over a one to 2 week period (Betizeau et al, 2013; Figures 1B–E and Supplementary Figure S1)
Summary
Radial migration of glutamatergic neurons from their birthplace in the germinal zones (GZ) to their final destination in the cortical plate (CP) is a complex process requiring a series of highly coordinated cellular events. Several studies have shown that electrical coupling between sister excitatory neurons ensures an important early step in the functional development of the cortex (Yu et al, 2009, 2012; Li Y. et al, 2012) During their radial migration sister excitatory neurons progressively and selectively form gap junctions with each other (He et al, 2015). These observations suggest that the spatial precision of radial migration is a key determinant of highly specific neuronal connectivity as has been shown in the spinal cord (Surmeli et al, 2011). These observations suggest that the area differences in progenitor cell and radial glia scaffold densities could require different migration strategies (Lukaszewicz et al, 2005; Betizeau et al, 2013)
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