Cellular composition and organization of the subventricular zone and rostral migratory stream in the adult and neonatal common marmoset brain

Abstract

The adult subventricular zone (SVZ) of the lateral ventricle contains neural stem cells. In rodents, these cells generate neuroblasts that migrate as chains toward the olfactory bulb along the rostral migratory stream (RMS). The neural-stem-cell niche at the ventricular wall is conserved in various animal species, including primates. However, it is unclear how the SVZ and RMS organization in nonhuman primates relates to that of rodents and humans. Here we studied the SVZ and RMS of the adult and neonatal common marmoset (Callithrix jacchus), a New World primate used widely in neuroscience, by electron microscopy, and immunohistochemical detection of cell-type-specific markers. The marmoset SVZ contained cells similar to type B, C, and A cells of the rodent SVZ in their marker expression and morphology. The adult marmoset SVZ had a three-layer organization, as in the human brain, with ependymal, hypocellular, and astro-cyte-ribbon layers. However, the hypocellular layer was very thin or absent in the adult-anterior and neonatal SVZ. Anti-PSA-NCAM staining of the anterior SVZ in whole-mount ventricular wall preparations of adult marmosets revealed an extensive network of elongated cell aggregates similar to the neuroblast chains in rodents. Time-lapse recordings of marmoset SVZ explants cultured in Matrigel showed the neuroblasts migrating in chains, like rodent type A cells. These results suggest that some features of neurogenesis and neuronal migration in the SVZ are common to marmosets, humans, and rodents. This basic description of the adult and neonatal marmoset SVZ will be useful for future studies on adult neurogenesis in primates.

Identification and characterization of neuroblasts in the subventricular zone and rostral migratory stream of the adult human brain

“…These Dcx+ cells co-expressed Tuj1 and PSA-NCAM ( Figure 2B-2J), suggesting that they are migrating neuroblasts. We also recognized that some neuroblasts formed chains within the RMS ( Figure 2E and Supplementary information, Figure S1) [6,7,[9][10][11]13]. Notably, at this time point, a ventral extension of the anterior horn of the lateral ventricle within the RMS was observed ( Figure 2B and 2I).…”

“…From the SVZ to the OB, the majority of migrating neuroblasts move along each other forming chains [6,7].The RMS appears more prominent in the early postnatal rodent brain than in the adult rodent brain [8]. A similar migration has been described in the neonatal and adult monkey brain [9][10][11][12][13]. However, the general configuration of the RMS in coronal sections of the monkey brain has not yet been unequivocally shown.…”

“…As shown in Figure 1, the RMS in the adult monkey brain extends from the ventral horn of the lateral ventricle to the olfactory tract [9][10][11][12][13]. It is surprising that the anatomical location of the RMS in the adult monkey brain can be observed in a coronal brain section ( Figure 1).…”

“…Every day, new neurons (neuroblasts) are generated in the adult monkey SVZ, and they migrate through an RMS to the OB [9][10][11][12][13]. To characterize the distribution of neuroblasts in the SVZ and RMS of the adult rhesus monkey, we performed double immunostaining for doublecortin (Dcx) and polysialylated neural cell adhesion molecule (PSA-NCAM) in coronal brain sections.…”

“…To characterize the distribution of neuroblasts in the SVZ and RMS of the adult rhesus monkey, we performed double immunostaining for doublecortin (Dcx) and polysialylated neural cell adhesion molecule (PSA-NCAM) in coronal brain sections. Neuroblasts in the monkey SVZ and RMS are Dcx+/PSA-NCAM+, and they form chain-like structures ( Figure 1) [9][10][11]13]. In the SVZ, neuroblasts are mainly found in the lateral and ventral regions ( Figure 1D).…”