Review articleNeurogenesis and neuronal migration in the postnatal ventricular-subventricular zone: Similarities and dissimilarities between rodents and primates
Introduction
In the 1960s, Altman and colleagues suggested that new neurons can be born in the adult mammalian brain (Altman, 2011). Following these pioneering studies, the mechanisms of adult neurogenesis have been extensively studied over the decades. It is now well-accepted that new neurons are produced after birth in two brain regions: the ventricular-subventricular zone (V-SVZ), located in the walls of the lateral ventricles, and the subgranular zone (SGZ) in the dentate gyrus of the hippocampus, with other regions of the central nervous system losing their neurogenic capacity after birth. In these two neurogenic niches, new neurons are produced from progenitors, or neural stem cells (NSCs). Although the basis of adult neurogenesis is similar among different mammalian species, the extent of neurogenesis and directions of neuroblast migration vary from rodents to primates as the brain becomes relatively larger and more complex (Akter et al., 2020; Dennis et al., 2016; Doetsch et al., 1997; Gil-Perotin et al., 2009; Kornack and Rakic, 2001; Lois et al., 1996; Lois and Alvarez-Buylla, 1994; Paredes et al., 2016a; Pencea et al., 2001; Sanai et al., 2011; Sawamoto et al., 2011; Wang et al., 2011).
Most of our knowledge regarding adult neurogenesis comes from studies using rodents owing to the expanded possibilities of their experimental use. Our understanding of adult neurogenesis in humans and non-human primates is gradually increasing. Consequently, we now know that some of the features of adult neurogenesis are not shared among rodents, humans, and non-human primates. In rodents and non-human primates, SGZ NSCs in the postnatal dentate gyrus continuously produce new neurons; however, the extent of postnatal neurogenesis in the human hippocampal dentate gyrus is under debate (Spalding et al., 2013; Sorrells et al., 2018; Boldrini et al., 2018). To solve the unanswered questions regarding adult neurogenesis in humans, new methodologies to study the generation of new neurons in adult human are needed as discussed in recent reviews (Kempermann et al., 2018; Snyder, 2018).
In contrast to the new neurons that are locally generated and differentiated within the hippocampus, those generated in the V-SVZ have greater potential to migrate long distances to other brain regions. Recent studies suggest mechanisms for neurogenesis and neuronal migration are also different among rodents, humans, and non-human primates. Therefore, in this review, we focus on the similarities and differences of postnatal V-SVZ neurogenesis between rodents and primates and its involvement in the endogenous repair processes.
Section snippets
V-SVZ organization
The V-SVZ is composed of ependymal cells, neuroblasts, astrocytes, and transit-amplifying cells in both rodents and primates (Doetsch et al., 1997; Gil- Perotin et al., 2009; Sawamoto et al., 2011). Ependymal cells form an epithelial layer that lines the ventricles. The V-SVZ astrocytes have been identified as the primary neural progenitors, i.e., NSCs in the adult brain (Doetsch et al., 1999). NSCs proliferate slowly and give rise to rapidly-dividing intermediate progenitors, which produce
Spatiotemporal patterns of V-SVZ neurogenesis
V-SVZ neuroblasts differentiate into interneurons in distinct layers of the OB. The majority of these interneurons are granule cells (GCs) in the granular cell layer, while the rest are periglomerular cells (PGCs) in the glomerular layer. GCs can be subdivided into three subtypes based on the location of their cell bodies: intermediate, deep, and superficial GCs (Price and Powell, 1970). PGCs can also be subdivided into three subtypes based on the expression of calretinin (CR), calbindin (CB),
Migration of V-SVZ-derived neuroblasts in the postnatal brain
In rodents, a large number of migrating neuroblasts are produced from NSCs and migrate through the rostral migratory stream (RMS) as an elongated, chain-like aggregate to reach their final destination, the olfactory bulb (OB), where they differentiate into interneurons (Doetsch et al., 1997,1999; Lois et al., 1996; Lois and Alvarez-Buylla, 1994). Conversely, there are very few migrating neuroblasts in the human RMS, which appear as singlets or in pairs, but do not form a chain, after 2 years of
Limits and challenges for endogenous repair in the primate brain
Neurogenesis in the adult V-SVZ is a potential target for regenerative therapies of the injured brain. After brain injury to areas such as the striatum and cortex, various chemokines and growth factors are upregulated, which stimulate the proliferation of NSCs and transit-amplifying cells in the V-SVZ and migration of neuroblasts (Fujioka et al., 2019; Sawada and Sawamoto, 2013). A successful approach for regenerating neuronal circuits for functional recovery after an injury has been reported
Conclusion
Neuroscientists show deep interest in how the human brain works and how it differs from those of other species. However, there are various technical limitations in studying the development of the human brain. Non-human primates can, therefore, be useful as model animals because they are more similar to humans than rodents. Considering the recent technical advances in generating transgenic primates (Sasaki et al., 2009; Park and Silva, 2019), modern genetic techniques, currently only applicable
Acknowledgments
We apologize to all whose work we could not cite because of space limitations. We are grateful to Jose Manuel Garcia-Verdugo, Chikako Nakajima, Mercedes Paredes, Masato Sawada, and Vicente Herranz Perez for their valuable comments, and Trent Rogers (Edanz Group) for editing drafts of this manuscript. This study was supported by research grants from the Japan Society for the Promotion of Science KAKENHI (17H01392, 17H05750, 19H04757, 19H04785, 18KK0213 [to K.S.], 17K07114[to N.K.]), the
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