Temporal features of adult neurogenesis: differences and similarities across mammalian species

Abstract

Production of new neurons continues throughout life in most invertebrates and vertebrates like crustaceans, fishes, reptiles, birds, and mammals including humans. Most studies have been carried out on rodent models and demonstrated that adult neurogenesis is located mainly in two structures, the dentate gyrus (DG) of the hippocampus and the sub-ventricular zone (SVZ). If adult neurogenesis is well preserved throughout evolution, yet there are however some features which differ between species. The present review proposes to target similarities and differences in the mechanism of mammalian adult neurogenesis by comparing selected species including humans. We will highlight the cellular composition and morphological organization of the SVZ in primates which differs from that of rodents and may be of functional relevance. We will particularly focus on the dynamic of neuronal maturation in rodents, primates, and humans but also in sheep which appears to be an interesting model due to its similarities with the primate brain.

Keywords: dentate gyrus; hippocampus; neuronal maturation; olfactory bulb; primate; rostral migratory stream; sheep; sub-ventricular zone.

Figure 1

Sub-ventricular zone organization and migration pathway to the main olfactory bulb. Ant SVZ, anterior sub-ventricular zone; post-SVZ, posterior sub-ventricular zone; yes, presence; no, absence.

Figure 2

Illustration of the migration pathway from the SVZ to the MOB in the sheep brain. Confocal images depicting fluorescent immunolabeling of DCX (red) and GFAP (green) in the anterior SVZ (A,B), in the dorsal part (C) and the ventral part (D) of the MOB, and in the granular cell layer of the MOB in sheep (E,F). Nuclei of cells are revealed by a Hoechst staining (blue). Note the presence of a hypocellular-like layer between the ependymal layer lining the lateral ventricle and chains of neuroblasts in the anterior SVZ (double white arrow in A) and the shift of DCX+ cells that are oriented parallel to the olfactory ventricle in the periventricular layer (E) and perpendicular to rows of granular cell nuclei in the GCL of the MOB (E,F). GCL, granular cell layer; LV, lateral ventricle; PL, periventricular layer; OV, olfactory ventricle.

Figure 3

Dynamic of neuronal maturation time of adult-born cells in the MOB. (A,B) Confocal images of double fluorescent immunolabeling of BrdU (green)/DCX (red), a marker of migrating neuroblasts (A) and BrdU (red)/NeuN (green) a marker of post-mitotic neurons (B) in the granular layer of the MOB in sheep. (C,D) Neuronal maturation time of different mammalian species (mouse, rat, sheep, marmoset, and macaque) are represented as percentage of newborn neuroblasts (C) and newborn neurons (D) across different survival times (Kornack and Rakic, ; Petreanu and Alvarez-Buylla, ; Winner et al., ; Brown et al., ; Sawamoto et al., ; Brus et al., 2013). Note that maximal neuronal maturation is reached in the first month post-injection in mice and rat whereas in sheep and primate the first new mature neurons are only observed at 3 months (90 days). The blue square represent the first adult-born neurons (BrdU+/NeuN+) observed in the MOB of the macaque monkey but no percentage was specified (Kornack and Rakic, 2001).

Figure 4

Dynamic of neuronal maturation time of adult-born cells in the DG. (A,B) Confocal images of double fluorescent immunolabeling of BrdU (green)/DCX (red), a marker of migrating neuroblasts (A) and BrdU (red)/NeuN (green) a marker of post-mitotic neurons (B) in the granular layer of the DG in sheep. (C,D) Neuronal maturation time of different mammalian species (mouse, rat, sheep and macaque) are represented as percentage of newborn neuroblasts (C) and newborn neurons (D) across 240 survival days reported by several studies (Cameron et al., ; Brown et al., ; Steiner et al., ; McDonald and Wojtowicz, ; Snyder et al., ; Kohler et al., ; Brus et al., 2013). Note that maximal neuronal maturation is reached in the first month post-injection in mice and rat whereas in sheep and primate new immature and mature neurons appear around 15–30 days post-injection and reach a maximum at 4 months in sheep and around 6 months in macaque monkey.

Figure 5

Comparative study of protocols used to estimate neuronal maturation of adult born neurons. Times in bold correspond to those represented in Figures 3, 4. Number of animals corresponds to the sample size by groups. BrdU, bromodeoxyuridine; DCX, Doublecortin; NeuN, neuron-specific nuclear protein; NSE, neuron specific enolase; DG, dentate gyrus; MOB, main olfactory bulb.