Septo-temporal distribution and lineage progression of hippocampal neurogenesis in a primate (Callithrix jacchus) in comparison to mice

Abstract

Adult born neurons in the hippocampus show species-specific differences in their numbers, the pace of their maturation and their spatial distribution. Here, we present quantitative data on adult hippocampal neurogenesis in a New World primate, the common marmoset (Callithrix jacchus) that demonstrate parts of the lineage progression and age-related changes. Proliferation was largely (∼70%) restricted to stem cells or early progenitor cells, whilst the remainder of the cycling pool could be assigned almost exclusively to Tbr2+ intermediate precursor cells in both neonate and adult animals (20–122 months). Proliferating DCX+ neuroblasts were virtually absent in adults, although rare MCM2+/DCX+ co-expression revealed a small, persisting proliferative potential. Co-expression of DCX with calretinin was very limited in marmosets, suggesting that these markers label distinct maturational stages. In adult marmosets, numbers of MCM2+, Ki67+, and significantly Tbr2+, DCX+, and CR+ cells declined with age. The distributions of granule cells, proliferating cells and DCX+ young neurons along the hippocampal longitudinal axis were equal in marmosets and mice. In both species, a gradient along the hippocampal septo-temporal axis was apparent for DCX+ and resident granule cells. Both cell numbers are higher septally than temporally, whilst proliferating cells were evenly distributed along this axis. Relative to resident granule cells, however, the ratio of proliferating cells and DCX+ neurons remained constant in the septal, middle, and temporal hippocampus. In marmosets, the extended phase of the maturation of young neurons that characterizes primate hippocampal neurogenesis was due to the extension in a large CR+/DCX- cell population. This clear dissociation between DCX+ and CR+ young neurons has not been reported for other species and may therefore represent a key primate-specific feature of adult hippocampal neurogenesis.

Adult neurogenesis and gliogenesis in the dorsal and ventral canine hippocampus

“…However, in the adult rat hippocampus the dorsal and ventral DG part were shown to possess equal neurogenic ability (Amrein et al, ; Bekiari et al, ; ), meaning that the possible structural and functional significance of the here and previously revealed inter‐species differentiations (Amrein et al, ; Hawken et al, ; Kempermann, Kuhn, & Gage, ; Kornack & Rakic, ; Snyder et al, ; Wu et al, ) in the dorso‐ventral aspects of adult neurogenesis have yet to be investigated.…”

“…Existing data from non‐human primates refer that in contrast to rodents, where the pool of DG proliferating cells comprises from radial glia‐like NSCs to DCX‐expressing neuroblasts (Plumpe et al, ), in the primate DG the proliferative pool consists almost exclusively of radial glia‐like NSCs since non‐human primate DCX + cells rarely proliferate (Amrein et al, ; Taffe et al, ). It seems that NSCs of the canine DG apply to the above aspect.…”

“…Newborn granule cells sequentially express DCX, NeuN, calretinin, and calbindin during the successive time frames of their differentiation and maturation process (Duan et al, ; Kempermann et al, ) and this expression pattern is conserved in all the up to date studied mammalian species. However, a growing number of studies show that new granule cells of the gyrencephalic species present a prolonged maturation period when compared to newborn neurons of the rodent DG (Amrein et al, ; Brus, Keller, & Levy, ; Kohler et al, ).…”

“…All immunoreactive cells in the SGZ and the GCL (Granule Cell Layer) were counted exhaustively under a ×40 objective (Nikon Eclipse 80i microscope; Y‐ IDP, Japan) with the use of a Nikon D‐Eclipse C1 camera. The total number of BrdU‐labeled cells counted in the sampled sections was multiplied by the inverse of the section sampling (×20) to calculate the absolute number of BrdU + cells per DG (Amrein et al, ; (Bekiari et al, ; ; Kronenberg et al, ).…”

“…Under a Nikon optical microscope (Nikon Eclipse 80i microscope; Y‐ IDP, Japan), serial photos of the granular cell layer in its full extent were captured for all stained sections (reference sections) and their neighbor sections (control sections) with a Nikon D‐Eclipse C1 camera at a ×40 magnification and calculations were made using the Image J software (version 1.47; NIH; RRID: SCR_003070) as previously described (Bekiari et al, 2015a; ). Obtained number was multiplied by the inverse of the section sampling (×60) to estimate the absolute number of granule cells per dDG and vDG (Amrein et al, ; Bekiari et al, ; ).…”