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. 2017 Dec 19:11:719.
doi: 10.3389/fnins.2017.00719. eCollection 2017.

Effects of Strain and Species on the Septo-Temporal Distribution of Adult Neurogenesis in Rodents

Franziska Wiget  1 , R Maarten van Dijk  1   2 , Estelle R Louet  1 , Lutz Slomianka  1   3 , Irmgard Amrein  1   3
Affiliations

Effects of Strain and Species on the Septo-Temporal Distribution of Adult Neurogenesis in Rodents

Franziska Wiget et al. Front Neurosci. .

Abstract

The functional septo-temporal (dorso-ventral) differentiation of the hippocampus is accompanied by gradients of adult hippocampal neurogenesis (AHN) in laboratory rodents. An extensive septal AHN in laboratory mice suggests an emphasis on a relation of AHN to tasks that also depend on the septal hippocampus. Domestication experiments indicate that AHN dynamics along the longitudinal axis are subject to selective pressure, questioning if the septal emphasis of AHN in laboratory mice is a rule applying to rodents in general. In this study, we used C57BL/6 and DBA2/Crl mice, wild-derived F1 house mice and wild-captured wood mice and bank voles to look for evidence of strain and species specific septo-temporal differences in AHN. We confirmed the septal > temporal gradient in C57BL/6 mice, but in the wild species, AHN was low septally and high temporally. Emphasis on the temporal hippocampus was particularly strong for doublecortin positive (DCX+) young neurons and more pronounced in bank voles than in wood mice. The temporal shift was stronger in female wood mice than in males, while we did not see sex differences in bank voles. AHN was overall low in DBA and F1 house mice, but they exhibited the same inversed gradient as wood mice and bank voles. DCX+ young neurons were usually confined to the subgranular zone and deep granule cell layer. This pattern was seen in all animals in the septal and intermediate dentate gyrus. In bank voles and wood mice however, the majority of temporal DCX+ cells were radially dispersed throughout the granule cell layer. Some but not all of the septo-temporal differences were accompanied by changes in the DCX+/Ki67+ cell ratios, suggesting that new neuron numbers can be regulated by both proliferation or the time course of maturation and survival of young neurons. Some of the septo-temporal differences we observe have also been found in laboratory rodents after the experimental manipulation of the molecular mechanisms that control AHN. Adaptations of AHN under natural conditions may operate on these or similar mechanisms, adjusting neurogenesis to the requirements of hippocampal function.

Keywords: Apodemus sylvaticus; Ki67; Mus domesticus; Myodes glareolus; doublecortin.

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Figures

Figure 1
Figure 1
Distribution of neurogenesis-related absolute cell counts along the septo-temporal axis. Neurogenesis assessment in dissected, straightened hippocampi in laboratory C57BL/6 (A) follows a general septal>temporal gradient, whereas DBA (B), house mice (C), wood mice (D), and bank voles (E) show a septal<temporal gradient for young neurons (DCX), and, except for DBA, also for cell proliferation (Ki67). Raw data of cell counts were re-distributed into 12 virtual sections to allow direct comparisons within and between species/strains, gray areas indicate 95% confidence intervals. (F) Shows representative images of hematoxylin-counterstained DCX+ young neurons (A') and Ki67+ cells (B') in the subgranular layer of the dentate gyrus. Scale bar = 20 μm.
Figure 2
Figure 2
Opposite neurogenesis gradient in laboratory C57BL/6. Values of young neurons and proliferating cells were re-calculated as percentage for each animal to allow statistical comparisons. (A) C57BL/6 is distinct from other species and strains in the septal subdivision with significantly more young neurons than all other species (all p < 0.01) and significantly fewer young neurons in the temporal subdivision (all comparisons p < 0.05). In the intermediate hippocampus, bank voles have higher DCX values than C57BL/6, DBA and house mice. (B) Septo-temporal distribution of proliferating cells is overall more similar, however, in the septal subdivision the extremes are represented by C57BL/6 (high) and house mice (low), which are significantly different from DBA, bank voles and wood mice. In the intermediate hippocampus, bank voles score higher than all other species (p = 0.002 to < 0.0001). In the temporal subdivision house mice have more proliferating cells than all other species (p = 0.006 to < 0.0001). As a proxy for young neuron survival, the ratio of DCX+ cells to Ki67+ cells is presented in (C), separately for the three hippocampal subdivision. Survival rate is lowest in DBA in the septal subdivision. Bank voles score higher in survival rate than DBA and wood mice in the intermediate (p < 0.01). In the temporal subdivision, neuronal survival in bank voles excels all other species values (p < 0.001). *p < 0.05, **p < 0.01, and ***p < 0.001; color-coding corresponds to the species/strain showing the difference, for exact values see results.
Figure 3
Figure 3
Radial location of DCX positive cells in bank voles and wood mice. DCX+ cells in wild rodents are not only found in the subgranular zone (SGZ, A,A'), but are found dispersed throughout the granular cell layer (GCL, B,B'). Quantitative assessment of DCX+ cells in the SGZ vs. those cells within the GCL reveals differences along the septo-temporal axis (C). While DCX+ cells in the SGZ predominate in the septal and intermediate hippocampus, significantly more DCX+ cells are found within the granule cell layer in the temporal subdivision. Scale bare (A,B) = 50 μm; (A',B') = 10 μm. **p < 0.01, and ***p < 0.001; for exact values see results.
Figure 4
Figure 4
Sex differences in DCX+ cells in wood mice along the hippocampal axis. The septal < temporal gradient in DCX+ cell distribution is more pronounced in female wood mice (A) as compared to males. Septally, they have lower values than males, while temporally females DCX+ values exceed those of males. In bank voles (B), males and females do not differ with regard to DCX+ cell distribution along the septo-temporal axis. *p < 0.05; for exact values see results.
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