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. 2013 Apr 18:7:59.
doi: 10.3389/fnins.2013.00059. eCollection 2013.

Habitat-specific shaping of proliferation and neuronal differentiation in adult hippocampal neurogenesis of wild rodents

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Habitat-specific shaping of proliferation and neuronal differentiation in adult hippocampal neurogenesis of wild rodents

Nicole Cavegn et al. Front Neurosci. .

Abstract

Daily life of wild mammals is characterized by a multitude of attractive and aversive stimuli. The hippocampus processes complex polymodal information associated with such stimuli and mediates adequate behavioral responses. How newly generated hippocampal neurons in wild animals contribute to hippocampal function is still a subject of debate. Here, we test the relationship between adult hippocampal neurogenesis (AHN) and habitat types. To this end, we compare wild Muridae species of southern Africa [Namaqua rock mouse (Micaelamys namaquensis), red veld rat (Aethomys chrysophilus), highveld gerbil (Tatera brantsii), and spiny mouse (Acomys spinosissimus)] with data from wild European Muridae [long-tailed wood mice (Apodemus sylvaticus), pygmy field mice (Apodemus microps), yellow-necked wood mice (Apodemus flavicollis), and house mice (Mus musculus domesticus)] from previous studies. The pattern of neurogenesis, expressed in normalized numbers of Ki67- and Doublecortin(DCX)-positive cells to total granule cells (GCs), is similar for the species from a southern African habitat. However, we found low proliferation, but high neuronal differentiation in rodents from the southern African habitat compared to rodents from the European environment. Within the African rodents, we observe additional regulatory and morphological traits in the hippocampus. Namaqua rock mice with previous pregnancies showed lower AHN compared to males and nulliparous females. The phylogenetically closely related species (Namaqua rock mouse and red veld rat) show a CA4, which is not usually observed in murine rodents. The specific features of the southern environment that may be associated with the high number of young neurons in African rodents still remain to be elucidated. This study provides the first evidence that a habitat can shape adult neurogenesis in rodents across phylogenetic groups.

Keywords: CA4; Ki67; Muridae; doublecortin; gender; habitat; hippocampus; neurogenesis.

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Figures

Figure 1
Figure 1
Representative images of immunohistological stainings for proliferating cells (Ki67: A,D) and young cells of the neuronal lineage (DCX: B,E) in Namaqua rock mouse (A–C) and spiny mouse (D–F). Condensed chromatin typical for dying cells (C,F) can be easily differentiated in Giemsa stained sections and were used for cell death quantification. Note that granule cells in the spiny mouse (E,F) are considerably smaller than those in the Namaqua rock mouse (B,C). Scale bar (A,C,D,F): 5 μm; (B,E): 10 μm.
Figure 2
Figure 2
Hematoxylin-eosin stained femur cross sections of a younger (A) and older (B) Namaqua rock mouse. Adhesion lines in the outer circumferential lamellae (arrows) and the formation of osteons (asterisk) in the older animals indicate maturation and re-organization of bone tissue while aging. (C) Lens weight and body weight for all southern African rodents, letters indicate the animals whose bone structures are shown at the left. Scale bar: 20 μm.
Figure 3
Figure 3
Boxplots of the distribution of estimated numbers of pyknotic cells, proliferating cells (Ki67), and young cells of the neuronal lineage (DCX) relative to total granule cells, i.e., normalized cell numbers. Southern African species do not differ from each other in any measurement, except for spiny mice which have exceptionally high ratios of proliferating cells in the dentate gyrus.
Figure 4
Figure 4
Within Namaqua rock mice, females that previously had one or several litters (parous) show reduced number of proliferating cells (Ki67) and young neuron (DCX) compared to males. Cell number estimates of parous females are statistically not different from nulliparous females.
Figure 5
Figure 5
In the scatterplot of normalized numbers of young differentiating neurons (estimated number of DCX-positive cells relative to the total granule cell number) to log-transferred normalized proliferating cell (estimated number of Ki67-positive cells relative to the total granule cell number) the species from the cold European climate (Dfb) are separated from those of the general warm southern African habitat (Cwa), which is described as temperate in the Köpper–Geiger climate classification. Southern African species show lower proliferation (P = 0.0003), but higher neuronal differentiation (P = 0.0036) than the rodents from the cold climate. Shaded areas indicate the 95% confidence interval.
Figure 6
Figure 6
Histological stains of the hippocampus in Namaqua rock mouse (A–C) and red veld rat (D–F) reveal common, for murine rodents unusual features. In coronal (A,D) and horizontal (B,E) sections of Giemsa-stained material, a transition from CA3 to CA4 pyramidal cell layer (arrow) can be distinguished. Timm staining (C,F) shows that the infra- and intra-pyramidal terminal field is largely restricted to the CA4 region. Scale bar: 200 μm.
Figure 7
Figure 7
Calbindin stained detail of the hippocampus in Namaqua rock mouse (A), red veld rat (B), highveld gerbil (C), and spiny mouse (D). While mature granule cell and their processes express this protein in all four species, expression is, in contrast to that in laboratory mice and rats, very heterogeneous: tiered in Namaqua rock mouse and red veld rat, mosaic in spiny mouse, and intermediate between these two forms in the highveld gerbil. Molecular layer (ml), granule cell layer (gcl), hilus (h), stratum radiatium (sr), mossy fibers (mf), pyramidal cell layer (pcl), stratum oriens (so). Scale bar: 50 μm.

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References

    1. Amrein I., Dechmann D. K., Winter Y., Lipp H. P. (2007). Absent or low rate of adult neurogenesis in the hippocampus of bats (Chiroptera). PLoS ONE 2:e455 10.1371/journal.pone.0000455 - DOI - PMC - PubMed
    1. Amrein I., Isler K., Lipp H.-P. (2011). Comparing adult hippocampal neurogenesis in mammalian species and orders: influence of chronological age and life stage. Eur. J. Neurosci. 34, 978–987 10.1111/j.1460-9568.2011.07804.x - DOI - PubMed
    1. Amrein I., Lipp H.-P. (2009). Adult hippocampal neurogenesis of mammals: evolution and life history. Biol. Lett. 5, 141–144 10.1098/rsbl.2008.0511 - DOI - PMC - PubMed
    1. Amrein I., Slomianka L. (2010). A morphologically distinct granule cell type in the dentate gyrus of the red fox correlates with adult hippocampal neurogenesis. Brain Res. 1328, 12–24 10.1016/j.brainres.2010.02.075 - DOI - PubMed
    1. Amrein I., Slomianka L., Lipp H. P. (2004a). Granule cell number, cell death and cell proliferation in the dentate gyrus of wild-living rodents. Eur. J. Neurosci. 20, 3342–3350 10.1111/j.1460-9568.2004.03795.x - DOI - PubMed

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