Hippocampal Neurogenesis and Cortical Cellular Plasticity in Wahlberg’s Epauletted Fruit Bat: A Qualitative and Quantitative Study

Abstract

Species-specific characteristics of neuronal plasticity emerging from comparative studies can address the functional relevance of hippocampal or cortical plasticity in the light of ecological adaptation and evolutionary history of a given species. Here, we present a quantitative and qualitative analysis of neurogenesis in young and adult free-living Wahlberg’s epauletted fruit bats. Using the markers for proliferating cell nuclear antigen (PCNA), bromodeoxyuridine (BrdU), doublecortin (DCX) and polysialic acid neural cell adhesion molecule (PSA-NCAM), our findings in the hippocampus, olfactory bulb and cortical regions are described and compared to reports in other mammals. Expressed as a percentage of the total number of granule cells, PCNA- and BrdU-positive cells accounted for 0.04 in young to 0.01% in adult animals; DCX-positive cells for 0.05 (young) to 0.01% (adult); PSA-NCAM-positive cells for 0.1 (young) to 0.02% (adult), and pyknotic cells for 0.007 (young) to 0.005% (adult). The numbers were comparable to other long-lived, late-maturing mammals such as primates. A significant increase in the total granule cell number from young to adult animals demonstrated the successful formation and integration of new cells. In adulthood, granule cell number appeared stable and was surprisingly low in comparison to other species. Observations in the olfactory bulb and rostral migratory stream were qualitatively similar to descriptions in other species. In the ventral horn of the lateral ventricle, we noted prominent expression of DCX and PSA-NCAM forming a temporal migratory stream targeting the piriform cortex, possibly reflecting the importance of olfaction to these species. Low, but persistent hippocampal neurogenesis in non-echolocating fruit bats contrasted the findings in echolocating microbats, in which hippocampal neurogenesis was largely absent. Together with the observed intense cortical plasticity in the olfactory system of fruit bats we suggest a differential influence of sensory modalities on hippocampal and cortical plasticity in this mammalian order.

From chemotaxis to the cognitive map: The function of olfaction

“…The OS interpretation of this labile pattern is that detector microbats, relying heavily on spatial audition, have fundamentally replaced their OS system and now require less plasticity in BE components (e.g., OB, dentate gyrus). This hypothesis is supported by new data from the same group on megabats, which show a much higher level of hippocampal neurogenesis than microbats, but lower than that seen in laboratory rodents (50). This, too, would be predicted by the OS hypothesis, as megabats appear to be the predictors of the chiropterans.…”

Microbats appear to have adult hippocampal neurogenesis, but post-capture stress causes a rapid decline in the number of neurons expressing doublecortin

“…Powers, 2013). It should be noted here that Amrein et al (2007) only studied species from the microchiropteran suborder of bats, and not the megachiropteran suborder, for which two recent reports have detailed the presence of adult hippocampal neurogenesis in a range of megachiropteran species (Gatome et al, 2010;Chawana et al, 2013), making the title and conclusions of the Amrein et al (2007) paper misleading as they use only the generic term bats.…”

Adult Hippocampal Neurogenesis in Natural Populations of Mammals

“…In contrast, in megachiropteran species, or fruiteating bats, all animals investigated so far show AHN, albeit at very low levels when compared with rodents. Robust but low numbers of proliferating cells and young neurons were found in wild Wahlberg's epauletted fruit bat (Epomophorus wahlbergi [Gatome et al 2010]) and in seven additional species of wild megachiropterans (Chawana et al 2013). In contrast to low or absent AHN in bats, high numbers of young cells of the neuronal lineage have been reported in the hippocampus of carnivores such as cats (Altman 1963), wild red foxes (Vulpes vulpes [Amrein and Slomianka 2010]), and several dog breeds (Hwang et al 2007;Siwak-Tapp et al 2007;De Nevi et al 2013).…”

“…Although the lack of neurogenesis is by now almost more interesting than its presence, DCX was the only marker used. DCX staining does show some species differences (Gatome et al 2010;Slomianka et al 2013;Amrein et al 2014) and may be weak when PSA-NCAM generates a strong signal or vice versa. Observations in Cetacea should be confirmed using multiple markers for proliferating cells and differentiating young neurons.…”

“…Age determination in small mammals has been performed using body weight in relation to season in combination with species-specific measures such as tooth wear (Amrein et al 2004b), or closure of the femoral and humeral epiphyseal plate (Amrein et al 2007;Gatome et al 2010). Epp et al (2009) have used eye lens weights, assessed in both wild rats and laboratory conspecifics of known age, for age estimation.…”