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.
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ABSTRACT: A previous study investigating potential adult hippocampal neurogenesis in microchiropteran bats failed to reveal a strong presence of this neural trait. As microchiropterans have a high field metabolic rate and a small body mass, it is possible that capture/handling stress may lead to a decrease in the detectable presence of adult hippocampal neurogenesis. Here we looked for evidence of adult hippocampal neurogenesis using immunohistochemical techniques for the endogenous marker doublecortin in 10 species of microchiropterans euthanized and perfusion fixed at specific time points following capture. Our results reveal that when euthanized and perfused within 15 minutes of capture, abundant putative adult hippocampal neurogenesis could be detected using doublecortin immunhistochemistry. Between 15 and 30 minutes post-capture, the detectable levels of doublecortin dropped dramatically and after 30 minutes post-capture, immunohistochemistry for doublecortin could not reveal any significant evidence of putative adult hippocampal neurogenesis. Thus, as with all other mammals studied to date apart from cetaceans, bats, including both microchiropterans and megachiropterans, appear to exhibit substantial levels of adult hippocampal neurogenesis. The present study underscores the concept that, as with laboratory experiments, studies conducted on wild-caught animals need to be cognizant of the fact that acute stress (capture/handling) may induce major changes in the appearance of specific neural traits.Neuroscience 08/2014; 277. DOI:10.1016/j.neuroscience.2014.07.063 · 3.33 Impact Factor
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ABSTRACT: The present study evaluated, using immunohistochemical methods, the presence and characteristics of proliferating and newly generated neurons in the brain of eight wild-caught adult Megachiropteran species. For the neurogenic patterns observed, direct homologies are evident in other mammalian species; however, there were several distinctions in the presence or absence of proliferating and immature neurons, and migratory streams that provide important clues regarding the use of the brain in the analysis of Chiropteran phylogenetic affinities. In all eight species studied, numerous Ki-67 and DCX immunopositive cells were identified in the subventricular zone (SVZ). These cells migrated to the olfactory bulb through a Primate-like rostral migratory stream (RMS) that is composed of dorsal and ventral substreams which merge before entering the olfactory bulb. Some cells were observed emerging from the RMS coursing caudally and dorsally to the rostral neocortex. In the dentate gyrus of all species, Ki-67 and DCX-expressing cells were observed in the granular cell layer and hilus. Similar to Primates, proliferating cells and immature neurons were identified in the SVZ of the temporal horn of Megachiropterans. These cells migrated to the rostral and caudal piriform cortex through a Primate-like temporal migratory stream. Sparsely distributed Ki-67 immunopositive, but DCX immunonegative, cells were identified in the tectum, brainstem and cerebellum. The observations from this study add to a number of neural characteristics that phylogenetically align Megachiropterans to Primates.Neuroscience 04/2013; DOI:10.1016/j.neuroscience.2013.04.020 · 3.33 Impact Factor
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ABSTRACT: Adult neurogenesis in mammals is typically observed in the subgranular zone of the hippocampal dentate gyrus and the subventricular zone. We investigated adult neurogenesis in the brain of a giant otter shrew (Potamogale velox), a semi-aquatic, central African rainforest mammal of the family Tenrecidae that belongs to the superorder Afrotheria. We examined neurogenesis immunohistochemically, using the endogenous marker doublecortin (DCX), which stains neuronal precursor cells and immature neurons. Our results revealed densely packed DCX positive cells in the entire extent of the subventricular zone from where cells migrated along the rostral migratory stream to the olfactory bulb. In the olfactory bulb, DCX expressing cells were primarily present in the granular cell layer with radially orientated dendrites and in the glomerular layer representing periglomerular cells. In the hippocampus, DCX positive cells were identified in the subgranular and granular layers of the dentate gyrus and strongly labeled DCX positive processes, presumably dendrites and axons of the newly generated granular cells, were observed in the CA3 regions. In addition, DCX immunoreactive cells were present in the olfactory tubercle, the piriform cortex and the endopiriform nucleus. While DCX positive fibres have been previously observed in the anterior commissure of hedgehog and mole, we were able to demonstrate the presence of DCX positive cells presumably migrating across the anterior commissure. Taken together, the giant otter shrew reveals patterns of neurogenesis similar to that seen in other mammals; however, the appearance of possible neuronal precursor cells in the anterior commissure is a novel observation.Neuroscience 02/2013; 238. DOI:10.1016/j.neuroscience.2013.02.025 · 3.33 Impact Factor