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Abstract
Bats are the only flying mammals and have well developed navigation abilities for 3D-space. Even bats with comparatively small home ranges cover much larger territories than rodents, and long-distance migration by some species is unique among small mammals. Adult proliferation of neurons, i.e., adult neurogenesis, in the dentate gyrus of rodents is thought to play an important role in spatial memory and learning, as indicated by lesion studies and recordings of neurons active during spatial behavior. Assuming a role of adult neurogenesis in hippocampal function, one might expect high levels of adult neurogenesis in bats, particularly among fruit- and nectar-eating bats in need of excellent spatial working memory. The dentate gyrus of 12 tropical bat species was examined immunohistochemically, using multiple antibodies against proteins specific for proliferating cells (Ki-67, MCM2), and migrating and differentiating neurons (Doublecortin, NeuroD). Our data show a complete lack of hippocampal neurogenesis in nine of the species (Glossophaga soricina, Carollia perspicillata, Phyllostomus discolor, Nycteris macrotis, Nycteris thebaica, Hipposideros cyclops, Neoromicia rendalli, Pipistrellus guineensis, and Scotophilus leucogaster), while it was present at low levels in three species (Chaerephon pumila, Mops condylurus and Hipposideros caffer). Although not all antigens were recognized in all species, proliferation activity in the subventricular zone and rostral migratory stream was found in all species, confirming the appropriateness of our methods for detecting neurogenesis. The small variation of adult hippocampal neurogenesis within our sample of bats showed no indication of a correlation with phylogenetic relationship, foraging strategy, type of hunting habitat or diet. Our data indicate that the widely accepted notion of adult neurogenesis supporting spatial abilities needs to be considered carefully. Given their astonishing longevity, certain bat species may be useful subjects to compare adult neurogenesis with other long-living species, such as monkeys and humans, showing low rates of adult hippocampal neurogenesis.
Highlights
Bats (Chiroptera) are the only mammals capable of active flight and, together with marine mammals (Cetacea), navigate effortlessly in their three-dimensional environments
Adult proliferation of neurons in mammals is thought to be restricted to two regions: a subventricular zone (SVZ) at the rostral end of the lateral ventricles, from where newly formed cells migrate towards the olfactory bulb, and a narrow zone below the granule cells of the dentate gyrus in the hippocampus that forms an integral part of the circuitry of this brain region
The latter approach has largely focused on demonstrating relations between experimentally altered adult hippocampal neurogenesis (AHN) and spatial learning abilities of rodents, variations in neurogenesis being taken as a marker for hippocampal functions
Summary
Bats (Chiroptera) are the only mammals capable of active flight and, together with marine mammals (Cetacea), navigate effortlessly in their three-dimensional environments. The hippocampus is thought to process spatiotemporal relationships as indicated by the presence of neurons active during spatial behavior (‘‘place cells’’) [2,3], the human hippocampus is required for establishing episodic memory. Adult proliferation of neurons in mammals is thought to be restricted to two regions: a subventricular zone (SVZ) at the rostral end of the lateral ventricles, from where newly formed cells migrate towards the olfactory bulb, and a narrow zone below the granule cells of the dentate gyrus in the hippocampus that forms an integral part of the circuitry of this brain region Proliferation of these progenitor cells is coined adult hippocampal neurogenesis (AHN), this term includes cells that later become glial cells.
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