Absent or low rate of adult neurogenesis in the hippocampus of bats (Chiroptera)

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.

Figure 1. Phylogenic tree of all extant bat families.

Names of species included in this study in brackets behind the corresponding family (adapted from Teeling et al. 2005 [43]).

Figure 2. Proliferating and migrating young neurons in the hippocampus of four representative bat species.

In the dentate gyrus of nectar and fruit eating Phyllostomus discolor (A,E,I) as well as in the insectivorous Hipposideros cyclops (B,F,J) we did not detect any proliferating cells with antibodies against Ki-67 (A,B) and MCM2 (E,F), no migrating new neurons can be found with antibody agains DCX (I,J). In contrast, in the sister species Hipposideros caffer (C,G,K) and in Mops condylurus (D,H,L), proliferating as well as migrating cells can be detected in the subgranular layer of the hippocampus (Ki-67: C,D; MCM2: G,H; DCX: K,L) Molecular layer in all examples on the right side of the granule cell layer, arrows indicate immuno­positive cells. Scale bar is 20µm.

Figure 3. Neurogenesis is not abolished in the rostral migratory stream; NeuroD immunoreactivity has an irregular distribution.

Examples of proliferating cells in the rostral migratory stream detected with antibody against Ki-67 (A–D) as well as their neuronal fate visualized with DCX (E–H) are illustrated for Phyllostomus discolor (A,E), Hipposideros cyclops (B,F), Hipposideros caffer (C,G), and Mops condylurus (D,H). Thus, animals with and without hippocampal neurogenesis do not differ in their neurogenetic activity in the rostral migratory stream. In Phyllostomus discolor, all granule cells in the hippocampus are positive for NeuroD (I), in Hipposideros cyclops (J), Hipposideros caffer (K) and Mops condylurus (L) no reactivity to the antibody against NeuroD could be detected. Scale bar is 20µm.

Figure 4. Mice and bats show similar proliferation activity in the RMS, but not in the hippocampus.

Immunohistochemistry against Ki-67 in wild trapped adult wood mouse (Apodemus flavicollis: A,C,D) shows intense proliferation activity in the RMS (A, insert C) as well as in the subgranular layer of the dentate gyrus (A, insert D). The same protocol applied to a neotropical bat (Phyllostomus discolor: B,E,F) visualizes a continuous band of proliferating cells along the RMS (B, insert E), but proliferating cells are completely missing in the granule cell layer (B, insert F). Scale bar in A,B is 1mm, in C-F 25µm.