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.

A morphologically distinct granule cell type in the dentate gyrus of the red fox correlates with adult hippocampal neurogenesis

“…Long life expectancy and late development of the hippocampal formation however might require other strategies. We have shown that in long living bats hippocampal neurogenesis in adulthood is the exception (Amrein et al, 2007). In other long-living species such as marmoset monkeys, proliferation occurs on a comparatively low level and also decreases with age (Leuner et al, 2007).…”

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

“…An earlier study of adult neurogenesis in microchiropterans led to the conclusion that the hippocampus of the species studied had absent to low rates of adult neurogenesis (Amrein et al, 2007). While possible reasons for the absence of adult hippocampal neurogenesis are raised, it appears that no specific conclusion is reached.…”

“…While possible reasons for the absence of adult hippocampal neurogenesis are raised, it appears that no specific conclusion is reached. One issue not raised by Amrein et al (2007) was whether the stress of capture/handling of these small mammals may have been an important factor in the lack of adult hippocampal neurogenesis. While Amrein et al (2007) state the the bats were "perfused rapidly after trapping", no estimate of the time that elapsed between trapping and perfusion is provided, thus it is possible that capture stress could pose a serious methodological problem; however, this does not explain the absence of adult hippocampal neurogenesis in the three neotropical bat species obtained from breeding colonies located in Germany, although again, no details regarding handling of these bats prior to perfusion is provided.…”

“…One issue not raised by Amrein et al (2007) was whether the stress of capture/handling of these small mammals may have been an important factor in the lack of adult hippocampal neurogenesis. While Amrein et al (2007) state the the bats were "perfused rapidly after trapping", no estimate of the time that elapsed between trapping and perfusion is provided, thus it is possible that capture stress could pose a serious methodological problem; however, this does not explain the absence of adult hippocampal neurogenesis in the three neotropical bat species obtained from breeding colonies located in Germany, although again, no details regarding handling of these bats prior to perfusion is provided. Given that the microchiropterans have high metabolic rates in comparison to other mammals (Austad and Fischer, 1991), it is possible that even a short period of stress, in the range of minutes, related to capture and handling may have a major effect of the expression of proteins in the microchiropteran brain, and in the case of Amrein et al (2007) lead to a false negative report of the absence of adult hippocampal neurogenesis in bat species -a finding that is becoming entrenched in the neurogenesis literature (e.g.…”

“…Bonfanti and Peretto, 2011;Powers, 2013). Given this potential confound in the study of Amrein et al (2007), we sought to analyze the relationship between capture stress and adult hippocampal neurogenesis in the wild-caught microchiropterans using immunohistochemistry for the doublecortin protein (DCX), an endogenous marker of adult hippocampal neurogenesis (Kempermann, 2012).…”