Adult neurogenesis in the brain of chiroptera
Date
2016
Authors
Chawana, Richard
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Abstract
The current thesis, studying adult neurogenesis in the brains of Chiroptera (bats), is a
collection of four related studies investigating the occurrence of neurogenesis in the two
suborders of adult bats, megachiroptera (megabats) and microchiroptera (microbats), from
different environments, including the wild and captive habitats. The studies were carried out in
order to understand the dynamics associated with adult neurogenesis in mammals living in their
natural habitat given that much of the current understanding is based on experiments done on
laboratory bred or captive raised animals. The investigation of megachiropterans and
microchiropterans was stimulated by the findings of a previous study which failed to show adult
neurogenesis in some microchiropteran species, which is in contrast to the almost universal
occurrence of the phenomenon in nearly all mammals. In addition, the use of chiropterans was
appealing given their behavioural attributes, which have been previously associated with the
occurrence of neurogenesis. These include such behaviours as good spatial abilities, high
sociality and complex behaviours such as fusion-fission sociality. In addition, the highly
debatable evolutionary history of chiropterans provided a framework in which to evaluate
specific neural characters in terms of phylogenetic relationships.
Using immunohistochemical methods, the presence and characteristics of proliferating
and newly generated neurons in the brain of eight wild-caught adult megachiropteran species
was examined. For the neurogenic patterns observed, direct homologies were evident in other
mammalian species. Numerous proliferating cells and immature neurons were identified in the
subventricular zone (SVZ) and the dentate gyrus. From the SVZ, these cells migrated to the
olfactory bulb through a typically mammalian rostral migratory stream (RMS). Some newlygenerated
cells were observed emerging from the RMS to the neocortex. Similar to primates,
proliferating cells and immature neurons were identified in the SVZ of the temporal horn of the
lateral ventricle of the megachiropterans and were observed to migrate to the rostral and caudal
piriform cortex through a primate-like temporal migratory stream.
A similar study using three microchiropteran species revealed almost similar findings.
However, distinct differences to the megachiropterans were noted, especially so in the migratory
pathway to the piriform cortex, where cells appeared to migrate from the RMS through an
insectivore-like ventral migratory stream to populate the entire piriform cortex. In addition
microchiropterans had immature axons in the anterior commissure, something which was not
observed in megachiropterans but was previously reported in insectivores.
Using immunohistochemical and stereological methods, the effect of animal capture and
handling on the occurrence of adult neurogenesis in 10 microchiropterans species was
investigated. These animals were euthanized and perfusion fixed at specific time points
following capture to investigate the effect of stress as a possible explanation for the negative
findings regarding adult hippocampal neurogenesis in microchiropterans reported in a previous
study. This investigation revealed that when euthanized and perfused within 15 minutes of
capture, abundant putative adult hippocampal neurogenesis could be detected using doublecortin
immunohistochemistry, but the ability to readily observe these cells rapidly diminishes if the
microchiropterans have not been euthanased within 15 minutes of capture.
Also using immunohistochemical and stereological methods, proliferative and immature
cells within the dentate gyrus of adult Egyptian fruit bats from three distinct environments (fifth
generation captive bred, wild-caught from the primary rainforest of central Africa and wildcaught
from the South African woodlands) was quantified and compared. Four previously
reported methods to assess the effect of the environment on proliferative and immature cells
were used. These include: (1) the comparison of raw totals of proliferative and immature cells;
and these totals standardized to (2) brain mass, (3) the volume of the granular cell layer (GCL),
and (4) the total number of granule cells in the dentate gyrus. For all methods, the numbers of
proliferative cells did not differ statistically amongst the three groups. For the immature cells
standardizations to brain mass and GCL volume revealed no difference between the three groups
studied; however, the raw numbers and standardization to total granule cell numbers indicated
that the two groups of wild-caught bats had significantly higher numbers of immature neurons
than the captive-bred bats.
In conclusion, the observation of the ventral migratory stream in the microchiropterans
and insectivores, in contrast to the temporal migratory stream in megachiropterans and primates
adds another neural characteristic supporting the diphyletic origin of Chiroptera, and aligns
microchiropterans with insectivores and megachiropterans with primates. In microchiropterans,
the presence of doublecortin, revealing adult neurogenesis, in the hippocampus is highly
sensitive to capture and handling. Lastly, the interpretation of the effect of the environment on
the numbers of immature neurons appears method dependent. It is possible that current methods
are not sensitive enough to reveal the effect of different environments on proliferative and
immature cells.
Description
A thesis submitted to the Faculty of Health Sciences, University of the Witwatersrand,
Johannesburg, in fulfillment of the requirements for the degree of Doctor of Philosophy.
April, 2016