Sex and seasonal changes in the rate of cell proliferation in the dentate gyrus of adult wild meadow voles

doi:10.1016/S0306-4522(98)00345-5

Neuroscience

Volume 89, Issue 3, March 1999, Pages 955-964

https://doi.org/10.1016/S0306-4522(98)00345-5 Get rights and content

Abstract

In order to study the neurobiological basis of seasonal changes in hippocampal structure and function, the rate of cell proliferation was examined in male and female wild meadow voles captured during different seasons. We found that the number of [³H]thymidine-labeled cells varied across the seasons and across sex in the meadow vole. Non-breeding female meadow voles had a higher rate of cell proliferation and cell death than males captured during either season or breeding females. These seasonal changes in the female meadow vole were associated with both fluctuating levels of adrenal steroids and gonadal steroids. Estradiol level was highly correlated with both the number of [³H]thymidine-labeled cells and the number of pyknotic cells in female meadow voles, with high levels of estradiol being associated with low levels of cell proliferation and cell death. Corticosterone level was associated with the number of [³H]thymidine-labeled cells in the hilus of female meadow voles. This seasonal change in the number of [³H]thymidine-labeled cells was also related to the overall volume of the hippocampus. At variance with past literature, there was no statistically significant sex difference favoring males in hippocampal volume, although the means were in the predicted direction. In male meadow voles, the number of pyknotic cells was related to testosterone level, with high levels of testosterone being associated with greater levels of cell death in the granular cell layer. There was also a suggestion that the number of [³H]thymidine-labeled cells in the hilus varied seasonally in males, with higher rates of cell proliferation during the breeding season than during the non-breeding season.

In summary, we found that there were large fluctuations across the season in the rate of cell proliferation in the dentate gyrus of adult female meadow voles. Females captured during the non-breeding season had higher rates of cell proliferation in the granule cell layer than females captured during the breeding season. This seasonal fluctuation was related to hormone levels, with high levels of corticosterone and estradiol being related to lower levels of cell proliferation. These seasonal changes in cell proliferation may be related to known changes in spatial learning in the meadow vole and provide insights into changes in the hippocampus that occur in other species, including primates.

Section snippets

Subjects

Adult meadow voles were captured using Sherman traps (H. B. Sherman Traps, Inc., Tallahassee, FL) from the field research center in Millbrook, New York during the months of November, January, April, June and July. Voles were maintained on the same light/dark cycle as the time of capture and were given crimped oats (Agway), and alfalfa pellets (Agway) and tap water ad libitium. Voles were individually housed in polyethylene cages with hardwood bedding. The months of November and January were

Body and brain weight

Regardless of season, males weighed more than females (main effect of sex: F_1,23=5.89, P=0.024). There was also a trend for voles to weigh more in the summer than the winter (main effect of season: F_1,23=4.22, P=0.051). The decrease in weight seen during the non-breeding season is consistent with the findings of Iverson and Turner.[23]There were no statistically significant differences in brain weight. However, when brain weight was corrected for by body weight, female brains weighed more than

Discussion

During the non-breeding season, female meadow voles had a greater density of [³H]thymidine-labeled cells in the granule cell layer of the dentate gyrus than male meadow voles (from either season) or female meadow voles captured during the breeding season. There was also a weak corresponding small change in the number of pyknotic cells across the season in female meadow voles, associated with the change in rate of cell proliferation. The rate of cell proliferation changed across the season in

Conclusion

In conclusion, the results from this study show that dentate gyrus neurogenesis and cell death are related, at least in female meadow voles, to seasonal changes in spatial learning ability. Both cell death and cell proliferation in the dentate gyrus appear to be regulated by multiple factors in male and female meadow voles. In adult female meadow voles, levels of estradiol and corticosterone were negatively related to cell proliferation and to cell death in the dentate gyrus. In male meadow

Acknowledgements

This research was supported by an NSERC post-doctoral fellowship to L.A.M.G. and a NIMH grant to B.S.M. The authors wish to thank Elizabeth Gould, Heather Cameron and Patima Tanapat for their comments and expertise. Part of this research was conducted at The Rockefeller University Field Research Center for Ecology and Ethology in Millbrook, N.Y and the authors gratefully thank Fernando Nottebohm and the staff at the Field Center for their assistance.

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Sex and seasonal changes in the rate of cell proliferation in the dentate gyrus of adult wild meadow voles

Abstract

Section snippets

Subjects

Body and brain weight

Discussion

Conclusion

Acknowledgements

Neuroscience

Neuroscience

Behav. Brain Res.

Horm. Behav.

Brain Res.

Neuroscience

Neuroscience

Neuroscience

Pain

Pain

Brain Res.

Brain Res.

Brain Res.

J. Neurosci. Meth.

Postnatal neurogenesis in the guinea-pig

Nature

Time of neuron origin in the hippocampal region: an autoradiographic study in the mouse

Expl Neurol.

Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees

Proc. natn. Acad. Sci. U.S.A.

Spring declines in Microtus pennsylvanicus and the role of steroid hormones

J. anim. Ecol.

Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus

J. Neurosci.

Oestrus and induced ovulation in the meadow vole, Microtus pennsylvanicus

J. Reprod. Fert.

Chronic subordination stress inhibits neurogenesis and decreases the volume of the granule cell layer

Soc. Neurosci. Abstr.

Sexually-dimorphic spatial learning in meadow voles, Microtus pennsylvanicus and deer mice, Peromyscus maniculatus

J. exp. Biol.

Exposure to predator odor suppresses cell proliferation in the dentate gyrus of adult rats via a cholinergic mechanism

Soc. Neurosci. Abstr.

Sex differences in spatial ability: an evolutionary hypothesis and test

Am. Nature

Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation

J. Neurosci.