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Seasonal differences in the morphology and spine density of hippocampal neurons in wild ground squirrels

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Abstract

Seasonally reproducing small mammals often undergo changes in brain anatomy throughout the year. Much of the research on this seasonal neuroplasticity has focused on changes in hippocampus volume and neurogenesis, with relatively little attention paid to neuronal morphology. Here, we test for sex, season and sex–season interaction effects on hippocampal neuron morphology and dendritic spine density in a seasonally reproducing rodent: Richardson’s ground squirrel (Urocitellus richardsonii). We quantified the morphology and spine densities of Golgi-stained pyramidal neurons and granule cells in the hippocampus and tested for differences between sexes and seasons with generalized linear models. Although we found no significant sex differences or sex–season interaction effects on any of our morphological measurements, there were significant differences in neuron morphology and spine density between breeding and non-breeding seasons. In the non-breeding season, ground squirrels had CA1 neurons with longer basal dendrites with more branches than in the breeding season. Non-breeding season animals also had higher apical and basal dendrite spine density in CA1 and CA3 neurons than breeding-season animals. Conversely, the spine densities of CA1 somata and granule cells were higher in breeding than in non-breeding season. These differences in neuron morphology and spine density between breeding and non-breeding seasons likely arise from a combination of activity levels, stress hormones, and photoperiod. Although the functional implications of seasonal changes in hippocampal neuron morphology and spine density are uncertain, our data suggest that ground squirrels may be a good model for understanding seasonal neuroplasticity in mammals.

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The data used in the study are available upon request; please contact the corresponding author.

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Acknowledgements

We wish to thank Rob and Janice Sutherland and Doug Smith for access to their properties, the University of Lethbridge grounds staff for permission to traps squirrels on campus, Russell Hossain for assistance in using the vibratome and the Golgi staining method, Maurice Needham for assistance with microscopy, and David Logue for statistical advice. Funding for this study was provided by grants from the Natural Science and Engineering Research Council (NSERC) [214562]; and Canada Foundation for Innovation [grant numbers 30215, 33598] to ANI.

Funding

Support for this study was provided by grants from the Natural Science and Engineering Research Council (NSERC) [214562]; and Canada Foundation for Innovation [grant numbers 30215, 33598] to ANI.

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  1. Department of Neuroscience, University of Lethbridge, Lethbridge, AB, T1K3M4, Canada

    B. Brinkman, A. Ngwenya, K. Fjordbotten, O. Stephen & A. N. Iwaniuk

  2. School of Anatomical Sciences, Faculty of Health Sciences, University of the Witwatersrand, 7 York Road, Parktown, Johannesburg, 2193, South Africa

    A. Ngwenya

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All the procedures outlined below adhered to the Canadian Council for Animal Care guidelines and were approved by the University of Lethbridge Animal Welfare Committee (Protocol #1502). Permits for collections and research were issued by the Alberta Department of Sustainable Resource Development (permit numbers: 55980, 55981, 53998, 53999, 18-226).

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Brinkman, B., Ngwenya, A., Fjordbotten, K. et al. Seasonal differences in the morphology and spine density of hippocampal neurons in wild ground squirrels. Brain Struct Funct 227, 2349–2365 (2022). https://doi.org/10.1007/s00429-022-02528-4

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