Short photoperiods impair spatial learning and alter hippocampal dendritic morphology in adult male white-footed mice (Peromyscus leucopus)

Abstract

Although seasonal changes in brain morphology and function are well established in songbirds, seasonal plasticity of brain structure and function remain less well documented in mammals. Nontropical animals display many adaptations to reduce energy use to survive winter, including cessation of reproductive activities. Because of the high energetic costs of brain tissue, we hypothesized that male white-footed mice (Peromyscus leucopus) would reduce brain size in response to short days as well as regress their reproductive systems. Because short days may decrease hippocampal volume and impair spatial learning and memory in rodents and because of the potential for seasonal plasticity in the hippocampus, we hypothesized that photoperiod alters hippocampal morphology to affect spatial learning and memory. Mice housed in either long or short days for 10 weeks were examined for performance in a water maze; brains were then removed and weighed, and hippocampal volumes were determined. We also measured dendritic morphology and spine density in the CA1, CA3, and dentate gyrus. Short days decreased brain mass and hippocampal volume compared with long days. Short days also impaired long-term spatial learning and memory relative to long days but did not affect sensory discrimination or other types of memory. Short days decreased apical (stratum lacunosum-moleculare) CA1 spine density, as well as increased basilar (stratum oriens) CA3 spine density. Results from this study suggest that photoperiod alters brain size and morphology, as well as cognitive function. Understanding the mechanisms mediating these photoperiod-induced alterations may provide insight for treatment of seasonal cognitive and affective disorders.

Figure 1.

Photoperiod-induced differences in spatial learning (via water maze). A, Latency to reach the hidden platform by block of training. B, Path length to reach the hidden platform by block of training. Each block represents three trials. Long-day, n = 7; short-day, n = 9. ^*p < 0.05.

Figure 2.

Photoperiod-induced differences in water-maze reversal learning and memory after relocation to the hidden platform. A, Latency to reach the relocated hidden platform by block of training. B, Path length to reach the hidden platform by block of training. C, Time spent in each quadrant of the pool including the quadrant in which the platform was hidden in the original hidden-platform trials and the quadrant in which the platform was hidden for the reversal trials. Long-day, n = 7; short-day, n = 9. ^*p < 0.05.

Figure 3.

Effects of photoperiod on dendritic complexity (via Sholl analysis) of hippocampal neurons. A, Pyramidal neuron complexity in the CA1 region (n = 5-10 neurons per brain). B, Pyramidal neuron complexity in the CA3 region (n = 5-10 neurons per brain). C, Granule neuron complexity in the dentate gyrus (n = 10 neurons per brain).

Figure 4.

Effects of photoperiod on spine density on terminal tips of hippocampal dendrites. A, Spine density of apical tips of pyramidal dendrites in CA1 and CA3 regions. B, Spine density of basilar tips of pyramidal dendrites in CA1 and CA3 regions and of granule cells in the dentate gyrus. C, Photomicrographs of apical spines in CA1 of long-day (left) and short-day (right) mice; magnification, 1000×. The dotted line represents the unipolarity of granule cells in the dentate gyrus; n = five 10 μm dendritic segments of spines per neuron. ^*p < 0.05.