Environmental Influences on Spatial Memory and the Hippocampus in Food-Caching Chickadees

Abstract

Cognitive abilities have been widely considered as a buffer against environmental harshness and instability, with better cognitive abilities being especially crucial for fitness in harsh and unpredictable environments. Although the brain is considered to be highly plastic and responsive to changes in the environment, the extent of such environment-induced plasticity and the relative contributions of natural selection to the frequently large variation in cognitive abilities and brain morphology both within and between species remain poorly understood. Food-caching chickadees present a good model to tackle these questions because they: (a) occur over a large gradient of environmental harshness largely determined by winter climate severity, (b) depend on food caches to survive winter and their ability to retrieve food caches is, at least in part, reliant on hippocampus-dependent spatial memory, and (c) regularly experience a distinct seasonal cycle of food caching and cache retrieval. Here we review a body of work, both comparative and experimental, on two species of food-caching chickadees and discuss how these data relate to our understanding of how environment-induced plasticity and natural selection generate environment-related variation in spatial memory and the hippocampus, both across populations as well as across seasons within the same population. We argue that available evidence suggests a relatively limited role of environmentinduced structural hippocampal plasticity underlying population variation. At the same time, evidence is consistent with the history of natural selection due to differences in winter climate severity and associated with heritable individual variation in spatial memory and the hippocampus. There appears to be no clear direct association between seasonal variation in hippocampus morphology and seasonal variation in demands of food caching. Finally, we suggest that experimental studies of hippocampal plasticity with captive birds should be viewed with some caution because captivity is associated with large reductions in many hippocampal traits, including volume and in some cases neurogenesis rates, but not neuron number. Comparative studies using captive birds, on the other hand, appear to provide more reliable results, as captivity does not appear to override population differences, especially in the number of hippocampal neurons. A key evolutionary question for understanding how environmental heterogeneity is associated with cognitive abilities concerns the relative contribution of environmentinduced effects (e.g., plasticity) and natural selection acting on heritable cognitive traits as a means of generating environment-related variation in cognition and neural traits (e.g., . At least in humans, there is sufficient evidence that both general cognition and specific cognitive traits are highly heritable and that individual variation in these traits is, at least in part, determined by genetics (e.g., Ando, Ono, & Wright, 2001;Haworth et al., 2010;McGee, 1979;Pedersen, Plomin, Nesselro...

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