The hippocampal formation is a highly plastic brain structure that undergoes structural remodeling in response to internal and external challenges such as metabolic imbalance and repeated stress. We investigated whether the extreme alterations in metabolic status that occur during the course of hibernation in European hamsters cause structural changes in the dendritic arborizations of the CA3 pyramidal neurons and their main excitatory afferents, the mossy fiber terminals (MFT), that originate in the dentate gyrus. We report that apical, but not basal, dendritic trees of Golgiimpregnated CA3 principal neurons are significantly shorter, less branched, and less spiny in hypothermic hamsters compared with active animals. After the induction of arousal from torpor, within 2 h, the apical dendritic lengths, branching patterns, and spine density estimations returned to levels found in active, euthermic hamsters. The ultrastructure of MFT in hibernating hamsters showed a significant reduction in synaptic vesicle density and in the percentage of MFT area covered by spine profiles. Awakened hamsters showed restoration of MFT morphology to that seen in active animals. MFT of torpid animals also showed a significant increase in the percentage area of mitochondrial profiles that remained higher 3 h after induced arousal from hibernation compared with euthermic controls. Thus, the torpid/awakening cycle of the hibernating European hamster causes a rapid and reversible morphological reorganization of intrahippocampal subregions involved in information processing. The reported reductions in morphological connectivity between the dentate gyrus and the CA3 subregions could underlie the cessation of exploratory activity and spatial navigation skills during hibernation.CA3 region ͉ hippocampus ͉ mossy fibers ͉ spines ͉ Golgi impregnation H ibernation is a highly regulated physiological response to adverse environmental conditions characterized by hypothermia and drastic reductions of metabolic rate (1). Hibernating species can adapt to anticipated scarcity in food supply and decreases in ambient temperature by storing food and increasing food intake for several weeks before winter starts (2). Once the animals enter into hibernation, they develop an energy conserving behavior and undergo deep bouts of hypothermia (or torpor) alternated with short euthermic intervals termed periodic arousals (3). By using fat stores as their primary source of energy and reducing carbohydrate metabolism, hibernating mammals sustain vital functions during prolonged periods without feeding and support periodic rewarming during interbout arousals (4).The physiological mechanisms triggering hibernation are very complex and far from being well known. Its seasonal occurrence is primarily regulated by the annual photoperiodic variations, and the neuroendocrine and neural mechanisms involved have been partly identified (5-8). The hippocampus, a target brain region for stressful challenges and adrenal steroids (9), has been postulated as a key structure in th...