When the weather closes in and winter threatens to bite, many animals hibernate to see them through the harsh winter months. During hibernation,metabolism is down-regulated by decreasing energy expenditure for long periods and reducing an animal's heart rate and blood flow, causing hypothermia, or torpor. These periods of torpor are periodically interrupted by short intervals of rewarming to euthermia, or normal body temperature. These rapid increases in metabolism and oxygenation can cause physiological stress and cellular damage. Scientists are interested in how animals survive during both torpor and rewarming, but the triggers are not fully understood. One candidate is the brain's hippocampus, as it is one of the first brain areas to regain normal EEG activity as the arousal process begins. This led Ana Magarinos and her colleagues at the Rockefeller University in New York and the Université Louis Pasteur in France to investigate changes in the hippocampus during the stress of torpor and arousal.

Structures within the hippocampus of birds and mammals mediate spatial behaviors such as the storage and retrieval of food within their territory,and the connections between neurons can be altered by repeated stress. During torpor, exploratory behavior such as searching for food halts temporarily, so the research team wondered if this might be caused by reversible changes in hippocampal structure during the stress of hibernation and arousal.

To investigate, they placed wild-caught European hamsters (Cricetus cricetus) in a 7°C cold room on a 24 h cycle of 8 h light and 16 h dark in the late autumn, monitoring hibernation bouts using implanted thermosensitive transmitters that measure body temperature. After normal torpor and arousal bouts were established, they removed the brains from active euthermic, hibernating or recently aroused animals and made slices, staining them to reveal neuronal structures.

To find out if hippocampal structure changed during hibernation, the team first analyzed the length and branching patterns of the neurons' dendrites,which link one neuron to many others and facilitate communication. They discovered that in torpid hamsters a type of hippocampal neuron called CA3 cells, which play a critical role in spatial memory, had shortened dendrites with less complex and less dense branching patterns than in active hamsters. This simplification of neuronal connections could limit excitatory input and be linked to behavioral suppression during torpor. In recently aroused hamsters, however, the dendritic simplification was rapidly reversed and was similar to branching patterns seen in active hamsters.

The team also analyzed the number of visible `spines' on the neurons, which receive synaptic inputs, and synaptic vesicle density, which would tell them how strongly neurons could communicate with each other. Not only were dendritic spines on the post-synaptic CA3 cells smaller, but the pre-synaptic cells sending the signals had fewer synaptic vesicles, further reducing excitatory input to the CA3 neurons. By contrast, they saw no changes in pyramidal neurons which are outside the hippocampus, and are not thought to play a role in hibernation.

The authors suggest that the simplification of dendritic branches helps limit excitatory input during torpor and may also interfere with the processing of incoming information. However, these changes are rapidly reversible, restoring normal connections, and function, during arousal. Research in other labs has shown that rodents perform better in water mazes as day length increases and that there is a direct correlation between hippocampal size and spatial ability. Which means that if you feel slow and stupid in the winter, blame it on your inner hamster!

Magarinos, A. M., McEwen, B. S., Saboureau, M. and Pevet, P.(
). Rapid and reversible changes in intrahippocampal connectivity during the course of hibernation in European hamsters.
Proc. Natl. Acad. Sci. USA