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The Journal of Neuroscience, October 11, 2006, 26(41):10590-10598; doi:10.1523/JNEUROSCI.2874-06.2006

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Development/Plasticity/Repair
Ubiquitous and Temperature-Dependent Neural Plasticity in Hibernators

Christina G. von der Ohe,¹ Corinna Darian-Smith,² Craig C. Garner,³ and H. Craig Heller¹

¹Department of Biological Sciences, Stanford University, Stanford, California 94305-5020, ²Department of Comparative Medicine, Stanford University, Stanford, California 94305-5342, and ³Department of Psychiatry and Behavioral Sciences, Stanford University, Palo Alto, California 94304-5485

Correspondence should be addressed to Christina von der Ohe, Department of Biological Sciences, 371 Serra Mall, Stanford University, Stanford, CA 94305-5020. Email: vonderohe{at}stanford.edu

Hibernating mammals are remarkable for surviving near-freezing brain temperatures and near cessation of neural activity for a week or more at a time. This extreme physiological state is associated with dendritic and synaptic changes in hippocampal neurons. Here, we investigate whether these changes are a ubiquitous phenomenon throughout the brain that is driven by temperature. We iontophoretically injected Lucifer yellow into several types of neurons in fixed slices from hibernating ground squirrels. We analyzed neuronal microstructure from animals at several stages of torpor at two different ambient temperatures, and during the summer. We show that neuronal cell bodies, dendrites, and spines from several cell types in hibernating ground squirrels retract on entry into torpor, change little over the course of several days, and then regrow during the 2 h return to euthermia. Similar structural changes take place in neurons from the hippocampus, cortex, and thalamus, suggesting a global phenomenon. Investigation of neural microstructure from groups of animals hibernating at different ambient temperatures revealed that there is a linear relationship between neural retraction and minimum body temperature. Despite significant temperature-dependent differences in extent of retraction during torpor, recovery reaches the same final values of cell body area, dendritic arbor complexity, and spine density. This study demonstrates large-scale and seemingly ubiquitous neural plasticity in the ground squirrel brain during torpor. It also defines a temperature-driven model of dramatic neural plasticity, which provides a unique opportunity to explore mechanisms of large-scale regrowth in adult mammals, and the effects of remodeling on learning and memory.

Key words: dendrite; spine; hibernation; torpor; temperature; plasticity

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Received July 6, 2006; revised Aug. 17, 2006; accepted Aug. 29, 2006.

Correspondence should be addressed to Christina von der Ohe, Department of Biological Sciences, 371 Serra Mall, Stanford University, Stanford, CA 94305-5020. Email: vonderohe{at}stanford.edu

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