Pronounced Neuroplasticity in the Primary Visual Cortex of the Thirteen-lined Ground Squirrel During Hibernation

Hibernating animals can show neuroplasticity throughout the hibernation season. In ground squirrels, decreased dendritic arborization in the hippocampus, somatosensory cortex, and thalamus during deep hibernation (“torpor”) suggests that this neuroplasticity is a brain-wide phenomenon. However, the degree to which neuroplasticity occurs in the visual system is not clear. While transient retinal changes have been reported during torpor, neuroplasticity beyond the retina remains unknown. Here, we characterized hibernation-related neuroplasticity in the primary visual cortex (V1), the first cortical area to receive visual information, in the thirteen-lined ground squirrel ( Ictidomys tridecemlineatus ). We compared neuronal morphology in Golgi-stained samples from male and female hibernating or non-hibernating squirrels. For the hibernating squirrels, brain tissue was sampled during two different epochs: torpor and inter-torpor arousal. Dendritic arborization decreased during torpor in V1 layer 2/3 pyramidal neurons, manifesting as decreases in dendritic length, number, and complexity. These changes fully reversed during inter-torpor arousal, indicating that on average dendritic arbors grew by 0.75 mm (65%) over ∼1.5 hours. No morphological differences between hibernating and non-hibernating squirrels were apparent when compared 6 months after the hibernation season. We also found no neuroplastic changes in V1 layer 4 spiny stellate neurons, unlike in this cell type the somatosensory cortex. Together, this revealed, for the first time, hibernation-related neuroplasticity in V1 in support of a brain-wide mechanism but with area-specific differences. The speed and magnitude of this naturally occurring neuroplasticity could make ground squirrel V1 a powerful translational model system for conditions requiring neuroplasticity, such as recovery from stroke. Significance Statement This study is the first demonstration of pronounced hibernation-related neuroplasticity in the primary visual cortex of ground squirrels. Layer 2/3 pyramidal neurons in the primary visual cortex (V1) reduced arborization during torpor. Within 1.5 hours after arousal from torpor, the arborization reversed to non-hibernation levels. The extent and speed of this naturally occurring neuroplasticity could make the relatively well-understood V1 of ground squirrels a powerful translational model system. Complementing insights on neuroplasticity in V1 during development, it has the potential to be leveraged for the study of treatment mechanisms and conditions requiring neuroplasticity, ranging from neurodegeneration to recovery after stroke.