Pronounced Neuroplasticity in the Primary Visual Cortex of the 13-Lined Ground Squirrel during Hibernation

Abstract

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 13-lined ground squirrel ( Ictidomys tridecemlineatus ). We compared neuronal morphology in Golgi-stained samples from male and female hibernating or nonhibernating squirrels. For the hibernating squirrels, the brain tissue was sampled during two different epochs: torpor and intertorpor 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 intertorpor arousal, indicating that on average dendritic arbors grew by 0.75 mm (65%) over ∼1.5 h. No morphological differences between hibernating and nonhibernating 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 in 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.