Transient enhancement of inhibition following visual cortical lesions in the mouse superior colliculus

Abstract

Numerous studies have investigated the effects of lesions of the primary visual cortex (V1) on visual responses in neurons of the superficial layer of the superior colliculus (sSC), which receives visual information from both the retina and V1. However, little is known about the changes in the local circuit dynamics of the sSC after receiving V1 lesions. Here, we show that surround inhibition of sSC neurons is transiently enhanced following V1 lesions in mice and that this enhancement may be attributed to alterations in the balance between excitatory and inhibitory inputs to sSC neurons. Extracellular recordings in vivo revealed that sSC neuronal responses to large visual stimuli were transiently reduced at about 1 week after visual cortical lesions compared with normal mice and that this reduction was partially recovered at about 1 month after the lesions. By using whole-cell patch-clamp recordings from sSC neurons in slice preparations obtained from mice that had received visual cortical lesions at 1 week prior to the recordings, we found cell type-dependent changes in the balance between excitation and inhibition. In non-GABAergic cells, inhibition predominated over excitation, whereas the excitation-inhibition balance did not change in GABAergic neurons. These results suggest that enhanced inhibition may be partially responsible for the reduced responses to large visual stimuli in some sSC neurons. Thus, we propose that the enhanced surround inhibition shortly after visual cortical lesions may prevent hyperexcitability in the sSC local circuit, contributing to reconstructing the finely tuned receptive field organization of sSC neurons after the visual cortical lesions.