Optogenetic activation of the inhibitory nigro-collicular circuit evokes contralateral orienting movements in mice

We report that increasing inhibition from the basal ganglia (BG) to the superior colliculus (SC) through the substantia nigra pars reticulata (nigra) using in vivo optogenetic activation of GABAergic terminals in mice produces contralateral orienting movements. These movements are unexpected because decreases, and not increases, in nigral activity are generally associated with the initiation of orienting movements. We found that, in slice recordings, the same optogenetic stimulation of nigral terminals producing movements in vivo evokes post-inhibitory rebound depolarization followed by Na⁺ spikes in SC output neurons. Moreover, blocking T-type Ca²⁺ channels in slices prevent post-inhibitory rebound and subsequent Na⁺ spiking in SC output neurons and also reduce the likelihood of contralateral orienting in vivo. On the basis of these results, we propose that, in addition to the permissive role, the BG may play an active role in the generation of orienting movements in mice by driving post-inhibitory rebound depolarization in SC output neurons.