VIP neurons desynchronize cortical assemblies

Neural synchronization on fast timescales has been linked to critical aspects of sensation, cognition and action, and impairments in synchronization are associated with neurological disease. Although the strength and spatial scale of neural synchronization varies dramatically with sensory and behavioral context, the circuit mechanisms that regulate the magnitude and spatial spread of neural oscillations are largely unknown. As in humans, monkeys, and cats, we found that in the mouse primary visual cortex (V1) the stimulus properties and behavioral state powerfully modulate gamma band synchronization. To reveal the underlying circuit that mediates this dependence, we used multi-site multi-electrode electrophysiology and cell type specific optogenetic suppression of vasoactive intestinal peptide (VIP) interneurons in awake mice. Our results show that VIP neurons potently control the gain and behavioral state-dependence of gamma band network synchronization by desynchronizing local and global networks on fine time scales. Importantly, VIP neurons preferentially decouple spatially separated cortical ensembles when they are processing non-matched stimulus features. Based on these data, we propose that cortical disinhibition by VIP interneurons fine-tunes the strength and spatial architecture of gamma-oscillating neural assemblies, which may facilitate the downstream generation of coherent visual percepts.