Abstract Gamma band synchronization can facilitate local and long-range communication in neural circuits. In the primary visual cortex (V1) the strength of synchronization on the local level is strongly tuned to the contrast, size and center/surround orientation of grating stimuli. On the global level, the synchronization of gamma oscillations across the retinotopic map crucially depends on matched stimulus properties in the corresponding locations in the visual field. Although these features of V1 gamma rhythms are likely to be crucial for how they might support cortico-cortical communication and visual perception, their neural basis remains largely unknown. We hypothesized VIP disinhibitory interneurons, which shape other tuning properties in V1 by inhibiting SST neurons, may be responsible for tuning local gamma band power and global gamma synchronization. To test these ideas, we combined multi-electrode electrophysiology, cell-type specific optogenetic suppression of VIP neurons and computational modeling. Contrary to expectations, our data show that on the local level, VIP activity has no role in tuning gamma power to stimulus properties; rather, it scales the gain of gamma oscillations linearly across stimulus space and across behavioral state. Conversely, on the global level, VIP neurons specifically suppress gamma synchronization (as measured by spectral coherence) between spatially separated cortical ensembles when they are processing non-matched stimulus features. A straightforward computational model of V1 shows that like-to-like connectivity across retinotopic space, and specific, but powerful VIP➔SST inhibition are sufficient to capture these seemingly opposed effects. These data demonstrate how VIP neurons differentially impact local and global properties of gamma rhythms depending on the global statistics of the retinal image. VIP neurons may thus construct temporal filters in the gamma band for spatially continuous image features, such as contours, to facilitate the downstream generation of coherent visual percepts.

Cortical VIP neurons locally control the gain but globally control the coherence of gamma band rhythms