Surface color and predictability determine contextual modulation of V1 firing and gamma oscillations

Abstract The integration of direct bottom-up inputs with contextual information is a canonical motif in neocortical circuits. In area V1, neurons may reduce their firing rates when the (classical) receptive field input can be predicted by the spatial context. We previously hypothesized that gamma-synchronization (30-80Hz) provides a complementary signal to rates, encoding whether stimuli are predicted from spatial context by preferentially synchronizing neuronal populations receiving predictable inputs. Here we investigated how rates and synchrony are modulated by predictive context. Large uniform surfaces, which have high spatial predictability, strongly suppressed firing yet induced prominent gamma-synchronization, but only when they were colored. Yet, chromatic mismatches between center and surround, breaking predictability, strongly reduced gamma-synchronization while increasing firing rates. Differences between colors, including strong gamma-responses to red, arose because of stimulus adaptation to a full-screen background, with a prominent difference in adaptation between M- and L-cone signaling pathways. Thus, synchrony signals whether RF inputs are predicted from spatial context and may encode relationships across space, while firing rates increase when stimuli are unpredicted from the context.