Alpha oscillations in early visual cortex support visual search through inhibition of neuronal excitability to Target and Distractor features

Abstract

Visual search models typically employ priority maps guiding attention towards Targets and away from Distractors. Ventral stream neurons have been shown to respond more strongly to Targets than Distractors, however it is debated whether neurons in early visual regions are similarly modulated. Neuronal alpha oscillations have long been suggested to inhibit Distractors, yet it has not been established if they contribute to the priority map. Here, we show that feature guidance modulates neuronal excitability in early visual regions (V1/V2). Importantly, we demonstrate that alpha oscillations in V1 facilitate search through functional inhibition. These results were obtained by exploiting the good spatio-temporal resolution of MEG and a novel high-frequency tagging approach (Rapid Invisible Frequency Tagging, RIFT). Using RIFT, we probed the neuronal excitability to a blue or yellow Target among blue and yellow Distractors in a classic visual search paradigm, when colour was a guiding feature or was irrelevant (unguided search). The colours were tagged at 60 and 67 Hz, respectively, making the flicker unperceivable. The RIFT responses (in V1/V2) to the Target colour were significantly enhanced whereas responses to Distractors were reduced in guided compared to unguided search. Importantly, strong alpha power in the early visual cortex before the onset of the search display predicted faster search times for guided and unguided searches. Alpha power also predicted reduced RIFT responses to all stimuli. Our results link feature guidance to gain modulation in V1/V2. This suggests that the priority map affects neuronal activity in early visual regions. Furthermore, we show that alpha oscillations in V1 are associated with enhanced performance and reduced neuronal excitability. We propose that functional inhibition by alpha oscillations sets a threshold on all stimuli. As alpha power decreases with the search display onset, it allows the boosted Targets to overcome the inhibition, enabling a more efficient search.