Synchronization of sensory gamma oscillations promotes multisensory communication

Abstract

Rhythmic neuronal activity in the gamma range is a signature of active cortical processing and its synchronization across distant sites has been proposed as a fundamental mechanism of network communication. While this has been shown within sensory modalities, we tested whether crosstalk between the senses relies on similar mechanisms. In two consecutive experiments, we used a task in which human participants (male and female) matched amplitude changes of concurrent visual, auditory and tactile stimuli. In this task, matching of congruent stimuli was associated with a behavioral benefit compared to matching of incongruent stimuli. In the first experiment, we used source-level analysis of high-density electroencephalography (EEG) and observed that cross-modal matching of congruent inputs was associated with relatively weaker coherence between gamma oscillations in early sensory regions. Next, we used bifocal high-definition transcranial alternating current stimulation (hd-tACS) to manipulate the strength of coupling between sensory cortices. Here, we used a lateralized version of the task in which hd-tACS was applied either ipsilateral or contralateral to the hemisphere receiving sensory stimuli. Ipsilateral gamma, but not alpha stimulation slowed responses to congruent trials whereas responding to incongruent trials was not changed by tACS. We speculate that fast responding to congruent stimuli involves decoupling of sensory gamma oscillations, which was prevented by tACS. These results indicate that synchronization of gamma oscillations promotes direct communication between sensory modalities. The framework of coupled gamma oscillations underlying cortical communication might thus be generalizable from processing within sensory streams to interactions between sensory networks. Significance statementCortical gamma oscillations structure segregated neural activity and were suggested to represent a fundamental mechanism of network communication. While there is ample evidence for the role of long-range gamma synchronization in unisensory processing, its significance in multisensory networks is still unclear. We show that direct interactions between sensory cortices rely on synchronization of gamma band activity. To that end, we carried out two consecutive experiments using state-of-the-art high-density electroencephalography (EEG) and high-definition transcranial alternating current stimulation (hd-tACS). By complementing an observational with an interventional method, we provide novel evidence for the role of synchronized gamma oscillations in multisensory communication.