Entrainment of traveling waves to rhythmic motor acts

Abstract

We hypothesized that rhythmic motor acts entrain neural oscillations in speech production brain regions. We tested this hypothesis in an experiment where a subject produced consonant-vowel (CV) syllables in a rhythmic fashion, while we performed ECoG recordings. Over the ventral sensorimotor cortex (vSMC) we detected significant concentration of phase across trials at the specific frequency of speech production. We also observed amplitude modulations. In addition we found significant coupling between the phase of brain oscillations at the frequency of speech production and their amplitude in the high-gamma range (i.e., phase-amplitude coupling, PAC). Furthermore, we saw that brain oscillations at the frequency of speech production organized as traveling waves (TWs), synchronized to the rhythm of speech production. It has been hypothesized that PAC is a mechanism to allow low-frequency oscillations to synchronize with high-frequency neural activity so that spiking occurs at behaviorally relevant times. If this hypothesis is true, when PAC coexists with TWs, we expect a specific organization of PAC curves. We observed this organization experimentally and verified that the peaks of high-gamma oscillations, and therefore spiking, occur at the same times across electrodes. Importantly, we observed that these spiking times were synchronized with the rhythm of speech production. To our knowledge, this is the first report of motor actions organizing (a) the phase coherence of low-frequency brain oscillations, (b) the coupling between the phase of these oscillations and the amplitude of high-frequency oscillations, and (c) TW. It is also the first demonstration that TWs induce an organization of PAC so that spiking across spatial locations is synchronized to behaviorally relevant times.