High frequency phase-spike synchronization of extracellular signals modulates causal interactions in monkey primary visual cortex

Functional correlates of Rhythms in the gamma band (30-100Hz) are observed in the mammalian brain with a large variety of functional correlates. Nevertheless, their functional role is still debated. One way to disentangle this issue is to go beyond usual correlation analysis and apply causality measures that quantify the directed interactions between the gamma rhythms and other aspects of neural activity. These measures can be further compared with other aspects of neurophysicological signals to find markers of neural interactions. In a recent study, we analyzed extracellular recordings in the primary visual cortex of 4 anesthetized macaques during the presentation of movie stimuli using a causality measure named Transfer Entropy. We found causal interactions between high frequency gamma rhythms (60-100Hz) recorded in different electrodes, involving in particular their phase, and between the gamma phase and spiking activity quantified by the instantaneous envelope of the MUA band (1-3kHz). Here, we further investigate in the same dataset the meaning of these phase-MUA and phase-phase causal interactions by studying the distribution of phases at multiple recording sites at lags around the occurrence of spiking events. First, we found a sharpening of the gamma phase distribution in one electrode when spikes are occurring in other recording site. This phenomena appeared as a form of phase-spike synchronization and was quantified by an information theoretic measure. We found this measure correlates significantly with phase-MUA causal interactions. Additionally, we quantified in a similar way the interplay between spiking and the phase difference between two recording sites (reflecting the well-know concept of phase synchronization). We found that, depending on the couple of recording site, spiking can correlate either with a phase synchronization or with a desynchronization with respect to the baseline. This effect correlates very well with the phase-phase causality measure. These results provide evidence for high frequency phase-spike synchronization to reflect communication between distant neural populations in V1. Conversely, both phase synchronization or desynchronization may favor neural communication between recording sites. This new result, which contrasts with current hypothesis on the role of phase synchronization, could be interpreted as the presence of inhibitory interactions that are suppressed by desynchronization. Finally, our findings give new insights into the role of gamma rhythms in regulating local computation in the visual cortex