Pre-stimulation alpha phase/power and gamma power modulate the strength of feedback and feedforward in human visual areas

Abstract

Primate visual cortical areas are organized in a hierarchical manner. Recent laminar studies in monkey visual cortex showed that alpha oscillations tend to propagate in the feedback direction and gamma oscillations in the feed-forward direction. Granger causality analysis in human magnetoencephalography showed that oscillations in these two frequency bands were similarly able to characterize the hierarchical cortical organization. Direct evidence for distinct frequency bands in feedforward and feedback information transfer in human cortex, however, is still lacking. Here, by studying stereoencephalography (sEEG) cortico-cortical evoked potential (CCEP) recordings from electrodes implanted in intact brain regions of epileptic patients, we investigated (1) whether alpha and gamma oscillations can characterize feedforward and feedback processing in human visual areas, and (2) if so, how they modulate the neural activities in lower or higher visual areas. Specifically, micro-stimulations were applied to sEEG electrodes in a stimulation site, while significant post-stimulation responses were measured at sEEG electrodes in response sites. Depending on the anatomical locations of the stimulation and response site electrodes, 406 feedforward pairs and 176 feedback pairs were tested in 8 patients. For all pairs, we measured Pearson correlation between pre-stimulation power in the stimulation site and CCEP amplitude in the response site, as well as circular-to-linear correlation between pre-stimulation phase and response amplitude. Results showed that pre-stimulation alpha power negatively modulates response amplitude in the feedback pairs, while pre-stimulation gamma power positively modulates response amplitude in the feedforward pairs. Furthermore, pre-stimulation alpha phase could also significantly modulate response amplitude in the feedback pairs, while no significant pre-stimulation phase effect could be observed at any frequency in the feedforward pairs. Altogether, our results show that alpha oscillatory phase and power and gamma power directly influence the strength of feedback and feedforward connections in human visual areas.

Acknowledgement: ERC Consolidator grant P-CYCLES Number 614244 to RV, Natural Science Foundation of China grant Number 31871138 to QC