Saccades and pre-saccadic stimulus repetition alter cortical network topology and dynamics: evidence from EEG and graph theoretical analysis

Abstract

Parietal and frontal cortex are involved in saccade generation, but their output signals also modify visual signals throughout cortex. These signals produce well-documented behavioral phenomena (saccades, saccadic suppression, various perisaccadic perceptual distortions) but their underlying influence on cortical network dynamics is not known. Here, we combined electroencephalography (EEG) with frequency-dependent source localization and graph theory analysis (GTA) to understand how saccades and pre-saccadic visual stimuli interactively alter cortical network dynamics in humans. 21 participants viewed series of 1-3 vertical or horizontal grids, followed by grid with the opposite orientation just before a horizontal saccade or continued fixation. EEG signals from the presaccadic interval (cue + 200ms, or equivalent fixation period) were used for source localization. Source localization (saccade - fixation) identified bilateral dorsomedial frontoparietal activity across frequency bands, whereas stimulus repetition produced band-specific modulations in left prefrontal, posterior parietal, and central-superior frontal and/or parietal cortex, with significant saccade-repetition interactions in frontal and parietal regions. GTA analysis revealed a saccade-specific functional network with major hubs in inferior parietal cortex (alpha) and the frontal eye fields (beta), and major saccade-repetition interactions in left prefrontal (theta) and supramarginal gyrus (gamma). Overall, quantitative measures of whole-brain network topology and dynamics (segregation, integration, synchronization, complexity) were enhanced during the presaccadic interval, but repetition interactions reduced synchronization and complexity. These results show that presaccadic signals have widespread, coherent influence on cortical network dynamics, likely responsible for both saccade production and the perceptual phenomena associated with saccades. HighlightsO_LISource localization & graph theory were used to analyze presaccadic EEG signals C_LIO_LIPresaccadic signals produced band-specific modulations/hubs in parietofrontal cortex C_LIO_LIFrontal/parietal eye fields showed extensive functional connectivity across all lobes C_LIO_LIPresaccadic stimulus repetition further modulated functional network connectivity C_LIO_LISaccades and repetition both influenced network clustering, integration, & complexity C_LI