Superposition model predicts EEG occipital activity during free viewing of natural scenes

Abstract

Visual event-related potentials (ERPs) produced by a stimulus are thought to reflect either an increase of synchronized activity or a phase realignment of ongoing oscillatory activity, with both mechanisms sharing the assumption that ERPs are independent of the current state of the brain at the time of stimulation. In natural viewing, however, visual inputs occur one after another at specific subject-paced intervals through unconstrained eye movements. We conjecture that during natural viewing, ERPs generated after each fixation are better explained by a superposition of ongoing oscillatory activity related to the processing of previous fixations, with new activity elicited by the visual input at the current fixation. We examined the electroencephalography (EEG) signals that occur in humans at the onset of each visual fixation, both while subjects freely viewed natural scenes and while they viewed a black or gray background. We found that the fixation ERPs show visual components that are absent when subjects move their eyes on a homogeneous gray or black screen. Single-trial EEG signals that comprise the ERP are predicted more accurately by a model of superposition than by either phase resetting or the addition of evoked responses and stimulus-independent noise. The superposition of ongoing oscillatory activity and the visually evoked response results in a modification of the ongoing oscillation phase. The results presented suggest that the observed EEG signals reflect changes occurring in a common neuronal substrate rather than a simple summation at the scalp of signals from independent sources.