Episodic memory formation in unrestricted viewing

Abstract

The brain systems of episodic memory and oculomotor control are tightly linked, suggesting a crucial role of eye movements in memory. But little is known about the neural mechanisms of memory formation across eye movements in naturalistic viewing behavior. Here, we leverage simultaneous recording and analysis of eye movements and EEG to examine the formation of episodic memory in free viewing. We designed a stimulus screen with multiple elements that together comprised an event. Participants were asked to memorize several of these events while their EEG and eye movements were concurrently recorded. A subsequent cued-recall test assessed participants' memory for the element associations that specified each event. We overcame the problem of overlapping EEG responses to sequential saccades in free viewing using a deconvolution approach. We segmented EEG relative to the fixation onsets and examined EEG power in the theta and alpha frequency bands, the putative oscillatory correlates of episodic encoding mechanisms. We found that high subsequent memory performance was predicted by three modulations of fixation-related EEG: 1) theta synchronization at fixations after saccades relevant to event integration, 2) theta synchronization at fixations after within-element scrutinizing saccades, 3) alpha desynchronization at fixations after saccades between elements that were incidental to the task. Thus, event encoding with unrestricted viewing behavior was characterized by three neural mechanisms, manifested in fixation-locked theta and alpha EEG activity that rapidly turned on and off during the unfolding eye movement sequences. These three distinct neural mechanisms may be the essential building blocks that subserve the buildup of coherent episodic memories during naturalistic viewing behavior.