Phase-locking saccades to posterior alpha oscillations improves the neural representation of visual objects during memory formation

Abstract

Visual memory formation begins with the intake and neural processing of discrete samples provided by gaze fixations and saccades. Past research has highlighted a functional relationship between the timing of saccades and oscillations in neural activity over posterior brain areas: saccades phase-lock to alpha oscillations (8-12 Hz) and the degree of phase-locking, in natural scenes, has been associated with subsequent recognition memory. Here, we tested the hypothesis that the putative memory encoding benefit arises due to improved neuronal processing and, ultimately, better neural representation of foveated items, when saccades are locked to alpha phase. In a co-registered magnetoencephalography (MEG) and eye-tracking paradigm, participants executed saccades from central fixation to images that appeared in the periphery, attempting to remember those images for later testing. Replicating past results, saccades to subsequently remembered images were preceded by greater inter-trial phase coherence in the alpha frequency band, at posterior MEG channels, consistent with the notion that the eye movements were phase-locked. Across participants, the degree of saccade phase-locking was positively correlated with how well visual and semantic properties of the images were represented in neural activity, within 200 ms of their foveation. This relationship was evident in responses localized to the left parieto-occipital and ventral temporal cortex, where greater saccade phase-locking was associated with improved visual and semantic representations, respectively. These results support the hypothesis that phase-locking saccades to alpha oscillations leads to improved neuronal representation of foveated stimuli, providing new mechanistic insight into how episodic memories are formed from discrete visual samples. Significance StatementVisual memories begin with discrete samples provided by eye movements and gaze fixations, from which the brain must extract information that is integrated into a coherent memory trace. This work examined the neural mechanisms that support this memory formation process, one eye movement at a time. The results identified a functioning coupling between saccade timing and neuronal oscillations in the alpha frequency band: when saccades are phase-locked to alpha oscillations, the brain can better process the visual information provided by gaze fixations. This indicates that precise coordination of saccade timing, with respect to neuronal oscillations, promotes more veridical neural representation of the resulting visual samples, from which accurate episodic memories can be constructed.