Eye Movements Actively Reinstate Spatiotemporal Mnemonic Content

Abstract

Eye movements support memory encoding by binding distinct elements of the visual world into coherent representations. However, the role of eye movements in memory retrieval is less clear. We propose that eye movements play a functional role in retrieval by reinstating the encoding context. By overtly shifting attention in a manner that broadly recapitulates the spatial locations and temporal order of encoded content, eye movements facilitate access to, and reactivation of, associated details. Such mnemonic gaze reinstatement may be obligatorily recruited when task demands exceed cognitive resources, as is often observed in older adults. We review research linking gaze reinstatement to retrieval, describe the neural integration between the oculomotor and memory systems, and discuss implications for models of oculomotor control, memory, and aging.

The intersection between the oculomotor and hippocampal memory systems: empirical developments and clinical implications

“…When considering the findings from Liu and colleagues 151 that showed an age-related increase in visual exploration in the face of decreased hippocampal engagement, we suggest that eye movements not only passively reveal the contents of memory, but they may also be a mechanism for actively supporting memory encoding and retrieval, mediated through the vast neural architecture that connects the two systems. 101,151,156,157 The purpose of eye movements…”

“…162 We have proposed that eye movements play a functional role at retrieval by generally reinstating the broad spatiotemporal encoding context in accordance with task demands and available cognitive resources (gaze reinstatement). 157 That is, eye movements are not simply another example of an effector system that passively reflects the outcome of memory retrieval, such as is the case with a button press or verbal response. Rather, eye movements may fundamentally contribute to the retrieval of information as it unfolds.…”

“…206,207 Such findings are aligned with the aforementioned purported function of eye movements during retrieval: to reinstate the spatiotemporal context of memories. 157 If the manner by which visual exploration occurs is important for reconstructing the details of memory, then disrupting visual exploration through repetitive lateral saccades (or stereotyped viewing patterns in general) should alter the engagement of the hippocampus and associated network, and disrupt the reestablishment of the specific spatial and temporal relations that serve as the foundation for recalling further associated details. The therapeutic benefits of alternating bilateral visual stimulation (not necessarily the movement of the eyes itself) have been associated with increased responses in the SC-mediodorsal thalamus circuit in the rodent.…”

Eye movements support behavioral pattern completion

“…Thus, to evaluate this claim more directly, the present study used eye movement (EM) monitoring to measure the overlap between participant-and stimulus-specific gaze patterns during encoding and retrieval (visualization) of degraded lure stimuli as a predictor of memory performance. Whereas behavioral responses reflect the outcome of an underlying retrieval process, EM-based reinstatement has been linked to the online maintenance and retrieval of relational information (for review, see Wynn, Shen, & Ryan, 2019), making it a powerful tool to assess reactivation.…”

“…Eye movements provide a unique window into cognitive processes as they unfold in time (for review, see Hannula, Althoff, Warren, Riggs, & Cohen, 2010). Research using EM monitoring suggests that EMs are involved in the binding of stimulus features into cohesive memory representations during encoding, and the retrieval of those features and the relations among them during retrieval (for review, see Hannula et al, 2010Hannula et al, , 2007Wynn, Shen, et al, 2019). For example, whereas fixed viewing impairs memory (Armson, Ryan, & Levine, 2019;Bochynska & Laeng, 2015;Henderson, Williams, & Falk, 2005;Johansson, Holsanova, Dewhurst, & Holmqvist, 2012;Johansson & Johansson, 2013), spontaneous gaze shifts to regions corresponding with previously encoded (i.e., viewed) image features has been shown to facilitate reactivation of those features and the relations among them (Noton & Stark, 1971a, 1971b; for review, see Wynn, Shen, et al, 2019).…”