Visual Sampling Predicts Hippocampal Activity

Abstract

Eye movements serve to accumulate information from the visual world, contributing to the formation of coherent memory representations that support cognition and behavior. The hippocampus and the oculomotor network are well connected anatomically through an extensive set of polysynaptic pathways. However, the extent to which visual sampling behavior is related to functional responses in the hippocampus during encoding has not been studied directly in human neuroimaging. In the current study, participants engaged in a face processing task while brain responses were recorded with fMRI and eye movements were monitored simultaneously. The number of gaze fixations that a participant made on a given trial was correlated significantly with hippocampal activation such that more fixations were associated with stronger hippocampal activation. Similar results were also found in the fusiform face area, a face-selective perceptual processing region. Notably, the number of fixations was associated with stronger hippocampal activation when the presented faces were novel, but not when the faces were repeated. Increases in fixations during viewing of novel faces also led to larger repetition-related suppression in the hippocampus, indicating that this fixation-hippocampal relationship may reflect the ongoing development of lasting representations. Together, these results provide novel empirical support for the idea that visual exploration and hippocampal binding processes are inherently linked.

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

“…Moreover, greater sampling behavior during initial viewing was associated with larger reductions in hippocampal activity across subsequent viewings. Such repetition‐related decreases in neural activity (i.e., repetition suppression) have been taken as a proxy for memory formation; thus, visual exploration was related to the development of lasting representations . These findings extended prior eye‐tracking research, which showed that an increase in visual exploration predicts later memory by suggesting that the underlying mechanism for such memory benefits is an increase in hippocampal activity.…”

“…However, other research using a perceptual discrimination task found that hippocampal activity was not related to the overall number of gaze fixations, in contrast with findings from Liu and colleagues . Instead, when features among objects had to be maintained and compared in the moment, hippocampal activity was related to revisitations of just‐sampled regions.…”

“…Given the inverse relationship between the duration and number of gaze fixations when viewing time is fixed, the prediction then would be that the number of gaze fixations would relate positively to hippocampal activity. Liu and colleagues demonstrated this prediction to be correct: the number of gaze fixations made while viewing novel stimuli in a perceptual judgment task was associated with stronger neural responses in the hippocampus (Fig. ).…”

“…Through movements across space and time, eye movements may be an outward manifestation of the hippocampal binding process . That is, saccades and gaze fixations serve as a mechanism to bind distinct elements into a coherent and lasting memory representation . These ideas harken back to early eye tracking research .…”

Rapid improvement of cognitive maps in the awake state

“…We propose that the consolidation and integration of new spatial memories can occur during ongoing task engagement, but might be less efficient than during awake quiescence, possibly due to additional demands on the memory system/hippocampal network. Indeed, the spot‐the‐difference game used in our task group is likely to have resulted in novel memory encoding, and recent findings demonstrate that the number of fixations made during the visual exploration of novel stimuli—as in the spot the difference game—positively predicts hippocampal activity (Liu, Shen, Olsen, & Ryan, ). The hypothesized increased demand/co‐current activity during task engagement may have a quantitative and/or qualitative impact on the coordinated reactivation of place and grid cells, resulting in a diminished improvement in cognitive map accuracy over time.…”