Changes in perceptual sampling contribute to representational drift

Abstract

Gradual changes in neural response patterns to the same stimulus over time, termed representational drift, have been widely observed across cortical areas. Drift is typically attributed to intrinsic neural dynamics driven by synaptic plasticity or turnover. Here we test a complementary hypothesis that drift arises due to systematic changes in behavior such as shifts in attention or gaze. We conducted a longitudinal eye-tracking experiment in which fourteen adults freely viewed naturalistic images across 6 experimental sessions spanning 2-4 weeks, with a subset of images repeated within and across sessions. For each participant, we quantified the similarity of fixation density maps between session pairs using the Wasserstein distance. Fixation patterns became increasingly dissimilar with greater temporal separation between sessions, indicating systematic and directional drift in gaze behavior. To assess whether these behavioral changes could plausibly induce changes in neural representations, we passed fixation-masked images through CORnet-S, a hierarchical deep neural network model of the primate ventral visual stream. Representational distances, quantified as the Frobenius norm of pairwise activation differences, increased with the number of sessions that separated the fixation maps across all four model layers (V1, V2, V4, IT). A kernel-based maximum mean discrepancy test further confirmed that the empirical distribution of representational distances differed significantly from shuffled controls. These findings suggest that small but systematic shifts in the sampling of a visual scene over time are sufficient to cause representational drift in visual cortex. More generally, these results suggest that subtle changes in behavior over time are inevitable, even in simple tasks, and that these changes may be sufficient to drive representational drift in the absence of intrinsic reconfigurations of neural codes. Author summaryIn studies of representational drift in visual cortex, shifts in attention and gaze across repeated stimulus exposures can produce drift-like neural patterns. While the current focus is on contributions of changes in visual sampling to drift, the results raise the possibility that other subtle changes in behavior, many that are hard to quantify, could drive drift in other domains.