Hippocampal Drift Rate Reflects the Temporal Organization of Memories

Abstract

When freely recalling past events, individuals tend to successively remember stimuli that were studied close together in time—a phenomenon known as temporal clustering. Temporal clustering is thought to occur because stimuli are encoded in relation to a slowly drifting internal context; this internal context representation is then reinstated during recall, leading to clustered recall of stimuli that share a similar internal context. While several lines of evidence implicate the hippocampus in supporting internal context representations, there is limited evidence directly linking hippocampal drift during memory encoding to subsequent temporal clustering during recall. In a human fMRI experiment ( n  = 38; 20 females and 18 males), we sought to influence the rate of internal context change during memory encoding and tested for corresponding effects on (1) temporal clustering and (2) hippocampal drift rate. To influence internal context, we manipulated the rate at which background scenes “switched” while a list of words was encoded. Afterward, subjects freely recalled as many words as possible. While switch rate had no effect on the total number of words recalled, it significantly influenced the degree of temporal clustering. Specifically, a higher switch rate was associated with less temporal clustering. Strikingly, this pattern was mirrored by drift rate in the hippocampus: a higher switch rate was associated with significantly lower hippocampal autocorrelation (more drift). Moreover, individual differences in hippocampal autocorrelation were positively correlated with temporal clustering. Collectively, this suggests that hippocampal drift rate during encoding and temporal clustering during recall each reflects a common internal context representation.