Temporal Indexing of Motor Memory

Abstract

Humans must store and retrieve distinct implicit motor memories in different contexts. Recent research has revealed the motor adaptation system's sensitivity to contextual cues related to posture, spatial goals, and visual inputs. However, to date, the role of one critical variable in implicit motor memory retrieval - the passage of time - remains underexplored, even though it is arguably more fundamental. Here we ask if different temporal intervals can act as effective contextual cues for retrieving competing motor adaptation memories at the subsecond level. We combined a visuomotor dual adaptation paradigm with a 'set-go' task to link opposite perturbation contexts with different movement preparation intervals. The preparation intervals (and their associated perturbations) were randomly interleaved during training, leading to consistent interference. After training, a testing phase revealed robust contextual modulation effects, such that distinct implicit motor memories were retrieved based on the time elapsed during the pre-movement preparatory interval. These contextual memory effects generalized to novel preparatory intervals in a highly structured fashion. Contextual motor memory separation was seen both when elapsed time had to be internally tracked (high uncertainty) and when it was aided by visual and symbolic cues (low uncertainty). Learning and generalization data across experiments could be parsimoniously explained by a computational model that indexed motor memories via a cerebellar granule-cell-like temporal basis set that tiled the delay interval. Our findings suggest that intrinsic timing processes in the cerebellum may function to index motor memories and generalize those memories to new temporal contexts.