Exposure-based sequence learning induces backward replay in the human visual cortex

Abstract

ABSTRACTThe brain demonstrates a sustained capacity for cortical plasticity, as extensively studied in task-dependent training contexts. However, the cortical plasticity induced by exposure-based learning has been largely ignored despite its potential significance in promoting generalization and adaptability, thereby allowing individuals to effortlessly apply their knowledge across diverse tasks. One of the key mechanisms underlying the cortical plasticity induced by learning is the replay of learned events, as originally described for rodents and recently identified in humans. In the current study, we recorded magnetoencephalography (MEG) signals to investigate the relationship between exposure-based sequence learning and replay in the human brain. Participants were exposed to a predefined sequence of four motion directions for 30 min, and subsequently presented with start/end motion direction of the sequence as a cue aiming to induce replay of the motion sequence. During the post-cue blank period, we observed a backward replay of the motion sequence in a time-compressed manner. These effects were marginally significant even for a very brief exposure. However, when we flashed the second or third motion direction of the sequence as a cue, no replay events were observed. Further analyses revealed that activity in the medial temporal lobe (MTL) preceded the ripple power in the visual cortex at replay onset, implying a potentially coordinated relationship between the activity in the MTL and visual cortex. Taken together, our study demonstrated the rapid development of replay events induced by simple visual exposure in humans, providing new insights into the mechanisms underlying cortical plasticity even without explicit training tasks.