Ensemble reactivations during brief rest drive fast learning of sequences

• 成果类型: Article
• 署名作者: Griffin, Sandon; Khanna, Preeya; Choi, Hoseok; Thiesen, Katherina; Novik, Lisa; Morecraft, Robert J.; Ganguly, Karunesh
• 署名单位: University of California System; University of California San Francisco; University of California System; University of California San Francisco; University of California System; University of California San Francisco; University of California System; University of California Davis; University of South Dakota
• 刊物名称: Nature
• ISSN/ISSBN: 0028-3152
• DOI: 10.1038/s41586-024-08414-9
• 发表日期: 2025-02-27
• 关键词: spacing practice sessions; primary motor cortex; movement preparation; ripple oscillations; neuron classes; monkey; replay; roles; consolidation; excitation

摘要

During motor learning, breaks in practice are known to facilitate behavioural optimizations. Although this process has traditionally been studied over long breaks that last hours to days1, 2, 3, 4, 5-6, recent studies in humans have demonstrated that rapid performance gains during early motor sequence learning are most pronounced after very brief breaks lasting seconds to minutes7, 8, 9-10. However, the precise causal neural mechanisms that facilitate performance gains after brief breaks remain poorly understood. Here we recorded neural ensemble activity in the motor cortex of macaques while they performed a visuomotor sequence learning task interspersed with brief breaks. We found that task-related neural cofiring patterns were reactivated during brief breaks. The rate and content of reactivations predicted the magnitude and pattern of subsequent performance gains. Of note, we found that performance gains and reactivations were positively correlated with cortical ripples (80-120 Hz oscillations) but anti-correlated with beta bursts (13-30 Hz oscillations), which ultimately dominated breaks after the fast learning phase plateaued. We then applied 20 Hz epidural alternating current stimulation (ACS) to motor cortex, which reduced reactivation rates in a phase-specific and dose-dependent manner. Notably, 20 Hz ACS also eliminated performance gains. Overall, our results indicate that the reactivations of task ensembles during brief breaks are causal drivers of subsequent performance gains. beta bursts compete with this process, possibly to support stable performance.