Consolidation of memory is believed to involve offline replay of neural activity. While amply demonstrated in rodents, evidence for replay in humans, particularly regarding motor memory, is less compelling. To determine whether replay occurs after motor learning, we sought to record from motor cortex during a novel motor task and subsequent overnight sleep. A 36-year-old man with tetraplegia secondary to cervical spinal cord injury enrolled in the ongoing BrainGate brain–computer interface pilot clinical trial had two 96-channel intracortical microelectrode arrays placed chronically into left precentral gyrus. Single- and multi-unit activity was recorded while he played a color/sound sequence matching memory game. Intended movements were decoded from motor cortical neuronal activity by a real-time steady-state Kalman filter that allowed the participant to control a neurally driven cursor on the screen. Intracortical neural activity from precentral gyrus and 2-lead scalp EEG were recorded overnight as he slept. When decoded using the same steady-state Kalman filter parameters, intracortical neural signals recorded overnight replayed the target sequence from the memory game at intervals throughout at a frequency significantly greater than expected by chance. Replay events occurred at speeds ranging from 1 to 4 times as fast as initial task execution and were most frequently observed during slow-wave sleep. These results demonstrate that recent visuomotor skill acquisition in humans may be accompanied by replay of the corresponding motor cortex neural activity during sleep.

SIGNIFICANCE STATEMENT Within cortex, the acquisition of information is often followed by the offline recapitulation of specific sequences of neural firing. Replay of recent activity is enriched during sleep and may support the consolidation of learning and memory. Using an intracortical brain–computer interface, we recorded and decoded activity from motor cortex as a human research participant performed a novel motor task. By decoding neural activity throughout subsequent sleep, we find that neural sequences underlying the recently practiced motor task are repeated throughout the night, providing direct evidence of replay in human motor cortex during sleep. This approach, using an optimized brain–computer interface decoder to characterize neural activity during sleep, provides a framework for future studies exploring replay, learning, and memory.

记忆的巩固被认为涉及神经活动的离线重放。虽然在啮齿类动物身上得到了充分证明，但人类重放的证据，特别是关于运动记忆的证据，却不太引人注目。为了确定运动学习后是否会发生重放，我们试图在新的运动任务和随后的夜间睡眠期间记录运动皮层的情况。一名因颈脊髓损伤继发四肢瘫痪的 36 岁男性参加了正在进行的 BrainGate 脑机接口试点临床试验，他将两个 96 通道皮质内微电极阵列长期放置在左中央前回中。当他玩颜色/声音序列匹配记忆游戏时，记录了单单元和多单元活动。通过实时稳态卡尔曼滤波器从运动皮层神经元活动中解码预期的运动，该滤波器允许参与者控制屏幕上的神经驱动光标。夜间在他睡觉时记录了中央前回的皮质内神经活动和 2 导联头皮脑电图。当使用相同的稳态卡尔曼滤波器参数进行解码时，过夜记录的皮质内神经信号会每隔一段时间重播记忆游戏中的目标序列，其频率明显高于偶然预期。重放事件发生的速度是初始任务执行速度的 1 到 4 倍，并且在慢波睡眠期间最常观察到。这些结果表明，人类最近获得视觉运动技能可能伴随着睡眠期间相应运动皮层神经活动的重放。

意义陈述在皮层内，信息的获取通常伴随着特定神经放电序列的离线重演。最近活动的重播在睡眠期间得到丰富，并可能有助于巩固学习和记忆。当人类研究参与者执行一项新的运动任务时，我们使用皮质内脑机接口记录并解码了运动皮层的活动。通过解码整个睡眠期间的神经活动，我们发现最近练习的运动任务背后的神经序列在整个晚上都会重复，这提供了睡眠期间人类运动皮层重播的直接证据。这种方法使用优化的脑机接口解码器来表征睡眠期间的神经活动，为未来探索重播、学习和记忆的研究提供了一个框架。