Learned Motor Patterns Are Replayed in Human Motor Cortex during Sleep
- Daniel B. Rubin1,2,
- Tommy Hosman3,4,
- Jessica N. Kelemen1,
- Anastasia Kapitonava1,
- Francis R. Willett5,
- Brian F. Coughlin1,
- Eric Halgren6,
- Eyal Y. Kimchi1,2,
- Ziv M. Williams7,8,
- John D. Simeral3,4,
- Leigh R. Hochberg1,2,3,4,*, and
- Sydney S. Cash1,2,*
- 1Center for Neurotechnology and Neurorecovery, Department of Neurology, Massachusetts General Hospital, Boston, Massachusetts 02114
- 2Harvard Medical School, Boston, Massachusetts 02114
- 3Center for Neurorestoration and Neurotechnology, Department of Veterans Affairs, Providence, Rhode Island 02908
- 4Carney Institute for Brain Science and School of Engineering, Brown University, Providence, Rhode Island 02912
- 5Hughes Medical Institute at Stanford University, Palo Alto, California 94305
- 6Departments of Neurosciences and Radiology, University of California at San Diego, La Jolla, California 92093
- 7Department of Neurosurgery, Massachusetts General Hospital, Boston, Massachusetts 02114
- 8Program in Neuroscience, Harvard-MIT Program in Health Sciences and Technology, Harvard Medical School, Boston, Massachusetts 02115
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Author contributions: D.B.R., T.H., Z.M.W., J.D.S., and L.R.H. designed research; D.B.R., T.H., J.N.K., A.K., Z.M.W., and S.S.C. performed research; D.B.R., T.H., F.R.W., E.H., E.Y.K., J.D.S., L.R.H., and S.S.C. analyzed data; D.B.R. wrote the first draft of the paper; D.B.R., T.H., J.N.K., A.K., F.R.W., B.F.C., E.H., E.Y.K., J.D.S., L.R.H., and S.S.C. edited the paper; D.B.R. wrote the paper; B.F.C., E.Y.K., and J.D.S. contributed unpublished reagents/analytic tools.
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↵*L.R.H. and S.S.C. contributed equally to this work as co-senior authors.
Abstract
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.
- Received October 15, 2021.
- Revision received February 4, 2022.
- Accepted February 28, 2022.
- Copyright © 2022 Rubin et al.
This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
