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Curr Biol. 2019 Apr 22;29(8):1346-1351.e4. doi: 10.1016/j.cub.2019.02.049. Epub 2019 Mar 28.

A Rapid Form of Offline Consolidation in Skill Learning.

Author information

1
Human Cortical Physiology and Neurorehabilitation Section, National Institute of Neurological Disorders and Stroke, Bethesda, Maryland 20814, USA. Electronic address: marlene.boenstrup@nih.gov.
2
CNBI, Center for Neuroprosthetics (CNP), École Polytechnique Fédérale de Lausanne (EPFL), 1015 Lausanne, Switzerland.
3
Human Cortical Physiology and Neurorehabilitation Section, National Institute of Neurological Disorders and Stroke, Bethesda, Maryland 20814, USA.
4
School of Psychological Sciences and Sagol School of Neuroscience, Tel Aviv University, Tel Aviv 69978, Israel.
5
Human Cortical Physiology and Neurorehabilitation Section, National Institute of Neurological Disorders and Stroke, Bethesda, Maryland 20814, USA. Electronic address: cohenl@ninds.nih.gov.

Abstract

The brain strengthens memories through consolidation, defined as resistance to interference (stabilization) or performance improvements between the end of a practice session and the beginning of the next (offline gains) [1]. Typically, consolidation has been measured hours or days after the completion of training [2], but the same concept may apply to periods of rest that occur interspersed in a series of practice bouts within the same session. Here, we took an unprecedented close look at the within-seconds time course of early human procedural learning over alternating short periods of practice and rest that constitute a typical online training session. We found that performance did not markedly change over short periods of practice. On the other hand, performance improvements in between practice periods, when subjects were at rest, were significant and accounted for early procedural learning. These offline improvements were more prominent in early training trials when the learning curve was steep and no performance decrements during preceding practice periods were present. At the neural level, simultaneous magnetoencephalographic recordings showed an anatomically defined signature of this phenomenon. Beta-band brain oscillatory activity in a predominantly contralateral frontoparietal network predicted rest-period performance improvements. Consistent with its role in sensorimotor engagement [3], modulation of beta activity may reflect replay of task processes during rest periods. We report a rapid form of offline consolidation that substantially contributes to early skill learning and may extend the concept of consolidation to a time scale in the order of seconds, rather than the hours or days traditionally accepted.

KEYWORDS:

beta activity; consolidation; human motor learning; magnetoencephalography; offline learning; procedural memory; reactivation; replay; skill learning

PMID:
30930043
PMCID:
PMC6482074
[Available on 2020-04-22]
DOI:
10.1016/j.cub.2019.02.049

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