A Rapid Form of Offline Consolidation in Skill Learning.
beta activity
consolidation
human motor learning
magnetoencephalography
offline learning
procedural memory
reactivation
replay
skill learning
Journal
Current biology : CB
ISSN: 1879-0445
Titre abrégé: Curr Biol
Pays: England
ID NLM: 9107782
Informations de publication
Date de publication:
22 04 2019
22 04 2019
Historique:
received:
05
01
2019
revised:
01
02
2019
accepted:
21
02
2019
pubmed:
2
4
2019
medline:
19
5
2020
entrez:
2
4
2019
Statut:
ppublish
Résumé
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.
Identifiants
pubmed: 30930043
pii: S0960-9822(19)30219-2
doi: 10.1016/j.cub.2019.02.049
pmc: PMC6482074
mid: NIHMS1524423
pii:
doi:
Types de publication
Journal Article
Research Support, N.I.H., Intramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1346-1351.e4Subventions
Organisme : Intramural NIH HHS
ID : Z99 NS999999
Pays : United States
Commentaires et corrections
Type : CommentIn
Informations de copyright
Published by Elsevier Ltd.
Références
J Exp Psychol Learn Mem Cogn. 2008 Jul;34(4):834-42
pubmed: 18605872
Trends Neurosci. 2011 Oct;34(10):504-14
pubmed: 21742389
Neural Comput. 1995 Nov;7(6):1129-59
pubmed: 7584893
Neuroscience. 2008 Jan 24;151(2):386-95
pubmed: 18063484
Neurosci Biobehav Rev. 2015 Mar;50:128-42
pubmed: 25446944
Curr Opin Neurobiol. 2016 Oct;40:72-80
pubmed: 27400290
Science. 2007 Nov 16;318(5853):1147-50
pubmed: 18006749
Proc Natl Acad Sci U S A. 2016 May 10;113(19):5206-11
pubmed: 27114514
Clin Neurophysiol. 1999 Nov;110(11):1842-57
pubmed: 10576479
Neuroimage. 2010 Jan 1;49(1):694-702
pubmed: 19732838
Science. 2014 Jun 6;344(6188):1173-8
pubmed: 24904169
Trends Cogn Sci. 2017 Aug;21(8):589-599
pubmed: 28578977
Phys Med Biol. 2003 Nov 21;48(22):3637-52
pubmed: 14680264
Br J Psychol. 1965 Aug;56:163-82
pubmed: 14340115
PLoS Biol. 2015 Sep 18;13(9):e1002263
pubmed: 26382320
Curr Biol. 2018 Aug 20;28(16):2515-2526.e4
pubmed: 30100342
Proc Natl Acad Sci U S A. 2016 Nov 15;113(46):13251-13256
pubmed: 27803331
Nat Rev Neurosci. 2012 Sep;13(9):658-64
pubmed: 22903222
Br J Psychol. 1965 Aug;56:157-62
pubmed: 14340114
Cold Spring Harb Perspect Biol. 2015 Aug 03;7(8):a021766
pubmed: 26238360
Neuron. 2011 Nov 3;72(3):443-54
pubmed: 22078504
Curr Opin Neurobiol. 2011 Apr;21(2):269-74
pubmed: 21353526
Cortex. 2014 Sep;58:281-8
pubmed: 23849672
Neuroimage. 2012 Jan 2;59(1):399-403
pubmed: 21784161
Proc Natl Acad Sci U S A. 2013 Nov 26;110(48):19591-6
pubmed: 24218550
Trends Neurosci. 2006 Jan;29(1):58-64
pubmed: 16290273
Nature. 2003 Oct 9;425(6958):616-20
pubmed: 14534587
Comput Intell Neurosci. 2011;2011:156869
pubmed: 21253357
Neuroimage. 2002 Jan;15(1):273-89
pubmed: 11771995
Neuron. 2010 Jan 28;65(2):280-90
pubmed: 20152133
Learn Mem. 2006 Sep-Oct;13(5):580-3
pubmed: 16980543
Nature. 2006 Mar 30;440(7084):680-3
pubmed: 16474382
Nat Neurosci. 2015 Aug;18(8):1109-15
pubmed: 26098758
Hippocampus. 2013 Nov;23(11):985-1004
pubmed: 23929594
Elife. 2017 Nov 06;6:
pubmed: 29106374
Curr Biol. 2010 Sep 14;20(17):1545-9
pubmed: 20817532
Exp Brain Res. 2009 May;195(1):15-26
pubmed: 19277618
Nat Neurosci. 2000 Aug;3(8):831-6
pubmed: 10903578
Psychol Bull. 2015 Jul;141(4):812-34
pubmed: 25822130
Neuron. 2002 Jul 3;35(1):205-11
pubmed: 12123620
Life Sci (1962). 1964 Mar;3:175-88
pubmed: 14151219
Neuron. 2014 Jan 8;81(1):69-76
pubmed: 24411732
Exp Neurol. 2013 Jul;245:15-26
pubmed: 23022918
Elife. 2017 Sep 11;6:
pubmed: 28892464
Neuropharmacology. 2015 Jan;88:155-63
pubmed: 25195191
PLoS One. 2013;8(1):e52805
pubmed: 23300993
Nat Rev Neurosci. 2004 Jul;5(7):576-82
pubmed: 15208699
J Neurosci. 2008 Nov 19;28(47):12284-93
pubmed: 19020022
Philos Trans A Math Phys Eng Sci. 2011 Oct 13;369(1952):3768-84
pubmed: 21893527
Curr Opin Neurobiol. 2010 Apr;20(2):156-65
pubmed: 20359884
Nat Neurosci. 2017 Feb 23;20(3):327-339
pubmed: 28230841