Practice makes imperfect: restorative effects of sleep on motor learning.
Emerging evidence suggests that sleep plays a key role in procedural learning, particularly in the continued development of motor skill learning following initial acquisition. We argue that a detailed examination of the time course of performance across sleep on the finger-tapping task, established as the paradigm for studying the effect of sleep on motor learning, will help distinguish a restorative role of sleep in motor skill learning from a proactive one. Healthy subjects rehearsed for 12 trials and, following a night of sleep, were tested. Early training rapidly improved speed as well as accuracy on pre-sleep training. Additional rehearsal caused a marked slow-down in further improvement or partial reversal in performance to observed levels below theoretical upper limits derived on the basis of early pre-sleep rehearsal. This decrement in learning efficacy does not occur always, but if and only if it does, overnight sleep has an effect in fully or partly restoring the efficacy and actual performance to the optimal theoretically achieveable level. Our findings re-interpret the sleep-dependent memory enhancement in motor learning reported in the literature as a restoration of fatigued circuitry specialized for the skill. In providing restitution to the fatigued brain, sleep eliminates the rehearsal-induced synaptic fatigue of the circuitry specialized for the task and restores the benefit of early pre-sleep rehearsal. The present findings lend support to the notion that latent sleep-dependent enhancement of performance is a behavioral expression of the brain's restitution in sleep.
Sheth
Bhavin R
BR
University of Houston, Houston, Texas, United States of America. brsheth@uh.edu
Janvelyan
Davit
D
Khan
Murtuza
M
D000293:Adolescent; D000328:Adult; D001921:Brain / Q000502:physiology; D005260:Female; D006801:Humans; D007858:Learning; D008297:Male; D008568:Memory; D009048:Motor Skills; D018794:Problem-Based Learning; D011597:Psychomotor Performance; D015203:Reproducibility of Results; D012890:Sleep; D013997:Time Factors; D014851:Wakefulness
Proc Natl Acad Sci U S A. 2002 Sep 3;99(18):11987-91
12193650
Nat Neurosci. 2002 Jul;5(7):677-81
12032542
J Mot Behav. 1996 Mar;28(1):71-79
12529225
Neuron. 2002 Jul 3;35(1):205-11
12123620
Psychol Res. 2004 Apr;68(2-3):126-37
14648225
Science. 1994 Jul 29;265(5172):679-82
8036518
J Exp Psychol Hum Percept Perform. 1983 Feb;9(1):86-102
6220126
Exp Brain Res. 2003 Sep;152(2):229-42
12879170
Psychophysiology. 1973 Jul;10(4):431-6
4719486
Nature. 1993 Sep 16;365(6443):250-2
8371779
Vision Res. 2006 Nov;46(23):4071-4
16979688
Learn Mem. 2003 Jul-Aug;10(4):275-84
12888546
Nature. 2003 Oct 9;425(6958):616-20
14534587
Proc Natl Acad Sci U S A. 1998 Feb 3;95(3):861-8
9448252
Learn Mem. 2004 Nov-Dec;11(6):705-13
15576888
Behav Brain Sci. 2005 Feb;28(1):51-64; discussion 64-104
16047457
J Cogn Neurosci. 2000 Mar;12(2):246-54
10771409
Nat Neurosci. 2000 Dec;3(12):1335-9
11100156
Neurobiol Learn Mem. 1998 Jul-Sep;70(1-2):119-36
9753592
Nat Neurosci. 2000 Dec;3(12):1237-8
11100141
Nature. 1996 Jul 18;382(6588):252-5
8717039
Annu Rev Psychol. 2006;57:139-66
16318592