Neural substrates of practice structure that support future off-line learning.
Off-line learning is facilitated when motor skills are acquired under a random practice schedule and retention suffers when a similar set of motor skills are practiced under a blocked schedule. The current study identified the neural correlates of a random training schedule while participants learned a set of four-element finger sequences using their nondominant hand during functional magnetic resonance imaging. A go/no go task was used to separately probe brain areas supporting sequence preparation and production. By the end of training, the random practice schedule, relative to the block schedule, recruited a broad premotor-parietal network as well as sensorimotor and subcortical regions during both preparation and production trials, despite equivalent motor performance. Longitudinal analysis demonstrated that preparation-related activity under a random schedule remained stable or increased over time. The blocked schedule showed the opposite pattern. Across individual subjects, successful skill retention was correlated with greater activity at the end of training in the ipsilateral left motor cortex, for both preparation and production. This is consistent with recent evidence that attributes off-line learning to training-related processing within primary motor cortex. These results reflect the importance of an overlooked aspect of motor skill learning. Specifically, how trials are organized during training-with a random schedule-provides an effective basis for the formation of enduring motor memories, through enhanced engagement of core regions involved in the active preparation and implementation of motor programs.
Wymbs
Nicholas F
NF
1Department of Psychological and Brain Sciences, Dartmouth College, Hanover, New Hampshire, USA.
Grafton
Scott T
ST
D001921:Brain / Q000502:physiology*; D001931:Brain Mapping; D005260:Female; D006801:Humans; D007858:Learning / Q000502:physiology*; D008279:Magnetic Resonance Imaging; D008297:Male; D008568:Memory / Q000502:physiology; D009048:Motor Skills / Q000502:physiology*; D009483:Neuropsychological Tests; D011214:Practice, Psychological; D011930:Reaction Time; D013997:Time Factors; D055815:Young Adult
J Neurosci. 2006 Jan 4;26(1):117-25
16399678
J Neurophysiol. 2000 Oct;84(4):2148-60
11024102
Neuroimage. 2002 Apr;15(4):870-8
11906227
J Cogn Neurosci. 2006 Dec;18(12):2167-76
17129198
Sleep. 2008 Aug;31(8):1149-56
18714787
J Neurosci. 2005 Oct 12;25(41):9398-405
16221848
Neuroreport. 2001 Dec 21;12(18):A111-24
11742260
Neuroimage. 1999 Sep;10(3 Pt 1):233-60
10458940
Annu Rev Neurosci. 2000;23:393-415
10845069
Neuroimage. 2001 Nov;14(5):1048-57
11697936
Curr Opin Neurobiol. 2006 Apr;16(2):213-21
16563734
J Neurosci. 2002 Oct 15;22(20):9024-34
12388609
Neuron. 2005 Mar 24;45(6):967-73
15797556
Cereb Cortex. 2006 Dec;16(12):1729-38
16400162
Curr Opin Neurobiol. 2005 Apr;15(2):161-7
15831397
J Neurosci. 2006 Nov 15;26(46):11888-92
17108162
Proc Natl Acad Sci U S A. 2005 Aug 30;102(35):12566-71
16107540
Learn Mem. 2003 Jul-Aug;10(4):275-84
12888546
Science. 2007 Jan 19;315(5810):393-5
17234951
Curr Opin Neurobiol. 2001 Dec;11(6):663-72
11741015
Annu Rev Neurosci. 2001;24:631-51
11520914
J Exp Psychol Hum Percept Perform. 2001 Apr;27(2):423-37
11318057
Exp Brain Res. 2002 Oct;146(3):369-78
12232693
Trends Neurosci. 2006 Jan;29(1):58-64
16290273
Nature. 2003 Oct 9;425(6958):616-20
14534587
Science. 1999 Mar 12;283(5408):1752-7
10073944
J Neurophysiol. 2004 Jul;92(1):653-9
14985413
J Neurosci. 2006 Nov 29;26(48):12466-70
17135408
Behav Brain Res. 2000 Nov;115(2):205-18
11000421
Neuropsychopharmacology. 2009 Jun;34(7):1843-53
19194375
J Neurosci. 1998 Nov 15;18(22):9420-8
9801380
J Neurosci. 2006 Mar 8;26(10):2704-13
16525049
Neuroimage. 2004 Apr;21(4):1732-47
15050594
Nat Neurosci. 2007 Sep;10(9):1206-13
17694051
Trends Cogn Sci. 2007 Oct;11(10):442-50
17905642
Science. 2000 Jan 14;287(5451):248-51
10634773
Science. 1997 Aug 8;277(5327):821-5
9242612
PLoS Biol. 2006 Oct;4(10):e316
16968135
J Neurophysiol. 2004 Apr;91(4):1748-62
14645381
Proc Natl Acad Sci U S A. 2002 Jan 22;99(2):1017-22
11805340
PLoS One. 2007 Apr 04;2(4):e341
17406665
Exp Brain Res. 2009 Jun;196(2):303-9
19462166
Curr Biol. 2004 Feb 3;14(3):208-12
14761652
Cereb Cortex. 1996 May-Jun;6(3):342-53
8670662
Science. 1982 Jul 30;217(4558):408-14
7046051
Nature. 2007 May 3;447(7140):83-6
17476267
J Cogn Neurosci. 2006 May;18(5):793-802
16768378
Neuroimage. 2004;23 Suppl 1:S208-19
15501092
Neurosci Lett. 2003 Feb 6;337(2):69-72
12527390
J Neurosci. 2007 Sep 19;27(38):10259-69
17881532
Neuroimage. 2002 Oct;17(2):825-41
12377157
Neuroimage. 2005 Nov 15;28(3):669-81
16054844
Neuroscientist. 2006 Jun;12(3):261-71
16684970
J Cogn Neurosci. 2004 Jan-Feb;16(1):127-38
15006042
J Neurophysiol. 1997 Mar;77(3):1325-37
9084600
Neuroimage. 2003 Oct;20(2):1052-63
14568475
J Neurosci. 2002 Feb 15;22(4):1397-406
11850466
Nat Rev Neurosci. 2007 Sep;8(9):700-11
17704812
J Cogn Neurosci. 2007 Nov;19(11):1854-71
17958488
Neuroimage. 2005 May 1;25(4):1325-35
15850749
Nature. 2002 Feb 7;415(6872):640-4
11807497
J Neurophysiol. 2007 Feb;97(2):1819-32
17182912
J Neurosci. 2005 Jul 6;25(27):6372-8
16000627
Cereb Cortex. 1999 Jan-Feb;9(1):35-49
10022494
Percept Mot Skills. 2004 Aug;99(1):116-26
15446636