Off-line consolidation of motor sequence learning results in greater integration within a cortico-striatal functional network

NeuroImage

Volumn 99, Issue , 2014, Pages 50-58

  Debas, Karen ^a,c   Carrier, Julie ^a,b,c   Barakat, Marc ^a,c   Marrelec, Guillaume ^a,d   Bellec, Pierre ^a   Tahar, Abdallah Hadj ^a   Karni, Avi ^e   Ungerleider, Leslie G ^f   Benali, Habib ^d   Doyon, Julien ^a,c,d  

^a CENTRE DE RECHERCHE   (Canada)

^b HÔPITAL DU SACRÉ COEUR DE MONTRÉAL   (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

^d UPMC Univ Paris 06   (France)

^e UNIVERSITY OF HAIFA   (Israel)

^f NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

Consolidation; FMRI; Functional connectivity; Motor learning; Networks; Sleep

Indexed keywords

ADULT; ARTICLE; BEHAVIOR CHANGE; BRAIN FUNCTION; BRAIN REGION; CONNECTOME; CONTROLLED STUDY; CORRELATIONAL STUDY; CORTICO STRIATAL NETWORK; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; LEARNING; MALE; MOTOR PERFORMANCE; MOTOR SEQUENCE LEARNING; MOTOR SYSTEM; NEUROIMAGING; NORMAL HUMAN; PRIORITY JOURNAL; SLEEP PATTERN; SLEEP WAKING CYCLE; BRAIN CORTEX; CIRCADIAN RHYTHM; EXECUTIVE FUNCTION; NEOSTRIATUM; NERVE CELL NETWORK; PHYSIOLOGY; SLEEP; YOUNG ADULT;

ADULT; CEREBRAL CORTEX; CIRCADIAN RHYTHM; EXECUTIVE FUNCTION; FEMALE; HUMANS; LEARNING; MALE; MOTOR SKILLS; NEOSTRIATUM; NERVE NET; PRACTICE (PSYCHOLOGY); SLEEP; YOUNG ADULT;

EID: 84903548115     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2014.05.022     Document Type: Article

References (66)

1. Albert N., Robertson E., Miall R. The resting human brain and motor learning. Curr. Biol. 2009, 19:1023-1027.
2. Albouy G., Sterpenich V., Balteau E., Vandewalle G., Desseilles M., Dang-Vu T., Darsaud A., Ruby P., Luppi P.H., Degueldre C., Peigneux P., Luxen A., Maquet P. Both the hippocampus and striatum are involved in consolidation of motor sequence memory. Neuron 2008, 58:261-272.
3. Albouy G., Fogel S., Pottiez H., Nguyen V.A., Ray L., Lungu O., Carrier J., Robertson E., Doyon J. Daytime sleep enhances consolidation of the spatial but not motoric representation of motor sequence memory. PLoS One 2013, 8:e52805.
4. Albouy G., Sterpenich V., Vandewalle G., Darsaud A., Gais S., Rauchs G., Desseilles M., Boly M., Dang-Vu T., Balteau E., Degueldre C., Phillips C., Luxen A., Maquet P. Interaction between hippocampal and striatal systems predicts subsequent consolidation of motor sequence memory. PLoS One 2013, 8:e59490.
5. Albouy G., Vandewalle G., Sterpenich V., Rauchs G., Desseilles M., Balteau E., et al. Sleep stabilizes visuomotor adaptation memory: a functional magnetic resonance imaging study. J. Sleep Res. 2013, 22:144-154.
6. Alexander G.E., Crutcher M.D. Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci. 1990, 13:266-271.
7. Barakat M., Doyon J., Debas K., Vandewalle G., Morin A., Poirier G., Martin N., Lafortune M., Karni A., Ungerleider L.G., Benali H., Carrier J. Fast and slow spindle involvement in the consolidation of a new motor sequence. Behav. Brain Res. 2010, 217(1):117-121.
8. Barakat M., Carrier J., Debas K., Lungu O., Fogel S., Vandewalle G., Hoge R.D., Bellec P., Karni A., Ungerleider L.G., Benali H., Doyon J. Sleep spindles predict neural and behavioral changes in motor sequence consolidation. Hum. Brain Mapp. 2013, 34(11):2918-2928.
9. Beckmann C.F., DeLuca M., Devlin J.T., Smith S.M. Investigations into resting-state connectivity using independent component analysis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2005, 360:1001-1013.
10. Bianciardi M., Fukunaga M., van Gelderen P., Horovitz S.G., de Zwart J.A., Duyn J.H. Modulation of spontaneous fMRI activity in human visual cortex by behavioral state. NeuroImage 2009, 45:160-168.
11. Boly M., Perlbarg V., Marrelec G., Schabus M., Laureys S., Doyon J., Pelegrini-Issac M., Maquet P., Benali H. Hierarchical clustering of brain activity during human nonrapid eye movement sleep. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:5856-5861.
12. Born J., Wilhelm I. System consolidation of memory during sleep. Psychol. Res. 2012, 76:192-203.
13. Buckner R.L., Sepulcre J., Talukdar T., Krienen F.M., Liu H., Hedden T., Andrews-Hanna J.R., Sperling R.A., Johnson K.A. Cortical hubs revealed by intrinsic functional connectivity: mapping, assessment of stability, and relation to Alzheimer's disease. J. Neurosci. Off. J. Soc. Neurosci. 2009, 29:1860-1873.
14. Calhoun V.D., Kiehl K.A., Pearlson G.D. Modulation of temporally coherent brain networks estimated using ICA at rest and during cognitive tasks. Hum. Brain Mapp. 2008, 29:828-838.
15. Cohen D.A., Pascual-Leone A., Press D.Z., Robertson E.M. Off-line learning of motor skill memory: a double dissociation of goal and movement. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:18237-18241.
16. Coynel D., Marrelec G., Perlbarg V., Pelegrini-Issac M., Van de Moortele P.F., Ugurbil K., Doyon J., Benali H., Lehericy S. Dynamics of motor-related functional integration during motor sequence learning. Neuroimage 2010, 49:759-766.
17. Damoiseaux J.S., Rombouts S.A., Barkhof F., Scheltens P., Stam C.J., Smith S.M., Beckmann C.F. Consistent resting-state networks across healthy subjects. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:13848-13853.
18. Dayan E., Cohen L.G. Neuroplasticity subserving motor skill learning. Neuron 2011, 72:443-454.
19. Debas K., Carrier J., Orban P., Barakat M., Lungu O., Vandewalle G., Hadj Tahar A., Bellec P., Karni A., Ungerleider L.G., Benali H., Doyon J. Brain plasticity related to the consolidation of motor sequence learning and motor adaptation. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:17839-17844.
20. Diekelmann S., Born J. The memory function of sleep. Nat. Rev. Neurosci. 2010, 11:114-126.
21. Diekelmann S., Wilhelm I., Born J. The whats and whens of sleep-dependent memory consolidation. Sleep Med. Rev. 2009, 13:309-321.
22. Doyon J., Ungerleider L.G. Functional anatomy of motor skill learning. Neuropsychology of memory 2002, 225-238. The Guilford Press, New York. third ed. L.R. Squire, D.L. Schacter (Eds.).
23. Doyon J., Benali H. Reorganization and plasticity in the adult brain during learning of motor skills. Curr. Opin. Neurobiol. 2005, 15:161-167.
24. Doyon J., Song A.W., Karni A., Lalonde F., Adams M.M., Ungerleider L.G. Experience-dependent changes in cerebellar contributions to motor sequence learning. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:1017-1022.
25. Doyon J., Penhune V., Ungerleider L.G., Doyon J., Penhune V., Ungerleider L.G. Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning. Neuropsychologia 2003, 41:252-262.
26. Doyon J., Bellec P., Amsel R., Penhune V., Monchi O., Carrier J., Lehericy S., Benali H. Contributions of the basal ganglia and functionally related brain structures to motor learning. Behav. Brain Res. 2009, 199:61-75.
27. Doyon J., Korman M., Morin A., Dostie V., Tahar A.H., Benali H., Karni A., Ungerleider L.G., Carrier J. Contribution of night and day sleep vs. simple passage of time to the consolidation of motor sequence and visuomotor adaptation learning. Exp. Brain Res. 2009, 195:15-26.
28. Dudai Y. The neurobiology of consolidations, or, how stable is the engram?. Annu. Rev. Psychol. 2004, 55:51-86.
29. Fischer S., Hallschmid M., Elsner A.L., Born J. Sleep forms memory for finger skills. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:11987-11991.
30. Fischer S., Nitschke M.F., Melchert U.H., Erdmann C., Born J. Motor memory consolidation in sleep shapes more effective neuronal representations. J. Neurosci. 2005, 25(49):11248-11255. (Dec).
31. Floyer-Lea A., Matthews P.M. Distinguishable brain activation networks for short- and long-term motor skill learning. J. Neurophysiol. 2005, 94(1):512-518. (Jul).
32. Fogel S.M., Smith C.T. The function of the sleep spindle: a physiological index of intelligence and a mechanism for sleep-dependent memory consolidation. Neurosci. Biobehav. Rev. 2011, 35:1154-1165.
33. Fogel S., Martin N., Lafortune M., Barakat M., Debas K., Laventure S., Latreille V., Gagnon J.F., Doyon J., Carrier J. NREM sleep oscillations and brain plasticity in aging. Front. Neurol. 2012, 3:176.
34. Fox M.D., Snyder A.Z., Vincent J.L., Raichle M.E. Intrinsic fluctuations within cortical systems account for intertrial variability in human behavior. Neuron 2007, 56:171-184.
35. Friston K.J., Frith C.D., Liddle P.F., Frackowiak R.S. Functional connectivity: the principal-component analysis of large (PET) data sets. J. Cereb. Blood Flow Metab. 1993, 13:5-14.
36. Gheysen F., Van Opstal F., Roggeman C., Van Waelvelde H., Fias W. Hippocampal contribution to early and later stages of implicit motor sequence learning. Exp. Brain Res. 2010, 202:795-807.
37. Grafton S.T., Hazeltine E., Ivry R. Functional mapping of sequence learning in normal humans. J. Cogn. Neurosci. 1995, 7:497-510.
38. Heitger M.H., Ronsse R., Dhollander T., Dupont P., Caeyenberghs K., Swinnen S.P. Motor learning-induced changes in functional brain connectivity as revealed by means of graph-theoretical network analysis. NeuroImage 2012, 61:633-650.
39. Hikosaka O., Nakahara H., Rand M.K., Sakai K., Lu X., Nakamura K., Miyachi S., Doya K. Parallel neural networks for learning sequential procedures. Trends Neurosci. 1999, 22:464-471.
40. Karni A., Meyer G., Jezzard P., Adams M.M., Turner R., Ungerleider L.G. Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 1995, 377:155-158.
41. Kelly R.E., Alexopoulos G.S., Wang Z., Gunning F.M., Murphy C.F., Morimoto S.S., Kanellopoulos D., Jia Z., Lim K.O., Hoptman M.J. Visual inspection of independent components: defining a procedure for artifact removal from fMRI data. J. Neurosci. Methods 2010, 189:233-245.
42. Lansink C.S., Goltstein P.M., Lankelma J.V., McNaughton B.L., Pennartz C.M. Hippocampus leads ventral striatum in replay of place-reward information. PLoS. Biol. 2009, 7:e1000173.
43. Laureys S., Peigneux P., Phillips C., Fuchs S., Degueldre C., Aerts J., Del Fiore G., Petiau C., Luxen A., van der Linden M., Cleeremans A., Smith C., Maquet P. Experience-dependent changes in cerebral functional connectivity during human rapid eye movement sleep. Neuroscience 2001, 105:521-525.
44. Ma L., Wang B., Narayana S., Hazeltine E., Chen X., Robin D.A., Fox P.T., Xiong J. Changes in regional activity are accompanied with changes in inter-regional connectivity during 4weeks motor learning. Brain Res. 2010, 1318:64-76.
45. Maquet P., Laureys S., Peigneux P., Fuchs S., Petiau C., Phillips C., Aerts J., Del Fiore G., Degueldre C., Meulemans T., Luxen A., Franck G., Van Der Linden M., Smith C., Cleeremans A. Experience-dependent changes in cerebral activation during human REM sleep. Nat. Neurosci. 2000, 3:831-836.
46. Marrelec G., Bellec P., Krainik A., Duffau H., Pelegrini-Issac M., Lehericy S., Benali H., Doyon J. Regions, systems, and the brain: hierarchical measures of functional integration in fMRI. Med. Image Anal. 2008, 12:484-496.
47. Peigneux P., Laureys S., Fuchs S., Destrebecqz A., Collette F., Delbeuck X., Phillips C., Aerts J., Del Fiore G., Degueldre C., Luxen A., Cleeremans A., Maquet P. Learned material content and acquisition level modulate cerebral reactivation during posttraining rapid-eye-movements sleep. Neuroimage 2003, 20:125-134.
48. Perlbarg V., Bellec P., Anton J.L., Pelegrini-Issac M., Doyon J., Benali H. CORSICA: correction of structured noise in fMRI by automatic identification of ICA components. Magn. Reson. Imaging. 2007, 25:35-46.
49. Perlbarg V., Marrelec G., Doyon J., Pélégrini-Issac M., Lehericy S., Benali H. NEDICA: detection of group functional networks in fMRI using spatial independent component analysis. 5th IEEE International Symposium on Biomedical Imaging: From Nano to Macro, 2008 2008, 1247-1250. ISBI.
50. Rauchs G., Desgranges B., Foret J., Eustache F. The relationships between memory systems and sleep stages. J. Sleep Res. 2005, 14:123-140.
51. Robertson E.M., Pascual-Leone A., Press D.Z. Awareness modifies the skill-learning benefits of sleep. Curr. Biol. 2004, 14:208-212.
52. Robertson E.M., Press D.Z., Pascual-Leone A. Off-line learning and the primary motor cortex. J. Neurosci. Off. J. Soc. Neurosci. 2005, 25:6372-6378.
53. Robinson S., Basso G., Soldati N., Sailer U., Jovicich J., Bruzzone L., Kryspin-Exner I., Bauer H., Moser E. A resting state network in the motor control circuit of the basal ganglia. BMC Neurosci. 2009, 10:137.
54. Rose M., Haider H., Salari N., Buchel C. Functional dissociation of hippocampal mechanism during implicit learning based on the domain of associations. J. Neurosci. Off. J. Soc. Neurosci. 2011, 31:13739-13745.
55. Schendan H.E., Searl M.M., Melrose R.J., Stern C.E. An fMRI study of the role of the medial temporal lobe in implicit and explicit sequence learning. Neuron 2003, 37:1013-1025.
56. Steele C.J., Penhune V.B. Specific increases within global decreases: a functional magnetic resonance imaging investigation of five days of motor sequence learning. J. Neurosci. 2010, 30:8332-8341.
57. Sun F.T., Miller L.M., Rao A.A., D'Esposito M. Functional connectivity of cortical networks involved in bimanual motor sequence learning. Cereb. Cortex 2007, 17:1227-1234.
58. Tamas Kincses Z., Johansen-Berg H., Tomassini V., Bosnell R., Matthews P.M., Beckmann C.F. Model-free characterization of brain functional networks for motor sequence learning using fMRI. Neuroimage 2008, 39:1950-1958.
59. Tononi G., Sporns O., Edelman G.M. A measure for brain complexity: relating functional segregation and integration in the nervous system. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:5033-5037.
60. Vahdat S., Darainy M., Milner T.E., Ostry D.J. Functionally specific changes in resting-state sensorimotor networks after motor learning. J. Neurosci. 2011, 31:16907-16915.
61. Varela F., Lachaux J.P., Rodriguez E., Martinerie J. The brainweb: phase synchronization and large-scale integration. Nat. Rev. Neurosci. 2001, 2:229-239.
62. Walker M.P., Brakefield T., Morgan A., Hobson J.A., Stickgold R. Practice with sleep makes perfect: sleep-dependent motor skill learning. Neuron 2002, 35:205-211.
63. Walker M.P., Stickgold R., Alsop D., Gaab N., Schlaug G. Sleep-dependent motor memory plasticity in the human brain. Neuroscience 2005, 133:911-917.
64. Wang Z., Liu J., Zhong N., Qin Y., Zhou H., Li K. Changes in the brain intrinsic organization in both on-task state and post-task resting state. NeuroImage 2012, 62:394-407.
65. Wilson M.A., McNaughton B.L. Reactivation of hippocampal ensemble memories during sleep. Science (New York, N.Y.) 1994, 265:676-679.
66. Witt K., Margraf N., Bieber C., Born J., Deuschl G. Sleep consolidates the effector-independent representation of a motor skill. Neuroscience 2010, 171:227-234.