Delineating the cortico-striatal-cerebellar network in implicit motor sequence learning

NeuroImage

Volumn 94, Issue , 2014, Pages 222-230

  Tzvi, Elinor ^a   Münte, Thomas F ^a   Krämer, Ulrike M ^a  

^a UNIVERSITY OF LÜBECK   (Germany)

Author keywords

Cerebellum; Dynamic causal modeling; Effective connectivity; FMRI; Motor sequence learning

Indexed keywords

ADULT; ARTICLE; BRAIN CORTEX; CAUSAL MODELING; CEREBELLUM; CEREBELLUM DISEASE; CONTROLLED STUDY; CORPUS STRIATUM; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; LEARNING; MALE; MATHEMATICAL MODEL; MOTOR PERFORMANCE; MOTOR SEQUENCE LEARNING; NERVE CELL NETWORK; NORMAL HUMAN; PRIORITY JOURNAL; RESPONSE TIME; BIOLOGICAL MODEL; COMPUTER SIMULATION; CONNECTOME; MOTOR CORTEX; MOVEMENT (PHYSIOLOGY); NERVE TRACT; PHYSIOLOGY; PROCEDURES; YOUNG ADULT;

ADULT; CEREBELLUM; COMPUTER SIMULATION; CONNECTOME; CORPUS STRIATUM; FEMALE; HUMANS; LEARNING; MALE; MODELS, NEUROLOGICAL; MOTOR CORTEX; MOTOR SKILLS; MOVEMENT; NERVE NET; NEURAL PATHWAYS; YOUNG ADULT;

EID: 84898609449     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2014.03.004     Document Type: Article

References (66)

1. Albus J.S. A theory of cerebellar function. Math. Biosci. 1971, 10:25-61.
2. Bernard J.A., Seidler R.D. Cerebellar contributions to visuomotor adaptation and motor sequence learning: an ALE meta-analysis. Front. Hum. Neurosci. 2013, 7:27.
3. Bo J., Peltier S.J., Noll D.C., Seidler R.D. Symbolic representations in motor sequence learning. Neuroimage 2011, 54:417-426.
4. Buckner R.L., Krienen F.M., Castellanos A., Diaz J.C., Yeo B.T. The organization of the human cerebellum estimated by intrinsic functional connectivity. J. Neurophysiol. 2011, 106:2322-2345.
5. Carbon M., Argyelan M., Ghilardi M.F., Mattis P., Dhawan V., Bressman S., Eidelberg D. Impaired sequence learning in dystonia mutation carriers: a genotypic effect. Brain 2011, 134:1416-1427.
6. Dayan E., Cohen L.G. Neuroplasticity subserving motor skill learning. Neuron 2011, 72:443-454.
7. Destrebecqz A., Cleeremans A. Can sequence learning be implicit? New evidence with the process dissociation procedure. Psychon. Bull. Rev. 2001, 8:343-350.
8. Destrebecqz A., Peigneux P., Laureys S., Degueldre C., Del Fiore G., Aerts J., Luxen A., Van Der Linden M., Cleeremans A., Maquet P. The neural correlates of implicit and explicit sequence learning: interacting networks revealed by the process dissociation procedure. Learn. Mem. 2005, 12:480-490.
9. Dirnberger G., Novak J., Nasel C. Perceptual sequence learning is more severely impaired than motor sequence learning in patients with chronic cerebellar stroke. J. Cogn. Neurosci. 2013, 25:2207-2215.
10. Doyon J., Gaudreau D., Laforce R., Castonguay M., Bedard P.J., Bedard F., Bouchard J.P. Role of the striatum, cerebellum, and frontal lobes in the learning of a visuomotor sequence. Brain Cogn. 1997, 34:218-245.
11. 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.
12. 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.
13. 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.
14. Friston K.J., Harrison L., Penny W. Dynamic causal modelling. Neuroimage 2003, 19:1273-1302.
15. Friston K., Mattout J., Trujillo-Barreto N., Ashburner J., Penny W. Variational free energy and the Laplace approximation. Neuroimage 2007, 34:220-234.
16. Galea J.M., Vazquez A., Pasricha N., de Xivry J.J., Celnik P. Dissociating the roles of the cerebellum and motor cortex during adaptive learning: the motor cortex retains what the cerebellum learns. Cereb. Cortex 2011, 21:1761-1770.
17. Gomez-Beldarrain M., Garcia-Monco J.C., Rubio B., Pascual-Leone A. Effect of focal cerebellar lesions on procedural learning in the serial reaction time task. Exp. Brain Res. 1998, 120:25-30.
18. Grafton S.T., Hazeltine E., Ivry R.B. Motor sequence learning with the nondominant left hand. A PET functional imaging study. Exp. Brain Res. 2002, 146:369-378.
19. Grefkes C., Eickhoff S.B., Nowak D.A., Dafotakis M., Fink G.R. Dynamic intra- and interhemispheric interactions during unilateral and bilateral hand movements assessed with fMRI and DCM. Neuroimage 2008, 41:1382-1394.
20. Grefkes C., Nowak D.A., Eickhoff S.B., Dafotakis M., Kust J., Karbe H., Fink G.R. Cortical connectivity after subcortical stroke assessed with functional magnetic resonance imaging. Ann. Neurol. 2008, 63:236-246.
21. Hardwick R.M., Rottschy C., Miall R.C., Eickhoff S.B. A quantitative meta-analysis and review of motor learning in the human brain. Neuroimage 2013, 67:283-297.
22. Hikosaka O., Nakamura K., Sakai K., Nakahara H. Central mechanisms of motor skill learning. Curr. Opin. Neurobiol. 2002, 12:217-222.
23. Ito M. Cerebellar control of the vestibulo-ocular reflex-around the flocculus hypothesis. Annu. Rev. Neurosci. 1982, 5:275-296.
24. Jackson G.M., Jackson S.R., Harrison J., Henderson L., Kennard C. Serial reaction time learning and Parkinson's disease: evidence for a procedural learning deficit. Neuropsychologia 1995, 33:577-593.
25. Jenkins I.H., Brooks D.J., Nixon P.D., Frackowiak R.S., Passingham R.E. Motor sequence learning: a study with positron emission tomography. J. Neurosci. 1994, 14:3775-3790.
26. Jin X., Costa R.M. Start/stop signals emerge in nigrostriatal circuits during sequence learning. Nature 2010, 466:457-462.
27. Jin X., Tecuapetla F., Costa R.M. Basal ganglia subcircuits distinctively encode the parsing and concatenation of action sequences. Nat. Neurosci. 2014, 17:423-430.
28. Jueptner M., Frith C.D., Brooks D.J., Frackowiak R.S., Passingham R.E. Anatomy of motor learning. II. Subcortical structures and learning by trial and error. J. Neurophysiol. 1997, 77:1325-1337.
29. Karabanov A., Cervenka S., de Manzano O., Forssberg H., Farde L., Ullen F. Dopamine D2 receptor density in the limbic striatum is related to implicit but not explicit movement sequence learning. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:7574-7579.
30. 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.
31. Karni A., Meyer G., Rey-Hipolito C., Jezzard P., Adams M.M., Turner R., Ungerleider L.G. The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:861-868.
32. Kass R.E., Raftery A.E. Bayes factors. J. Am. Stat. Assoc. 1995, 90:773-795.
33. Laforce R., Doyon J. Distinct contribution of the striatum and cerebellum to motor learning. Brain Cogn. 2001, 45:189-211.
34. Lehericy S., Benali H., Van de Moortele P.F., Pelegrini-Issac M., Waechter T., Ugurbil K., Doyon J. Distinct basal ganglia territories are engaged in early and advanced motor sequence learning. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:12566-12571.
35. Ma L.S., Wang B.Q., Narayana S., Hazeltine E., Chen X.Y., Robin D.A., Fox P.T., Xiong J.H. Changes in regional activity are accompanied with changes in inter-regional connectivity during 4weeks motor learning. Brain Res. 2010, 1318:64-76.
36. Marr D. A theory of cerebellar cortex. J. Physiol. 1969, 202:437-470.
37. Matsuzaka Y., Picard N., Strick P.L. Skill representation in the primary motor cortex after long-term practice. J. Neurophysiol. 2007, 97:1819-1832.
38. Molinari M., Leggio M.G., Solida A., Ciorra R., Misciagna S., Silveri M.C., Petrosini L. Cerebellum and procedural learning: evidence from focal cerebellar lesions. Brain 1997, 120(Pt 10):1753-1762.
39. Muellbacher W., Ziemann U., Wissel J., Dang N., Kofler M., Facchini S., Boroojerdi B., Poewe W., Hallett M. Early consolidation in human primary motor cortex. Nature 2002, 415:640-644.
40. Nissen M.J., Bullemer P. Attentional requirements of learning - evidence from performance-measures. Cogn. Psychol. 1987, 19:1-32.
41. Nitsche M.A., Schauenburg A., Lang N., Liebetanz D., Exner C., Paulus W., Tergau F. Facilitation of implicit motor learning by weak transcranial direct current stimulation of the primary motor cortex in the human. J. Cogn. Neurosci. 2003, 15:619-626.
42. Ohyama T., Nores W.L., Murphy M., Mauk M.D. What the cerebellum computes. Trends Neurosci. 2003, 26:222-227.
43. Pascual-Leone A., Grafman J., Clark K., Stewart M., Massaquoi S., Lou J.S., Hallett M. Procedural learning in Parkinson's disease and cerebellar degeneration. Ann. Neurol. 1993, 34:594-602.
44. Penhune V.B., Steele C.J. Parallel contributions of cerebellar, striatal and M1 mechanisms to motor sequence learning. Behav. Brain Res. 2012, 226:579-591.
45. Penny W.D., Stephan K.E., Daunizeau J., Rosa M.J., Friston K.J., Schofield T.M., Leff A.P. Comparing families of dynamic causal models. PLoS Computational Biology 2010, 6:e1000709.
46. Pool E.M., Rehme A.K., Fink G.R., Eickhoff S.B., Grefkes C. Network dynamics engaged in the modulation of motor behavior in healthy subjects. Neuroimage 2013, 82:68-76.
47. Reis J., Schambra H.M., Cohen L.G., Buch E.R., Fritsch B., Zarahn E., Celnik P.A., Krakauer J.W. Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:1590-1595.
48. Robertson E.M. The serial reaction time task: implicit motor skill learning?. J. Neurosci. 2007, 27:10073-10075.
49. Rose M., Haider H., Salari N., Buchel C. Functional dissociation of hippocampal mechanism during implicit learning based on the domain of associations. J. Neurosci. 2011, 31:13739-13745.
50. Schambra H.M., Abe M., Luckenbaugh D.A., Reis J., Krakauer J.W., Cohen L.G. Probing for hemispheric specialization for motor skill learning: a transcranial direct current stimulation study. J. Neurophysiol. 2011, 106:652-661.
51. Schmahmann J.D., Pandya D.N. The cerebrocerebellar system. Int. Rev. Neurobiol. 1997, 41:31-60.
52. Schulz R., Wessel M.J., Zimerman M., Timmerman J., Gerloff C., Hummel F.C. White matter integrity of specific dentato-thalamo-cortical pathways is associated with learning gains in precise movement timing. Cereb. Cortex 2014, 10.1093/cercor/bht356.
53. Seidler R.D., Purushotham A., Kim S.G., Ugurbil K., Willingham D., Ashe J. Cerebellum activation associated with performance change but not motor learning. Science 2002, 296:2043-2046.
54. Seidler R.D., Purushotham A., Kim S.G., Ugurbil K., Willingham D., Ashe J. Neural correlates of encoding and expression in implicit sequence learning. Exp. Brain Res. 2005, 165:114-124.
55. Seitz R.J., Roland E., Bohm C., Greitz T., Stone-Elander S. Motor learning in man: a positron emission tomographic study. Neuroreport 1990, 1:57-60.
56. Shin J.C., Ivry R.B. Spatial and temporal sequence learning in patients with Parkinson's disease or cerebellar lesions. J. Cogn. Neurosci. 2003, 15:1232-1243.
57. Spencer R.M., Ivry R.B. Sequence learning is preserved in individuals with cerebellar degeneration when the movements are directly cued. J. Cogn. Neurosci. 2009, 21:1302-1310.
58. 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.
59. Stephan K.E., Penny W.D., Daunizeau J., Moran R.J., Friston K.J. Bayesian model selection for group studies. Neuroimage 2009, 46:1004-1017.
60. Stephan K.E., Penny W.D., Moran R.J., den Ouden H.E., Daunizeau J., Friston K.J. Ten simple rules for dynamic causal modeling. Neuroimage 2010, 49:3099-3109.
61. 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.
62. Toni I., Krams M., Turner R., Passingham R.E. The time course of changes during motor sequence learning: a whole-brain fMRI study. Neuroimage 1998, 8:50-61.
63. Torriero S., Oliveri M., Koch G., Caltagirone C., Petrosini L. Interference of left and right cerebellar rTMS with procedural learning. J. Cogn. Neurosci. 2004, 16:1605-1611.
64. Wilkinson L., Teo J.T., Obeso I., Rothwell J.C., Jahanshahi M. The contribution of primary motor cortex is essential for probabilistic implicit sequence learning: evidence from theta burst magnetic stimulation. J. Cogn. Neurosci. 2010, 22:427-436.
65. Willingham D.B. A neuropsychological theory of motor skill learning. Psychol. Rev. 1998, 105:558-584.
66. Wolpert D.M., Miall R.C., Kawato M. Internal models in the cerebellum. Trends Cogn. Sci. 1998, 2:338-347.