Corticomotor excitability and plasticity following complex visuomotor training in young and old adults

European Journal of Neuroscience

Volumn 34, Issue 11, 2011, Pages 1847-1856

  Cirillo, John ^a   Todd, Gabrielle ^b   Semmler, John G ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

Author keywords

Aging; Motor cortex; Motor skill; Transcranial magnetic stimulation

Indexed keywords

ACTION POTENTIAL; ADULT; ARTICLE; CONTROLLED STUDY; ELECTROMYOGRAPHY; ELECTROSTIMULATION; EVOKED MUSCLE RESPONSE; FEMALE; HUMAN; HUMAN EXPERIMENT; MALE; METACARPOPHALANGEAL JOINT; MOTOR PERFORMANCE; NERVE CELL PLASTICITY; NERVE EXCITABILITY; NORMAL HUMAN; PHYSICAL ACTIVITY; PRIORITY JOURNAL; PROXIMAL INTERPHALANGEAL JOINT; TRAINING; TRANSCRANIAL MAGNETIC STIMULATION; VISUOMOTOR COORDINATION;

ADULT; AGE FACTORS; AGED; ELECTROMYOGRAPHY; EVOKED POTENTIALS, MOTOR; FEMALE; FINGERS; HUMANS; MIDDLE AGED; MOTOR CORTEX; MOTOR SKILLS; MOVEMENT; MUSCLE, SKELETAL; NEURONAL PLASTICITY; TRANSCRANIAL MAGNETIC STIMULATION; YOUNG ADULT;

EID: 82455167882     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2011.07870.x     Document Type: Article

References (73)

1. Bath, K.G. & Lee, F.S. (2006) Variant BDNF (Val66Met) impact on brain structure and function. Cogn Affect Behav Neurosci, 6, 79-85.
2. Brown, R.M., Robertson, E.M. & Press, D.Z. (2009) Sequence skill acquisition and off-line learning in normal aging. PLoS ONE, 4, e6683.
3. Bütefisch, C.M., Davis, B.C., Wise, S.P., Sawaki, L., Kopylev, L., Classen, J. & Cohen, L.G. (2000) Mechanisms of use-dependent plasticity in the human motor cortex. Proc. Natl. Acad. Sci. USA, 97, 3661-3665.
4. Cheeran, B., Talelli, P., Mori, F., Koch, G., Suppa, A., Edwards, M., Houlden, H., Bhatia, K., Greenwood, R. & Rothwell, J.C. (2008) A common polymorphism in the brain derived neurotrophic factor gene (BDNF) modulates human cortical plasticity and the response to rTMS. J. Physiol., 586, 5717-5725.
5. Chen, R., Classen, J., Gerloff, C., Celnik, P., Wassermann, E.M., Hallett, M. & Cohen, L.G. (1997) Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology, 48, 1398-1403.
6. Chen, R., Tam, A., Bütefisch, C., Corwell, B., Ziemann, U., Rothwell, J.C. & Cohen, L.G. (1998) Intracortical inhibition and facilitation in different representations of the human motor cortex. J. Neurophysiol., 80, 2870-2881.
7. Cheney, P.D. & Fetz, E.E. (1980) Functional classes of primate corticomotoneuronal cells and their relation to active force. J. Neurophysiol., 44, 773-791.
8. Cirillo, J., Lavender, A.P., Ridding, M.C. & Semmler, J.G. (2009) Motor cortex plasticity induced by paired associative stimulation is enhanced in physically active individuals. J. Physiol., 587, 5831-5842.
9. Cirillo, J., Rogasch, N.C. & Semmler, J.G. (2010) Hemispheric differences in use-dependent corticomotor plasticity in young and old adults. Exp. Brain Res., 205, 57-68.
10. Classen, J. & Cohen, L. (2003). Practice-induced plasticity in the human motor cortex. In Boniface, S. & Ziemann, U. (Eds), Plasticity in the Human Nervous System: Investigations with Transcranial Magnetic Stimulation. Cambridge University Press, Cambridge, UK, pp. 90-106.
11. Classen, J., Liepert, J., Wise, S.P., Hallett, M. & Cohen, L.G. (1998) Rapid plasticity of human cortical movement representation induced by practice. J. Neurophysiol., 79, 1117-1123.
12. Cotman, C.W. & Berchtold, N.C. (2002) Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci., 25, 295-301.
13. Courchesne, E., Chisum, H.J., Townsend, J., Cowles, A., Covington, J., Egaas, B., Harwood, M., Hinds, S. & Press, G.A. (2000) Normal brain development and aging: quantitative analysis at in vivo MR imaging in healthy volunteers. Radiology, 216, 672-682.
14. Craig, C.L., Marshall, A.L., Sjostrom, M., Bauman, A.E., Booth, M.L., Ainsworth, B.E., Pratt, M., Ekelund, U., Yngve, A., Sallis, J.F. & Oja, P. (2003) International physical activity questionnaire: 12-country reliability and validity. Med. Sci. Sports Exerc., 35, 1381-1395.
15. Doherty, T.J., Vandervoort, A.A. & Brown, W.F. (1993) Effects of ageing on the motor unit: a brief review. Can. J. Appl. Physiol., 18, 331-358.
16. Fathi, D., Ueki, Y., Mima, T., Koganemaru, S., Nagamine, T., Tawfik, A. & Fukuyama, H. (2010) Effects of aging on the human motor cortical plasticity studied by paired associative stimulation. Clin. Neurophysiol., 121, 90-93.
17. Flament, D., Goldsmith, P., Buckley, C.J. & Lemon, R.N. (1993) Task dependence of responses in first dorsal interosseous muscle to magnetic brain stimulation in man. J. Physiol., 464, 361-378.
18. Fogelholm, M., Malmberg, J., Suni, J., Santtila, M., Kyrolainen, H., Mantysaari, M. & Oja, P. (2006) International Physical Activity Questionnaire: validity against fitness. Med. Sci. Sports Exerc., 38, 753-760.
19. Folstein, M.F., Folstein, S.E. & McHugh, P.R. (1975) "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res., 12, 189-198.
20. Freitas, C., Perez, J., Knobel, M., Tormos, J.M., Oberman, L., Eldaief, M., Bashir, S., Vernet, M., Pena-Gomez, C. & Pascual-Leone, A. (2011) Changes in cortical plasticity across the lifespan. Front Aging Neurosci, 3, 1-8.
21. Fritsch, B., Reis, J., Martinowich, K., Schambra, H.M., Ji, Y., Cohen, L.G. & Lu, B. (2010) Direct current stimulation promotes BDNF-dependent synaptic plasticity: potential implications for motor learning. Neuron, 66, 198-204.
22. Gallasch, E., Christova, M., Krenn, M., Kossev, A. & Rafolt, D. (2009) Changes in motor cortex excitability following training of a novel goal-directed motor task. Eur. J. Appl. Physiol., 105, 47-54.
23. Garry, M.I., Kamen, G. & Nordstrom, M.A. (2004) Hemispheric differences in the relationship between corticomotor excitability changes following a fine-motor task and motor learning. J. Neurophysiol., 91, 1570-1578.
24. Grabiner, M.D. & Enoka, R.M. (1995) Changes in movement capabilities with aging. Exerc. Sport Sci. Rev., 23, 65-104.
25. Hinder, M.R., Schmidt, M.W., Garry, M.I., Carroll, T.J. & Summers, J.J. (2011) Absence of cross-limb transfer of performance gains following ballistic motor practice in older adults. J. Appl. Physiol., 110, 166-175.
26. Hoogendam, J.M., Ramakers, G.M. & Di Lazzaro, V. (2010) Physiology of repetitive transcranial magnetic stimulation of the human brain. Brain Stimul, 3, 95-118.
27. Jernigan, T.L., Archibald, S.L., Fennema-Notestine, C., Gamst, A.C., Stout, J.C., Bonner, J. & Hesselink, J.R. (2001) Effects of age on tissues and regions of the cerebrum and cerebellum. Neurobiol. Aging, 22, 581-594.
28. Kleim, J.A., Chan, S., Pringle, E., Schallert, K., Procaccio, V., Jimenez, R. & Cramer, S.C. (2006) BDNF val66met polymorphism is associated with modified experience-dependent plasticity in human motor cortex. Nat. Neurosci., 9, 735-737.
29. Kossev, A.R., Schrader, C., Dauper, J., Dengler, R. & Rollnik, J.D. (2002) Increased intracortical inhibition in middle-aged humans; a study using paired-pulse transcranial magnetic stimulation. Neurosci. Lett., 333, 83-86.
30. Kujirai, T., Caramia, M.D., Rothwell, J.C., Day, B.L., Thompson, P.D., Ferbert, A., Wroe, S., Asselman, P. & Marsden, C.D. (1993) Corticocortical inhibition in human motor cortex. J. Physiol., 471, 501-519.
31. Li Voti, P., Conte, A., Suppa, A., Iezzi, E., Bologna, M., Aniello, M.S., Defazio, G., Rothwell, J.C. & Berardelli, A. (2011) Correlation between cortical plasticity, motor learning and BDNF genotype in healthy subjects. Exp. Brain Res., 212, 91-99.
32. Liepert, J., Classen, J., Cohen, L.G. & Hallett, M. (1998) Task-dependent changes of intracortical inhibition. Exp. Brain Res., 118, 421-426.
33. Light, K.E. & Spirduso, W.W. (1990) Effects of adult aging on the movement complexity factor of response programming. J Gerontol, 45, P107-P109.
34. McGinley, M., Hoffman, R.L., Russ, D.W., Thomas, J.S. & Clark, B.C. (2010) Older adults exhibit more intracortical inhibition and less intracortical facilitation than young adults. Exp. Gerontol., 45, 671-678.
35. McHughen, S.A., Rodriguez, P.F., Kleim, J.A., Kleim, E.D., Marchal Crespo, L., Procaccio, V. & Cramer, S.C. (2010) BDNF val66met polymorphism influences motor system function in the human brain. Cereb. Cortex, 20, 1254-1262.
36. McNevin, N.H., Wulf, G. & Carlson, C. (2000) Effects of attentional focus, self-control, and dyad training on motor learning: implications for physical rehabilitation. Phys. Ther., 80, 373-385.
37. Meintzschel, F. & Ziemann, U. (2006) Modification of practice-dependent plasticity in human motor cortex by neuromodulators. Cereb. Cortex, 16, 1106-1115.
38. Missitzi, J., Gentner, R., Geladas, N., Politis, P., Karandreas, N., Classen, J. & Klissouras, V. (2011) Plasticity in human motor cortex is in part genetically determined. J. Physiol., 589, 297-306.
39. Muellbacher, W., Ziemann, U., Boroojerdi, B., Cohen, L. & Hallett, M. (2001) Role of the human motor cortex in rapid motor learning. Exp. Brain Res., 136, 431-438.
40. Muellbacher, W., Ziemann, U., Wissel, J., Dang, N., Kofler, M., Facchini, S., Boroojerdi, B., Poewe, W. & Hallett, M. (2002) Early consolidation in human primary motor cortex. Nature, 415, 640-644.
41. Muir, R.B. & Lemon, R.N. (1983) Corticospinal neurons with a special role in precision grip. Brain Res., 261, 312-316.
42. Muller-Dahlhaus, J.F., Orekhov, Y., Liu, Y. & Ziemann, U. (2008) Interindividual variability and age-dependency of motor cortical plasticity induced by paired associative stimulation. Exp. Brain Res., 187, 467-475.
43. Ofori, E., Samson, J.M. & Sosnoff, J.J. (2010) Age-related differences in force variability and visual display. Exp. Brain Res., 203, 299-306.
44. Oldfield, R.C. (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia, 9, 97-113.
45. Oliviero, A., Profice, P., Tonali, P.A., Pilato, F., Saturno, E., Dileone, M., Ranieri, F. & Di Lazzaro, V. (2006) Effects of aging on motor cortex excitability. Neurosci. Res., 55, 74-77.
46. Peinemann, A., Lehner, C., Conrad, B. & Siebner, H.R. (2001) Age-related decrease in paired-pulse intracortical inhibition in the human primary motor cortex. Neurosci. Lett., 313, 33-36.
47. Pellicciari, M.C., Miniussi, C., Rossini, P.M. & De Gennaro, L. (2009) Increased cortical plasticity in the elderly: changes in the somatosensory cortex after paired associative stimulation. Neuroscience, 163, 266-276.
48. Perez, M.A., Lungholt, B.K., Nyborg, K. & Nielsen, J.B. (2004) Motor skill training induces changes in the excitability of the leg cortical area in healthy humans. Exp. Brain Res., 159, 197-205.
49. Rao, S.M., Binder, J.R., Bandettini, P.A., Hammeke, T.A., Yetkin, F.Z., Jesmanowicz, A., Lisk, L.M., Morris, G.L., Mueller, W.M., Estkowski, L.D., Wong, E.C., Haughton, V.M. & Hyde, J.S. (1993) Functional magnetic resonance imaging of complex human movements. Neurology, 43, 2311-2318.
50. Ravussin, E. & Bogardus, C. (1989) Relationship of genetics, age, and physical fitness to daily energy expenditure and fuel utilization. Am. J. Clin. Nutr., 49, 968-975.
51. Ridding, M.C. & Ziemann, U. (2010) Determinants of the induction of cortical plasticity by non-invasive brain stimulation in healthy subjects. J. Physiol., 588, 2291-2304.
52. Robertson, E.M., Press, D.Z. & Pascual-Leone, A. (2005) Off-line learning and the primary motor cortex. J. Neurosci., 25, 6372-6378.
53. Rogasch, N.C., Dartnall, T.J., Cirillo, J., Nordstrom, M.A. & Semmler, J.G. (2009) Corticomotor plasticity and learning of a ballistic thumb training task are diminished in older adults. J. Appl. Physiol., 107, 1874-1883.
54. Rosenkranz, K. & Rothwell, J.C. (2006) Differences between the effects of three plasticity inducing protocols on the organization of the human motor cortex. Eur. J. Neurosci., 23, 822-829.
55. Rosenkranz, K., Williamon, A. & Rothwell, J.C. (2007) Motorcortical excitability and synaptic plasticity is enhanced in professional musicians. J. Neurosci., 27, 5200-5206.
56. Roshan, L., Paradiso, G.O. & Chen, R. (2003) Two phases of short-interval intracortical inhibition. Exp. Brain Res., 151, 330-337.
57. Rossi, S., Hallett, M., Rossini, P.M. & Pascual-Leone, A. (2009) Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin. Neurophysiol., 120, 2008-2039.
58. Rothwell, J.C., Hallett, M., Berardelli, A., Eisen, A., Rossini, P. & Paulus, W. (1999) Magnetic stimulation: motor evoked potentials. The International Federation of Clinical Neurophysiology. Electroencephalogr. Clin. Neurophysiol. Suppl., 52, 97-103.
59. Sale, M.V. & Semmler, J.G. (2005) Age-related differences in corticospinal control during functional isometric contractions in left and right hands. J. Appl. Physiol., 99, 1483-1493.
60. Sawaki, L., Boroojerdi, B., Kaelin-Lang, A., Burstein, A.H., Bütefisch, C.M., Kopylev, L., Davis, B. & Cohen, L.G. (2002) Cholinergic influences on use-dependent plasticity. J. Neurophysiol., 87, 166-171.
61. Sawaki, L., Yaseen, Z., Kopylev, L. & Cohen, L.G. (2003) Age-dependent changes in the ability to encode a novel elementary motor memory. Ann. Neurol., 53, 521-524.
62. Smith, C.D., Umberger, G.H., Manning, E.L., Slevin, J.T., Wekstein, D.R., Schmitt, F.A., Markesbery, W.R., Zhang, Z., Gerhardt, G.A., Kryscio, R.J. & Gash, D.M. (1999) Critical decline in fine motor hand movements in human aging. Neurology, 53, 1458-1461.
63. Stinear, C.M. & Byblow, W.D. (2003) Role of intracortical inhibition in selective hand muscle activation. J. Neurophysiol., 89, 2014-2020.
64. Tecchio, F., Zappasodi, F., Pasqualetti, P., De Gennaro, L., Pellicciari, M.C., Ercolani, M., Squitti, R. & Rossini, P.M. (2008) Age dependence of primary motor cortex plasticity induced by paired associative stimulation. Clin. Neurophysiol., 119, 675-682.
65. Todd, G., Rogasch, N.C., Flavel, S.C. & Ridding, M.C. (2009) Voluntary movement and repetitive transcranial magnetic stimulation over human motor cortex. J. Appl. Physiol., 106, 1593-1603.
66. Todd, G., Kimber, T.E., Ridding, M.C. & Semmler, J.G. (2010) Reduced motor cortex plasticity following inhibitory rTMS in older adults. Clin. Neurophysiol., 121, 441-447.
67. Tormos, J.M., Canete, C., Tarazona, F., Catala, M.D., Pascual-Leone Pascual, A. & Pascual-Leone, A. (1997) Lateralized effects of self-induced sadness and happiness on corticospinal excitability. Neurology, 49, 487-491.
68. Voelcker-Rehage, C. (2008) Motor-skill learning in older adults-a review of studies on age-related differences. Eur. Rev. Aging. Phys. Act., 5, 5-16.
69. Walker, M.P., Brakefield, T., Morgan, A., Hobson, J.A. & Stickgold, R. (2002) Practice with sleep makes perfect: sleep-dependent motor skill learning. Neuron, 35, 205-211.
70. Wassermann, E.M. (2002) Variation in the response to transcranial magnetic brain stimulation in the general population. Clin. Neurophysiol., 113, 1165-1171.
71. Wexler, B.E., Fulbright, R.K., Lacadie, C.M., Skudlarski, P., Kelz, M.B., Constable, R.T. & Gore, J.C. (1997) An fMRI study of the human cortical motor system response to increasing functional demands. Magn. Reson. Imaging, 15, 385-396.
72. Ziemann, U., Muellbacher, W., Hallett, M. & Cohen, L.G. (2001) Modulation of practice-dependent plasticity in human motor cortex. Brain, 124, 1171-1181.
73. Zoghi, M., Pearce, S.L. & Nordstrom, M.A. (2003) Differential modulation of intracortical inhibition in human motor during selective activation of an intrinsic hand muscle. J. Physiol., 550, 933-946.