Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-25T04:04:28.039Z Has data issue: false hasContentIssue false
  • English
  • Français

The Time Course of Changes in Motor Cortex Excitability Associated with Voluntary Movement

Published online by Cambridge University Press:  02 December 2014

Robert Chen  and
Mark Hallett
Robert Chen
Affiliation:
Division of Neurology, University Health Network and University of Toronto, Toronto
Mark Hallett
Affiliation:
The Human Motor Control Section, National Institutes of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

The excitability of the motor cortex is modulated before and after voluntary movements. Transcranial magnetic stimulation studies showed increased corticospinal excitability from about 80 and 100 ms before EMG onset for simple reaction time and self-paced movements, respectively. Following voluntary movements, there are two phases of increased corticospinal excitability from 0 to approximately 100 ms and from approximately 100 to 160 ms after EMG offset. The first phase may correspond to the frontal peak of motor potential in movement-related cortical potentials studies and the movement-evoked magnetic field I (MEFI) in magnetoencephalographic (MEG) studies, and likely represents a time when decreasing output from the motor cortex falls below that required for activation of spinal motoneurons, but is still above resting levels. The second phase of increased corticospinal excitability may be due to peripheral proprioceptive inputs or may be centrally programmed representing a subthreshold, second agonist burst. This may correspond to the MEFII in MEG studies. Corticospinal excitability was reduced below baseline levels from about 500 to 1,000 ms after EMG offset, similar to the timing of increase in the power (event-related synchronization, ERS) of motor cortical rhythm. Similarly, motor cortex excitability is reduced at the time of ERS of motor cortical rhythm following median nerve stimulation. These findings support the hypothesis that ERS represents an inactive, idling state of the cortex. The time course of cortical activation is abnormal in movement disorders such as Parkinson’s disease and dystonia, reflecting abnormalities in both movement preparation and in cortical excitability following movement.

Résumé

RÉSUMÉ

L’excitabilité du cor- tex moteur est modulée avant et après les mouvements volontaires. Des études de stimulation magnétique transcrânienne ont montré une augmentation de l’excitabilité corticospinale précédant de 80 et 100 ms le début de la réponse ÉMG pour le temps de réaction simple et l’activité motrice autocom- mandée respectivement. Après un mouvement volontaire, il y a deux phases d’excitabilité corticospinale accrue de 0 à approximativement 100 ms et d’approximativement 100 à 160 ms après la fin de la réponse ÉMG. La première phase peut correspondre au pic frontal du potentiel moteur dans les études de potentiels corticaux reliés aux mouvements et le champ magnétique I évoqué par le mouvement (MEFI) dans les études magnétoencéphalo- graphiques (MEG), et représente vraisemblablement un moment où l’influx nerveux du cortex moteur tombe sous le niveau requis pour l’activation des motoneurones spinaux, mais demeure au-dessus du niveau observé au repos. La deuxième phase d’augmentation de l’excitabilité corticospinale peut être due à des influx proprioceptifs périphériques ou peut être programmée centralement, représentant une poussée agoniste secondaire sous le seuil. Ceci peut correspondre au MEFII dans les études MEG. L’excitabilité corticospinale était diminuée sous le niveau de base d’environ 500 à 1,000 ms après la fin de la réponse ÉMG, comme au moment de l’augmentation de la puissance (synchronisation reliée à l’événement, SRE) du rythme cortical moteur. Pareillement, l’excitabilité du cortex moteur est diminuée au moment des SRE du rythme cortical moteur après une stimulation du nerf médi- an. Ces observations supportent l’hypothèse que la SRE représente le cortex à l’état inactif. Le processus de l’activation corticale est anormal dans les désordres du mouvement tels la maladie de Parkinson et la dystonie, ce qui témoigne d’anomalies dans la préparation du mouvement et dans l’ex- citabilité corticale après le mouvement.

Type
Review Article
Information
Canadian Journal of Neurological Sciences , Volume 26 , Issue 3 , November 1999 , pp. 163 - 169
Copyright
Copyright © The Canadian Journal of Neurological 1999

References

1. Jackson, JH. On the comparative study of diseases of the nervous system. Brit Med J 1889; 355–362.Google Scholar
2. Leyton, ASF, Sherrington, CS. Observations on the excitable cortex of the chimpanzee, orangutan, and gorilla. Q J Exp Physiol 1917; 11: 135–222.CrossRefGoogle Scholar
3. Penfield, W, Jasper, H. Epilepsy and the Functional Anatomy of the Human Brain. Boston: Little, Brown, 1954.Google Scholar
4. Evarts, EV. Pyramidal tract activity associated with a conditional hand movement in the monkey. J Neurophysiol 1966; 29: 1011–1027.Google Scholar
5. Luschei, ES, Johnson, RA, Glickstein, M. Response of neurones in the motor cortex during performance of a simple repetitive arm movement. Nature 1968; 217: 190–191.Google Scholar
6. Godschalk, M, Lemon, RN, Nijs, HGT, Kuypers, HGJM. Behaviour of neurones in monkeys periarcuate and precentrai cortex before and during visually guided arm and hand movements. Exp Brain Res 1981; 44: 113–116.Google Scholar
7. Fetz, EE, Finocchio, DV. Operant conditioning of specific patterns of neural and muscular activity. Science 1971; 174: 431–435.CrossRefGoogle ScholarPubMed
8. Riehle, A, Requin, J. Monkey primary motor and premotor cortex:single-cell activity related to prior information about direction and extent of an intended movement. J Neurophysiol 1989; 61: 534–549.Google Scholar
9. Thach, WT. Timing of activity in cerebellar dentate nucleus and cerebral motor cortex during prompt volitional movement. Brain Res 1975; 88: 233–241.Google Scholar
10. Starr, A, Caramia, M, Zarola, F, Rossini, PM. Enhancement of motor cortical excitability in humans by non-invasive electrical stimulation appears prior to voluntary movement. Electroencephalogr Clin Neurophysiol 1988; 70: 26–32.Google Scholar
11. Rossini, PM, Zarola, F, Stalberg, E, Caramia, M. Pre-movement facilitation of motor-evoked potentials in man during transcranial stimulation of the central motor pathways. Brain Res 1988; 458: 20–30.CrossRefGoogle ScholarPubMed
12. Pascual-Leone, A, Valls-Solé, J, Wassermann, EM, et al. Effects of focal transcranial magnetic stimulation on simple reaction time to acoustic, visual and somatosensory stimuli. Brain 1992; 115: 1045–1059.Google Scholar
13. Tomberg, C, Caramia, MD. Prime mover muscle in finger lift or finger flexion reaction times: identification with transcranial magnetic stimulation. Electroencephalogr Clin Neurophysiol 1991; 81: 319–322.CrossRefGoogle ScholarPubMed
14. Hoshiyama, M, Kitamura, Y, Koyama, S, et al. Reciprocal change of motor evoked potentials preceding voluntary movements in humans. Muscle Nerve 1996; 19: 125–131.3.0.CO;2-G>CrossRefGoogle ScholarPubMed
15. Chen, R, Yaseen, Z, Cohen, LG, Hallett, M. The time course of corti-cospinal excitability in reaction time and self-paced movements. Ann Neurol 1998; 44: 317–325.Google Scholar
16. Gottlieb, GL, Agarwal, GC, Stark, L. Interactions between voluntary and postural mechanisms of the human motor system. J Physiol (Lond) 1970; 33: 365–381.Google Scholar
17. Pierrot-Deseilligny, E, Lacert, P, Cathala, HP. Amplitude et variabilité des réflexes monosynaptiques avant un mouvement volontaire. Physiol Behav 1971; 7: 495–508.Google Scholar
18. Eichenberger, A, Rüegg, DG. Relation between the specific H reflex activation preceding a voluntary movement and movement parameters in man. J Physiol (Lond) 1984; 347: 545–559.CrossRefGoogle ScholarPubMed
19. Deecke, L, Scheid, P, Kornhuber, HH. Distribution of readiness potential, pre-motion positivity, and motor potential of the human cerebral cortex preceding voluntary finger movements. Exp Brain Res 1969; 7: 158–168.Google Scholar
20. Toro, C, Deuschl, G, Thatcher, R, et al. Event-related desynchronization and movement-related cortical potentials on the ECoG and EEG. Electroencephalogr Clin Neurophysiol 1994; 93: 380–389.Google Scholar
21. Pfurtscheller, G, Aranibar, A. Event-related desynchronization detected by power measurements of scalp EEG. Electroencephalogr Clin Neurophysiol 1989; 72: 250–258.Google Scholar
22. Neshige, R, Lüders, H, Shibasaki, H. Recording of movement-related potentials from scalp and cortex in man. Brain 1988; 111: 719–736.Google Scholar
23. Shibasaki, H, Barrett, G, Halliday, E, Halliday, AM. Components of the movement-related cortical potential and their scalp topography. Electroencephalogr Clin Neurophysiol 1980; 49: 213–226.Google Scholar
24. Tarkka, IM, Hallett, M. Topography of scalp-recorded motor potentials in human finger movements. J Clin Neurophysiol 1991; 8: 331–341.Google Scholar
25. Rektor, I, Fève, A, Buser, P, Bathien, N, Lamarche, M. Intracerebral recording of movement related readiness potentials: an exploration in epileptic patients. Electroencephalogr Clin Neurophysiol 1994; 90: 273–283.Google Scholar
26. Neshige, R, Lüders, H, Friedman, L, Shibasaki, H. Recording of movement-related potentials from the human cortex. Ann Neurol 1988; 24: 439–445.Google Scholar
27. Ikeda, A, Lüders, HO, Burgress, RC, Shibasaki, H. Movement-related potentials recorded from supplementary motor area and primary motor area. Role of supplementary motor area in voluntary movements. Brain 1992; 115: 1017–1043.CrossRefGoogle ScholarPubMed
28. Nagamine, T, Toro, C, Balish, M, Deuschl, G, Wang, B. Cortical magnetic and electric fields associated with voluntary finger movements. Brain Topography 1994; 6: 175–183.Google Scholar
29. Nagamine, T, Kajola, M, Salmelin, R, Shibasaki, H, Hari, R. Movement-related slow cortical magnetic fields and changes of spontaneous MEG- and EEG-brain rhythms. Electroencephalogr Clin Neurophysiol 1996; 99: 274–286.Google Scholar
30. Llinàs, RR. The intrinsic electrophysiological properties of mam- malian neurons: insights into central nervous system function. Science 1988; 242: 1654–1664.Google Scholar
31. Jasper, H, Penfield, W. Electrocorticograms in man: effect of volun- tary movement upon the electrical activity of the precentrai gyrus. Arch Psychiatrie Zeitschr Neurol 1949; 183: 163–174.Google Scholar
32. Gastaut, H, Terzian, H, Gastaut, Y. Etude d’une activité électroencéphalographique méconnue: “Le rhythme rolandique en arceau”. Marseille Med 1952; 89: 296–310.Google Scholar
33. Salmelin, R, Hari, R. Spatiotemporal characteristics of sensorimotor neuromagnetic rhythms related to thumb movement. Neuroscience 1994; 60: 537–550.Google Scholar
34. Salmelin, R, Hämäläinen, M, Kajola, M, Hari, R. Functional segregation of movement-related rhythmic activity in the human brain. Neuroimage 1995; 2: 237–243.Google Scholar
35. Salenius, S, Portin, K, Kajola, M, Salmelin, R, Hari, R. Cortical control of human motoneuron firing during isometric contraction. J Neurophysiol 1997; 77: 3401–3405.Google Scholar
36. Pfurtscheller, G, Stancák, A Jr., Neuper, C. Post-movement beta syn- chronization. A correlate of an idling motor area? Electroencephalogr Clin Neurophysiol 1996; 98: 281–293.Google Scholar
37. Chatrian, GE, Petersen, MC, Lazarte, JA. The blocking of the rolandic wicket rhythm and some central changes related to movement. Electroencephalogr Clin Neurophysiol 1959; 11: 497–510.CrossRefGoogle ScholarPubMed
38. Leocani, L, Toro, C, Manganotti, P, Zhuang, P, Hallett, M. Event-related coherence and event-related desynchronization/synchronization in the 10 Hz and 20 Hz EEG during self-paced movements. Electroencephalogr Clin Neurophysiol 1997; 104: 199–206.Google Scholar
39. Amassian, VE, Quirk, GJ, Stewart, M. A comparison of corticospinal activation by magnetic coil and electrical stimulation of monkey motor cortex. Electroencephalogr Clin Neurophysiol 1990; 77: 390–401.Google Scholar
40. Rothwell, JC, Thompson, PD, Day, BL, Boyd, S, Marsden, CD. Stimulation of the human motor cortex through the scalp. Exp Physiol 1991; 76: 159–200.Google Scholar
41. Nakamura, H, Kitagawa, H, Kawaguchi, Y, Tsuji, H. Direct and indirect activation of human corticospinal neurons by transcranial magnetic and electrical stimulation. Neurosci Lett 1996; 210: 45–48.Google Scholar
42. Picard, N, Smith, GA. Primary motor cortical activity related to the weight and texture of grasped objects in the monkey. J Neurophysiol 1992; 68: 1867–1881.Google Scholar
43. Fetz, EE, Baker, MA. Operantly conditioned patterns of precentrai unit activity and correlated responses in adjacent cells and contralateral muscles. J Neurophysiol 1973; 36: 179–204.CrossRefGoogle ScholarPubMed
44. Hallett, M, Shahani, BT, Young, RR. EMG analysis of stereotyped voluntary movements in man. J Neurol Neurosurg Psychiatry 1975; 38: 1154–1162.Google Scholar
45. Hallett, M, Marsden, CD. Ballistic flexion movements of the human thumb. J Physiol (Lond) 1979; 294: 33–50.Google Scholar
46. Brown, SHC, Cooke, JD. Amplitude- and instruction-dependent modulation of movement-related electromyogram activity in humans. J Physiol (Lond) 1981; 316: 97–107.Google Scholar
47. Marsden, CD, Obeso, JA, Rothwell, JC. The function of the antagonist muscle during fast limb movements in man. J Physiol (Lond) 1983; 335: 1–13.CrossRefGoogle ScholarPubMed
48. Menick, HM, Benecke, R, Meyer, W, Hohne, J, Conrad, B. Human ballistic finger flexion: uncoupling of the three-burst pattern. Exp Brain Res 1984; 55: 127–133.Google Scholar
49. Lestienne, F. Effects of inertial load and velocity on the braking process of voluntary limb movements. Exp Brain Res 1979; 35: 407–418.CrossRefGoogle ScholarPubMed
50. Sanes, JN, Jennings, VA. Centrally programmed patterns of muscle activity in voluntary motor behavior of humans. Exp Brain Res 1984; 54: 23–32.CrossRefGoogle ScholarPubMed
51. Terada, K, Ikeda, A, Nagamine, T, Shibasaki, H. Movement-related cortical potentials associated with voluntary muscle relaxation. Electroencephalogr Clin Neurophysiol 1995; 95: 335–345.CrossRefGoogle ScholarPubMed
52. Rothwell, JC, Higuchi, K, Obeso, JA. The offset cortical potential: an electrical correlate of movement inhibition in man. Mov Disord 1998; 13: 330–335.CrossRefGoogle ScholarPubMed
53. Pfurtscheller, G. Event-related synchronization (ERS): an electro- physiological correlate of cortical areas at rest. Electroencephalogr Clin Neurophysiol 1992; 83: 62–69.Google Scholar
54. Stancák, A Jr., Pfurtscheller, G. Desynchronization and recovery of β rhythms during brisk and slow self-paced finger movements in man. Neurosci Lett 1995; 196: 21–24.Google Scholar
55. Hari, R, Salmelin, R. Human cortical oscillations: a neuromagnetic view through the skull. Trends Neurosci 1997; 20: 44–49.Google Scholar
56. Evarts, EV. Motor cortex reflexes associated with learned movement. Science 1973; 179: 501–503.Google Scholar
57. Wiesendanger, M. Input from muscle and cutaneous nerves of the hand and forearm to neurons of the precentrai gyrus of baboons and monkeys. J Physiol (Lond) 1973; 228: 203–219.Google Scholar
58. Porter, R, Rack, PM. Timing of responses in the motor cortex monkeys to an unexpected disturbance of finger position. Brain Res 1976; 103: 201–213.Google Scholar
59. Salenius, S, Schnitzler, A, Salmelin, R, Jousmäki, V, Hari, R. Modulation of human cortical rolandic rhythms during natural sensorimotor tasks. Neuroimage 1997; 5: 221–228.Google Scholar
60. Schnitzler, A, Salenius, S, Salmelin, R, Jousmäki, V, Hari, R. Involvement of primary motor cortex in motor imagery: a neuromagnetic study. Neuroimage 1997; 6: 201–208.CrossRefGoogle ScholarPubMed
61. Chen, R, Corwell, B, Cohen, LG, Hallett, M. Reduction of motor cortex excitability after median nerve stimulation. Muscle Nerve 1998; 21: 1585. (Abstract).Google Scholar
62. Pascual-Leone, A, Valls-Solé, J, Brasil-Neto, JP, Cohen, LG, Hallett, M. Akinesia in Parkinson’s disease. I. Shortening of simple reaction time with focal, single-pulse transcranial magnetic stimulation. Neurology 1994; 44: 884–891.CrossRefGoogle ScholarPubMed
63. Jahanshahi, M, Jenkins, IH, Brown, RG, et al. Self-initiated versus externally triggered movements. I. An investigation using measurement of regional cerebral blood flow with PET and movement-related potentials in normal and Parkinson’s disease subjects. Brain 1995; 118: 913–933.Google Scholar
64. Marsden, CD. Slowness of movement in Parkinson’s disease. Mov Disord 1989; 4 (Suppl. 1): S26–S37.Google Scholar
65. Dietz, MA, Goetz, CG, Stebbins, GT. Evaluation of a modified inverted walking stick as a treatment for parkinsonian freezing episodes. Mov Disord 1990; 5: 243–247.CrossRefGoogle ScholarPubMed
66. Benecke, R, Rothwell, JC, Dick, JP, Day, BR, Marsden, CD. Performance of simultaneous movements in patients with Parkinson’s disease. Brain 1986; 109: 739–757.Google Scholar
67. Benecke, R, Rothwell, JC, Dick, JP, Day, BR, Marsden, CD. Disturbance of sequential movements in patients with Parkinson’s disease. Brain 1987; 110: 361–379.CrossRefGoogle ScholarPubMed
68. Dick, JPR, Rothwell, JC, Day, BL, et al. The Bereitshaftspotential is abnormal in Parkinson’s disease. Brain 1989; 112: 233–244.Google Scholar
69. Samuel, M, Ceballos-Baumann, AO, Blin, J, et al. Evidence for lateral premotor and parietal overactivity in Parkinson’s disease during sequential and bimanual movements. A PET study. Brain 1997; 120: 963–976.CrossRefGoogle ScholarPubMed
70. Cunnington, R, Iansek, R, Johnson, KA, Bradshaw, JL. Movement-related potentials in Parkinson’s disease. Motor imagery and movement preparation. Brain 1997; 120: 1339–1353.CrossRefGoogle ScholarPubMed
71. Defebvre, L, Bourriez, JL, Dujardin, K, et al. Spatiotemporal study of Bereitschaftspotential and event-related desynchronization during voluntary movement in Parkinson’s disease. Brain Topography 1994; 6: 237–244.Google Scholar
72. Ikeda, A, Kaji, R, Terada, K, et al. Dissociation between contingent negative variation (CNV) and Bereitschaftspotential (BP) in patients with parkinsonism. Electroencephalogr Clin Neurophysiol 1997; 102: 142–151.Google Scholar
73. Cunnington, R, Iansek, R, Bradshaw, JL, Phillips, JG. Movement-related potentials in Parkinson’s disease. Presence and predictability of temporal and spatial cues. Brain 1995; 118: 935–950.Google Scholar
74. Brown, P, Marsden, CD. EEG desynchronization during movement and bradykinesia in Parkinson’s disease. Mov Disord 1998; 13 (Suppl. 2): 57 (Abstract).Google Scholar
75. Wang, HC, Lees, AJ, Brown, P. EEG desynchronization prior to movement and bradykinesia in Parkinson’s disease. Mov Disord 1998; 13 (Suppl. 2): 35 (Abstract).Google Scholar
76. Brown, P, Marsden, CD. What do the basal ganglia do? Lancet 1998; 351: 1801–1804.Google Scholar
77. Pfurtscheller, G, Pichler-Zalaudek, K, Ortmayr, B, Diez, J, Reisecker, F. Postmovement beta synchronization in patients with Parkinson’s disease. J Clin Neurophysiol 1998; 15: 243–250.Google Scholar
78. Deuschl, G, Toro, C, Matsumoto, J, Hallett, M. Movement-related cortical potentials in writer’s cramp. Ann Neurol 1995; 38: 862–868.Google Scholar
79. Van Der Kamp, W, Rothwell, JC, Thompson, PD, Day, BL, Marsden, CD. The movement-related cortical potential is abnormal in patients with idiopathic torsion dystonia. Mov Disord 1995; 10: 630–633.Google Scholar
80. Toro, C, Deuschl, G, Hallett, M. Movement-related EEG desynchronization in patients with hand cramps: evidence for cortical involvement in hand cramps. Neurology 1998; 43: A379 (Abstract).Google Scholar