Training-related decrease in antagonist muscles activation is associated with increased motor cortex activation: Evidence of central mechanisms for control of antagonist muscles

Experimental Brain Research

Volumn 220, Issue 3-4, 2012, Pages 287-295

  Dal Maso, Fabien ^a   Longcamp, Marieke ^a,b   Amarantini, David ^a,c  

^a UNIVERSITÉ PAUL SABATIER   (France)

^b CNRS   (France)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Agonist and antagonist muscles activation; Central adaptations; Isometric contractions; Motor cortex oscillations; Strength training

Indexed keywords

ADULT; ARTICLE; BICEPS BRACHII MUSCLE; CONTROLLED STUDY; ELECTRODE; ELECTROENCEPHALOGRAPHY; ELECTROMYOGRAPHY; ENDURANCE; FORCE; GASTROCNEMIUS MUSCLE; HUMAN; IMPEDANCE; ISOMETRICS; KNEE; MALE; MOTOR CORTEX; MUSCLE CONTRACTION; MUSCLE STRENGTH; MUSCLE TRAINING; OSCILLATION; PRIORITY JOURNAL; RECTUS FEMORIS MUSCLE; TORQUE; VASTUS MEDIALIS MUSCLE;

ADAPTATION, PHYSIOLOGICAL; ADULT; ELECTROENCEPHALOGRAPHY; ELECTROMYOGRAPHY; HUMANS; ISOMETRIC CONTRACTION; KNEE JOINT; MALE; MOTOR CORTEX; MOVEMENT; MUSCLE, SKELETAL; RESISTANCE TRAINING;

EID: 84864285981     PISSN: 00144819     EISSN: 14321106     Source Type: Journal    
DOI: 10.1007/s00221-012-3137-1     Document Type: Article

References (66)

1. Amarantini D, Rao G, Berton E (2010) A two-step EMG-andoptimization process to estimate muscle force during dynamic movement. J Biomech 43:1827-1830
2. Andrykiewicz A, Patino L, Naranjo JR, Witte M, Hepp-Reymond MC, Kristeva R (2007) Corticomuscular synchronization with small and large dynamic force output. BMC Neurosci 8:101
3. Baratta R, Solomonow M, Zhou BH, Letson D, Chuinard R, D'Ambrosia R (1988) Muscular coactivation. The role of the antagonist musculature in maintaining knee stability. Am J Sports Med 16:113-122
4. Basmajian JV (1977) Motor learning and control: a working hypothesis. Phys Med Rehabil 58:38-41
5. Basmajian JV, De Luca CJ (eds) (1985) Muscles alive, their functions revealed by electromyography. Williams & Wilkins, Baltimore
6. Bigot J, Longcamp M, Dal Maso F, Amarantini D (2011) A new statistical test based on the wavelet cross-spectrum to detect time-frequency dependence between non-stationary signals: application to the analysis of cortico-muscular interactions. Neuroimage 55:1504-1518
7. Brown P, Salenius S, Rothwell JC, Hari R (1998) Cortical correlate of the Piper rhythm in humans. J Neurophysiol 80:2911-2917 (Pubitemid 29029223)
8. Bru B, Amarantini D (2008) Influence of sporting expertise on the EMG-torque relationship during isometric contraction in man. Comput Methods Biomech Biomed Eng 11:43-44
9. Buzsaki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304:1926-1929
10. Carolan B, Cafarelli E (1992) Adaptations in coactivation after isometric resistance training. J Appl Physiol 73:911-917
11. Centomo H, Amarantini D, Martin L, Prince F (2008) Differences in the coordination of agonist and antagonist muscle groups in below-knee amputee and able-bodied children during dynamic exercise. J Electromyogr Kinesiol 18:487-494 (Pubitemid 351615054)
12. Chapman JP, Chapman LJ, Allen JJ (1987) The measurement of foot preference. Neuropsychologia 25:579-584 (Pubitemid 17113245)
13. Corser T (1973) Cocontraction and reciprocal relaxation in the ankle plantar flexors and dorsiflexors during rapid stepping and jumping. Electromyogr Clin Neurophysiol 13:289-306
14. Crone NE, Miglioretti DL, Gordon B, Sieracki JM, Wilson MT, Uematsu S, Lesser RP (1998) Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. I. Alpha and beta event-related desynchronization. Brain 121(Pt 12):2271-2299 (Pubitemid 28552466)
15. Dai TH, Liu JZ, Sahgal V, Brown RW, Yue GH (2001) Relationship between muscle output and functional MRI-measured brain activation. Exp Brain Res 140:290-300 (Pubitemid 32835333)
16. De Luca CJ, Mambrito B (1987) Voluntary control of motor units in human antagonist muscles: coactivation and reciprocal activation. J Neurophysiol 58:525-542 (Pubitemid 17142663)
17. Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics. J Neurosci Methods 134:9-21
18. Delorme A, Sejnowski T, Makeig S (2007) Enhanced detection of artifacts in EEG data using higher-order statistics and independent component analysis. Neuroimage 34:1443-1449 (Pubitemid 46187079)
19. Dettmers C, Fink GR, Lemon RN, Stephan KM, Passingham RE, Silbersweig D, Holmes A, Ridding MC, Brooks DJ, Frackowiak RS (1995) Relation between cerebral activity and force in the motor areas of the human brain. J Neurophysiol 74:802-815
20. Duchateau J, Enoka RM (2002) Neural adaptations with chronic activity patterns in able-bodied humans. Am J Phys Med Rehabil 81:S17-S27 (Pubitemid 35192963)
21. Falvo MJ, Sirevaag EJ, Rohrbaugh JW, Earhart GM (2010) Resistance training induces supraspinal adaptations: evidence frommovementrelated cortical potentials. Eur J Appl Physiol 109:923-933
22. Folland JP, Williams AG (2007) The adaptations to strength training: morphological and neurological contributions to increased strength. Sports Med 37:145-168 (Pubitemid 46155818)
23. Gribble PL, Mullin LI, Cothros N, Mattar A (2003) Role of cocontraction in arm movement accuracy. J Neurophysiol 89:2396-2405 (Pubitemid 36570204)
24. Griffin L, Cafarelli E (2005) Resistance training: cortical, spinal, and motor unit adaptations. Can J Appl Physiol 30:328-340 (Pubitemid 40880712)
25. Griffin L, Cafarelli E (2007) Transcranial magnetic stimulation during resistance training of the tibialis anterior muscle. J Electromyogr Kinesiol 17:446-452 (Pubitemid 46856879)
26. Hakkinen K, Kallinen M, Izquierdo M, Jokelainen K, Lassila H, Malkia E, Kraemer WJ, Newton RU, Alen M (1998) Changes in agonist-antagonist EMG, muscle CSA, and force during strength training in middle-aged and older people. J Appl Physiol 84:1341-1349 (Pubitemid 28158701)
27. Hakkinen K, Alen M, Kallinen M, Newton RU, Kraemer WJ (2000) Neuromuscular adaptation during prolonged strength training, detraining and re-strength-training in middle-aged and elderly people. Eur J Appl Physiol 83:51-62 (Pubitemid 32015607)
28. Halliday DM, Conway BA, Farmer SF, Rosenberg JR (1998) Using electroencephalography to study functional coupling between cortical activity and electromyograms during voluntary contractions in humans. Neurosci Lett 241:5-8 (Pubitemid 28079020)
29. Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G (2000) Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol 10:361-374
30. Karni A, Meyer G, Jezzard P, Adams MM, Turner R, Ungerleider LG (1995) Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 377:155-158
31. Kilavik BE, Ponce-Alvarez A, Trachel R, Confais J, Takerkart S, Riehle A (2011) Context-related frequency modulations of macaque motor cortical LFP beta oscillations. Cereb Cortex 13:203-209
32. Kilner JM, Baker SN, Salenius S, Hari R, Lemon RN (2000) Human cortical muscle coherence is directly related to specific motor parameters. J Neurosci 20:8838-8845
33. Kristeva R, Patino L, Omlor W (2007) Beta-range cortical motor spectral power and corticomuscular coherence as a mechanism for effective corticospinal interaction during steady-state motor output. Neuroimage 36:785-792 (Pubitemid 46907622)
34. Lattier G, Millet GY, Maffiuletti NA, Babault N, Lepers R (2003) Neuromuscular differences between endurance-trained, powertrained, and sedentary subjects. J Strength Cond Res 17:514-521 (Pubitemid 37152353)
35. Levenez M, Garland SJ, Klass M, Duchateau J (2008) Cortical and spinal modulation of antagonist coactivation during a submaximal fatiguing contraction in humans. J Neurophysiol 99:554-563 (Pubitemid 351253217)
36. Lotze M, Scheler G, Tan HRM, Braun C, Birbaumer N (2003) The musician's brain: functional imaging of amateurs and professionals during performance and imagery. Neuroimage 20:1817-1829 (Pubitemid 37468287)
37. Magill RA (2011) Motor learning: concepts and applications, 9th edn. McGraw Hill, New York, pp 28-32
38. Manal K, Buchanan TS (2000) Limitations of inverse dynamics in identifying quadriceps avoidance. Proc Am Soc Biomech 24:143
39. Masakado Y, Nielsen JB (2008) Task-and phase-related changes in cortico-muscular coherence. Keio J Med 57:50-56 (Pubitemid 351744046)
40. Miller JP, Croce RV, Hutchins R (2000) Reciprocal coactivation patterns of the medial and lateral quadriceps and hamstrings during slow, medium and high speed isokinetic movements. J Electromyogr Kinesiol 10:233-239
41. Mima T, Simpkins N, Oluwatimilehin T, Hallett M (1999) Force level modulates human cortical oscillatory activities. Neurosci Lett 275:77-80 (Pubitemid 29502540)
42. Mullany H, O'Malley M, St Clair Gibson A, Vaughan C (2002) Agonist-antagonist common drive during fatiguing knee extension efforts using surface electromyography. J Electromyogr Kinesiol 12:375-384 (Pubitemid 35291939)
43. Muthukumaraswamy SD (2011) Temporal dynamics of primary motor cortex gamma oscillation amplitude and piper corticomuscular coherence changes during motor control. Exp Brain Res 212:623-633
44. Neuper C, Pfurtscheller G (2001) Event-related dynamics of cortical rhythms: frequency-specific features and functional correlates. Int J Psychophysiol 43:41-58 (Pubitemid 33115236)
45. Olney SJ, Winter DA (1985) Predictions of knee and ankle moments of force in walking from EMG and kinematic data. J Biomech 18:9-20 (Pubitemid 15137544)
46. Omlor W, Patino L, Hepp-Reymond MC, Kristeva R (2007) Gammarange corticomuscular coherence during dynamic force output. Neuroimage 34:1191-1198 (epub 2006 Dec 1119) (Pubitemid 46394474)
47. Patino L, Chakarov V, Schulte-Monting J, Hepp-Reymond MC, Kristeva R (2006) Oscillatory cortical activity during a motor task in a deafferented patient. Neurosci Lett 401:214-218 (Pubitemid 43729530)
48. Perez MA, Lundbye-Jensen J, Nielsen JB (2007) Task-specific depression of the soleus H-reflex after cocontraction training of antagonistic ankle muscles. J Neurophysiol 98:3677-3687
49. Pfurtscheller G, Lopes da Silva FH (1999) Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin Neurophysiol 110:1842-1857 (Pubitemid 29454610)
50. Pfurtscheller G, Neuper C (1992) Simultaneous EEG 10 Hz desynchronization and 40 Hz synchronization during finger movements. NeuroReport 3:1057-1060 (Pubitemid 23034700)
51. Pfurtscheller G, Graimann B, Huggins JE, Levine SP, Schuh LA (2003) Spatiotemporal patterns of beta desynchronization and gamma synchronization in corticographic data during self-paced movement. Clin Neurophysiol 114:1226-1236 (Pubitemid 36776820)
52. Rao G, Amarantini D, Berton E (2009) Influence of additional load on the moments of the agonist and antagonist muscle groups at the knee joint during closed chain exercise. J Electromyogr Kinesiol 19:459-466
53. Remaud A, Guevel A, Cornu C (2007) Antagonist muscle coactivation and muscle inhibition: effects on external torque regulation and resistance training-induced adaptations. Neurophysiol Clin 37:1-14 (Pubitemid 46533929)
54. Salmelin R, Hamalainen M, Kajola M, Hari R (1995) Functional segregation of movement-related rhythmic activity in the human brain. Neuroimage 2:237-243 (Pubitemid 26018338)
55. Sanes JN, Donoghue JP (2000) Plasticity and primary motor cortex. Annu Rev Neurosci 23:393-415 (Pubitemid 30350048)
56. Semmler JG, Sale MV, Meyer FG, Nordstrom MA (2004) Motor-unit coherence and its relation with synchrony are influenced by training. J Neurophysiol 92:3320-3331 (Pubitemid 39506310)
57. Shiavi R, Frigo C, Pedotti A (1998) Electromyographic signals during gait: criteria for envelope filtering and number of strides. Med Biol Eng Comput 36:171-178
58. Stepien M, Conradi J, Waterstraat G, Hohlefeld FU, Curio G, Nikulin VV (2011) Event-related desynchronization of sensorimotor EEG rhythms in hemiparetic patients with acute stroke. Neurosci Lett 488:17-21
59. Stokes IA, Gardner-Morse M (2003) Spinal stiffness increases with axial load: another stabilizing consequence of muscle action. J Electromyogr Kinesiol 13:397-402 (Pubitemid 36798112)
60. Tallon-Baudry C, Bertrand O, Delpuech C, Pernier J (1996) Stimulus specificity of phase-locked and non-phase-locked 40 Hz visual responses in human. J Neurosci 16:4240-4249 (Pubitemid 26192419)
61. Tanaka R (1974) Reciprocal Ia inhibition during voluntary movements in man. Exp Brain Res 21:529-540
62. Thickbroom GW, Phillips BA, Morris I, Byrnes ML, Mastaglia FL (1998) Isometric force-related activity in sensorimotor cortex measured with functional MRI. Exp Brain Res 121:59-64 (Pubitemid 28284664)
63. Tyc F, Boyadjian A, Devanne H (2005) Motor cortex plasticity induced by extensive training revealed by transcranial magnetic stimulation in human. Eur J Neurosci 21:259-266 (Pubitemid 40193894)
64. Ushiyama J, Takahashi Y, Ushiba J (2010) Muscle dependency of corticomuscular coherence in upper and lower limb muscles and training-related alterations in ballet dancers and weightlifters. J Appl Physiol 109:1086-1095
65. van Duinen H, Renken R, Maurits NM, Zijdewind I (2008) Relation between muscle and brain activity during isometric contractions of the first dorsal interosseus muscle. Hum Brain Mapp 29:281-299 (Pubitemid 351374389)
66. Varela F, Lachaux JP, Rodriguez E, Martinerie J (2001) The brainweb: phase synchronization and large-scale integration. Nat Rev Neurosci 2:229-239 (Pubitemid 33673064)