A dynamic network involving MI-SI, Sll-insular, medial insular, and cingulate cortices controls muscular activity during an isometric contraction reaction time task

Human Brain Mapping

Volumn 30, Issue 2, 2009, Pages 675-688

  Jouanin, Jean Claude ^a,c   Pérès, Michel ^a   Ducorps, Antoine ^b   Renault, Bernard ^b  

^a Army Department   (France)

^b PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^c Institut de Medecine Aerospatiale du Service de Sante des Armees   (France)

Author keywords

Brain plasticity; Event related magnetic fields; Isometric contraction; M1 S1; Medial insula; MEG; Muscle fatigue; Posterior cingulate cortex; Reaction time; SII insula

Indexed keywords

ADULT; ARTICLE; BRAIN CORTEX; ELECTROMYOGRAPHY; EVOKED MUSCLE RESPONSE; FINGER; HAND MUSCLE; HUMAN; HUMAN EXPERIMENT; MAGNETOENCEPHALOGRAPHY; MALE; MUSCLE FATIGUE; MUSCLE ISOMETRIC CONTRACTION; NORMAL HUMAN; PRIORITY JOURNAL; REACTION TIME; VISUAL STIMULATION;

ADULT; BRAIN MAPPING; CEREBRAL CORTEX; ELECTROMYOGRAPHY; GYRUS CINGULI; HUMANS; ISOMETRIC CONTRACTION; MAGNETOENCEPHALOGRAPHY; MALE; MOTOR CORTEX; MUSCLE FATIGUE; MUSCLE STRENGTH; MUSCLE, SKELETAL; NERVE NET; NEURONAL PLASTICITY; PSYCHOMOTOR PERFORMANCE; REACTION TIME; SOMATOSENSORY CORTEX; YOUNG ADULT;

EID: 59949085968     PISSN: 10659471     EISSN: None     Source Type: Journal    
DOI: 10.1002/hbm.20534     Document Type: Article

References (86)

1. Asmussen E (1979): Muscle fatigue. Med Sci Sports Exerc 11:313-321.
2. Balzamo E, Marquis P, Chauvel P, Regis J (2004): Short-latency components of evoked potentials to median nerve stimulation recorded by intracerebral electrodes in the human pre- and postcentral areas. Clin Neurophysiol 115:1616-1623.
3. Baumgartner C, Doppelbauer L, Deecke L, Barth DS, Zeithlofer J, Lindinger G, Sutherling W (1991): Neuromagnetic investigation of somatotopy of human hand somatosensory cortex. Exp Brain Res 87:641-648.
4. Belhaj-Saïf A, Fourment A, Maton B (1996): Adaptation of the pre-central cortical command to elbow muscle fatigue. Exp Brain Res 111:405-416.
5. Bigland-Ritchie B (1981): EMG/force relations and fatigue in human voluntary contractions. Exerc Sports Sci Rev 9:75-117.
6. Bigland-Ritchie B, Furbush F, Woods JJ (1986): Fatigue of intermittent submaximal voluntary contractions: Central and peripheral factors. J Appl Physiol 61:421-429.
7. Bingel U, Lorenz J, Glauche V, Knab R, Glascher J, Weiller C, Buchel C (2004): Somatotopic organization of human somatosensory cortices for pain: A single trial fMRI study. Neuroimage 23:224-232.
8. Brasil-Neto JP, Cohen LG, Hallet M (1994). Central fatigue as revealed by postexercise decrement of motor evoked potentials. Muscle Nerve 17:713-719.
9. Brooks JCW, Tracey I (2007). The insula: A multidimensional integration site of pain. Pain 128:1-2.
10. Brooks JCW, Zambreanu L, Godinez A, Craig AD, Tracey I (2005): Somatotopic organization of the human insula to painful heat studied with high-resolution functional imaging. Neuroimage 27:201-209.
11. Cheyne D, Endo H, Takeda T, Weinberg H (1997): Sensory feedback contributes to early mouvement-evoked fields during voluntary finger movements in humans. Brain Res 771:196-202.
12. Cheyne D, Bakhtazad L, Gaetz W (2006). Spatiotemporal mapping of cortical activity accompanying voluntary movements using an event-related beamforming approach. Hum Brain Mapp 27:213-229.
13. Ciubotariu A, Arendt-Nielsen L, Graven-Nielsen T (2004): The influence of muscle pain and fatigue on the activity of synergistic muscles of the leg. Eur J Appl Physiol 91:604-614.
14. Conway BA, Halliday DM, Farmer SF, Shanani U, Mass P, Weir AI, Rosenberg JR (1995): Synchronization between motor cortex and spinal motoneural pool during the performance of a maintained motor task in man. J Physiol 489:917-924.
15. Craig AD, Reiman EM, Evans A, Bushnell MC (1996): Functional imaging of an illusion of pain. Nature 384:258-260.
16. 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.
17. Dettmers C, Fink GR, Leman RN, Stephan KM, Passingham RE, Silbersweigh 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.
18. Dettmers C, Lemon RN, Stephan KM, Fink GR, Fractowiak RS (1996): Cerebral activation during the exertion of sustained static force in man. Neuroreport 7:2103-2110.
19. Di Guilio C, Daniele F, Tipton C (2006): Angelo Mosso and muscular fatigue: 116 years after the first congress of physiologists: IUPS commemoration. Adv Physiol Edu 30:51-57.
20. Endo H, Kizuka T, Masuda T, Takeda T (1999): Automatic activation in the human primary motor cortex synchronized with movement preparation. Cogn Brain Res 3:229-239.
21. Endo H, Takeda T, Kizuka T, Kikuchi Y, Masuda T, Kumagai T (1996): Estimation of movement-related brain activities with visual stimuli. Visualization of information processing in the human brain: Electroencephal Clin Neurophysiol, Suppl. 47: 273-281.
22. Ferretti A, Babiloni C, Del Gratta C, Caulo M, Tartao A, Bonomo L, Rossini PM, Romani GL (2003): Functional topography of the secondary somatosensory cortex for nonpainful and painful stimuli: An fMRI study. Neuroimage 20:1625-1638.
23. Forss N, Jousmaki V (1998): Sensorimotor integration in human primary and secondary somatosensory cortices. Brain Res 781:259-267.
24. Fuglevand AJ, Zackowski KM, Juey KA, Enoka RM (1993): Impairment of neuromuscular propagation during human fatiguing contractions at submaximal forces. J Physiol 460:549-572.
25. Gandevia SC (1998): Neural control in human muscle fatigue: Changes in muscle afferents, moto neurons and moto cortical drive. Acta Physiol Scand 162:275-283.
26. Gandevia SC (2001): Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81:1725-1789.
27. Garcia-Larrea L, Frot M, Valeriani M (2003): Brain generators of laser-evoked potentials: From dipoles to functional significance. Clin Neurophysiol 33:279-292.
28. Garland SJ, Enoka RM, Serrano LP, Robinson GA (1994): Behaviour of motor units in human biceps brachii during a submaximal fatiguing contraction. J Appl Physiol 76:2411-2419.
29. Gelnar PA, Krauss BR, Sheehe PR, Szeverenyl NM, Apkarian V (1999): A comparative fMRI study of cortical representations for thermal painful, vibrotactile, and motor performance tasks. Neuroimage 10:460-482.
30. Gerdle B, Karlssson S (1994): The mean frequency of the knee extensors is torque dependent both in the unfatigued and the fatigued states. Clin Physiol 14:419-432.
31. Gross J, Tass PA, Salenius S, Hari R, Freund HJ, Schnitzler A (2000): Cortico-muscular synchronization during isometric muscle contraction in humans as revealed by magnetoencepha-lography. J Physiol 527:623-631.
32. Hagberg M (1981): Muscular endurance and surface electro-myogram in isometric and dynamic exercise. J Appl Physiol 51: 1-7.
33. Hari R, Forss N (1999): Magnetoencephalography in the study of human somatosensory cortical processing. Phil Trans R Soc Lond 354:1145-1154.
34. Henderson LA, Gandevia SC, Macefield VG (2007). Somatotopic organizationb of the processing of muscle and cutaneous pain in the left and right insula cortex: A single-trial fMRI study. Pain 128:20-30.
35. Howland EW, Wakai RT, Mjaanes BA, Balog JP, Cleeland CS (1995): Whole head mapping of magnetic fields following painful electric finger shock. Cogn Brain Res 2:165-172.
36. Iannetti GD, Zambreanu L, Cruccu G, Tracey I (2005): Operculoinsular cortex encodes pain intensity at the earliest stages of cortical processing as indicated by amplitude of laser-evoked potentials in humans. Neuroscience 131:199-208.
37. Inui K, Tran DT, Qiu Y, Wang X, Hoshiyama M, Kakigi R (2003): A comparative magnetoencephalographic study of cortical activations evoked by noxious and innocuous somatosensory stimulations. Neuroscience 120:235-248.
38. Ishibashi H, Tobimatsu S, Shigeto H, Morioka T, Yamamoto T, Fukui M (2000): Differential interaction of somatosensory inputs in the human primary sensory cortex: A magnetoence-phalographic study. Clin Neurophysiol 111:1095-1102.
39. Jouanin JC, Kahn JF, Grucza R, Monod H (1993): Changes in the heart rate and electromyogram beyond the limit time of an isotonic isometric contraction. Eur J Appl Physiol 67:208-212.
40. Kahn JF, Monod H (1989): Fatigue induced by static work. Ergonomics 32:839-846.
41. Kakigi R, Koyama S, Hoshiyama M, Wanatabe S, Shimojo M, Kitamura Y (1995): Gating of somatosensory evoked responses during active finger movements: Magnetoencephalographic studies. J Neurol Sci 128:195-204.
42. Kakigi R, Inui K, Tran DT, Qiu Y, Wang X, Watanabe S, Hoshiyama M (2004): Human brain processing and central mechanisms of pain as observed by electro- and magneto-encepha-lography. J Chin Med Assoc 67:377-386.
43. Kleine BU, Stegeman DF, Mund D, Anders C (2001): Influence of motoneurons firing synchronization on SEMG characteristics in dependence of electrode position. J Appl Physiol 91:1588-1599.
44. Kristeva R, Cheyne D, Lang W, Lindinger G, Deecke L (1990): Movement-related potentials accompanying unilateral and bilateral finger movements with different inertial loads. Electro-encephal Clin Neurophysiol 75:410-418.
45. Kristeva R, Cheyne D, Deecke L (1991): Neuromagnetic fields accompanying unilateral and bilateral voluntary movements: Topography and analysis of cortical sources. Electroenceph Clin Neurophysiol 81:284-298.
46. Kristeva-Feige R, Walter H, Lutkenhoner B, Hampson S, Ross B, Knorr Y, Steinmetz H, Cheyne D (1994): A neuromagnetic study of the functional organization of the sensorimotor cortex. Eur J Neurosci 6:632-639.
47. Lin YY, Simoes C, Forss N, Hari R (2000): Differential effects of muscle contraction form various body parts on neuromagnetic somatosensory responses. Neuroimage 11:334-340.
48. Liu JZ, Dai TH, Sahghal V, Brown RW, Yue GH (2002): Nonlinear cortical modulation of muscle fatigue: A functional MRI study. Brain Res 957:320-329.
49. Liu JZ, Shan ZY, Zhang LD, Sahgal V, Brown RW, Yue GH (2003): Human brain activation during sustained and intermittent sub-maximal fatigue muscle contractions: An fMRI study. J Neuro-physiol 90:300-312.
50. Löscher WN, Cresswell AG, Thorstensson A (1996): Central fatigue during a long-lasting submaximal contraction of the triceps surae. Exp Brain Res 108:305-314.
51. Mannion AF, Dolan P (1996): Relationship between myoelectric and mechanical manifestations of fatigue in the quadriceps femoris muscle group. Eur J Appl Physiol 74:411-419.
52. Maton B (1981): Human motor unit activity during the onset of muscle fatigue in submaximal isometric isotonic contraction. Eur J Appl Physiol 46:271-281.
53. Maton B (1991): Central nervous changes in fatigue induced by local work. In: Atlan G, Beliveau L,Bouissou P, Masson, editors. Muscle Fatigue: Biochemical and Physiological Aspects, Mason, Paris. pp 207-221.
54. Maton B, Gamet D (1989): The fatigability of two agonistic muscles in human isometric voluntary submaximal contraction: An EMG study. II. Motor unit firing rate and recruitment. Eur J Appl Physiol 58:369-374.
55. Masakado Y, Ushiba J, Tomita Y, Chino N (2004): Cortical neuro-magnetic activity associated with cutaneomuscular reflex. Electromyog Clin Neurophysiol 44:83-87.
56. Meunier S, Garnero L, Ducorps A, Mazières L, Lehericy S, Tézenas du Montcel S, Renault B, Vidailhet M (2001): Human brain mapping in dystonia reveals both endophenotypic traits and adaptive reorganization. Ann Neurol 50:521-527.
57. Mima T, Nagamine T, Nakamura K, Shibasaki H (1998): Attention modulates both primary and second somatosensory cortical activities in humans: A magnetoencephalography study. J Neu-rophysiol 80:2215-2221.
58. Niddam DM, Yeh TC, Wu YT, Lee PL, Ho LT, Arendt-Nielsen L, Chen AC, Hsieh JC (2002): Event-related functional MRI study on central representation of acute muscle pain induced by electrical stimulation. Neuroimage 17:1437-1450.
59. Nordlund MN, Thortensson A, Cresswell AG (2004): Central and peripheral contributions to fatigue in relation to level of activation during repeated maximal voluntary isometric plantar flexions. J Appl Physiol 96:218-225.
60. Onishi H, Soma T, Kameyama S, Oishi M, Fuijmoto A, Oyama M, Furusawa A, Kurokawa Y (2006). Cortical neuromagnetic activation accompanying two types of voluntary finger extension. Brain Res 1123:112-118.
61. Oshiro Y, Fuijita N, Tanaka H, Hirabuki N, Nakamura H, Yoshiya I (1998): Functional mapping of pain-related activation with echo-planar MRI: Significance of the SII-insular region. Neuro-report 9:2285-2289.
62. Ostrowsky K, Magnin M, Ryvlin P, Isnard J, Guenot M, Maugière F (2002): Representation of pain and somatic sensation in the human insula: A study of responses to direct electrical cortical stimulation. Cerebral Cortex 12:376-385.
63. Paasüke M, Ereline J, Gapeyeva H (1999): Neuromuscular fatigue during repeated exhaustive submaximal static contractions of knee extensor muscles in endurance-trained, power-trained and untrained men. Acta Physiol Scand 166:319-326.
64. Peyron R, Laurent B, Garcia-Larrea L (2000): Functional imaging of brain responses to pain. A review and meta-analysis. Neuro-physiol Clin 30:263-288.
65. Peyron R, Frot M, Schneider F, Garcia-Larrea L, Mertens P, Barral FG, Sindou M, Laurent B, Maugiere F (2002): Role of operculoinsular cortices in human pain processing: Converging evidence from PET, fMRI, dipole modelling, and intracerebral recordings of evoked potentials. Neuroimage 17:1336-1446.
66. Pizzela V, Tecchio F, Romani JL, Rossini PM (1999): Functional localization of the sensory hand area with respect to the motor central gyrus knob. Neuroreport 10:3809-3814.
67. Qiu Y, Inui K, Wang X, Nguyen BT, Tran TD, Kakigi R (2004): Effects of distraction on magnetoencephalographic responses ascending through C-fibers in humans. Clin Neurophysiol 115: 636-646.
68. Ringler R, Greiner L, Kohlloeffel L, Handwerker HO, Forster C (2003): BOLD effects in different areas of the cerebral cortex during painful mechanical stimulation. Pain 105:445-453.
69. Ruben J, Schwiemann J, Deuchert M, Meyer M, Krause T, Curio G, Villringer K, Kurth R, Villringer A (2001): Somatotopic organization of human secondary somatosensory cortex. Cereb Cortex 11:463-473.
70. Salenius S, Portin K, Salmelin R, Hari R (1997): Cortical control of human motoneuron firing during isometric contraction. J Neu-rophysiol 77:3401-3405.
71. Schreckenberger M, Siessmeier T, Viertmann A, Landvogt C, Buchnolz HG, Rolke R, Treede RD, Bartenstein P, Birklein F (2005): The unpleasantness of tonic pain is encoded by the insular cortex. Neurology 64:1175-1183.
72. Sohn MK, Garven-Nielsen L, Arendt-Nielsen l, Svensson P (2000): Inhibition of the motor unit firing during experimental muscle pain in humans. Muscle Nerve 23:1219-1226.
73. Suk J, Ribary U, Cappell J, Yamamoto T, Llinas R (1991): Anatomical localization revealed by MEG recordings of the human somatosensory system. Electroencephalog Clin Neurophysiol 78:185-196.
74. Svensson P, Minoshima S, Beydoun A, Morrow TJ, Casey KL (1997): Cerebral processing of acute skin and muscle pain in humans. J Neurophysiol 78:450-460.
75. Talairach J, Tournoux P (1988): Coplanar Stereotaxic Atlas of the Human Brain. Stuttgart: Thieme Medical Publisher. p 122.
76. Taylor JL, Allen GM, Butler JE, Gandevia SC (2000). Supraspinal fatigue during intermittent maximal voluntary contractions of the human elbow flexors. J Appl Physiol 89:305-313.
77. Tran TD, Inui K, Hoshiyama M, Lam K, Qiu Y, Kakigi R (2002): Cerebral activation by the signals ascending through unmyelinated C-fibers in humans: An magnetoencephalographic study. Neuroscience 113:375-386.
78. Vallbo AB (1971): Muscle spindle response at the onset of isometric voluntary contractions in man. Time difference between fusimotor and skeletal motor effects. J Physiol 218: 405-431.
79. Vogt BA, Berger GR, Derbyshire SW (2003): Structural and functional dichotomy of human midcingulate cortex. Eur J Neuro-sci 18:3134-3144.
80. Vrána J, Poláček H, Stančák A (2005): Somatosensory-evoked potentials are influenced differently by isometric muscle contraction of stimulated and non-stimulated hand in humans. Neurosci Lett 386:170-175.
81. Wannier TM, Maier MA, Hepp-Reymond MC (1991): Contrasting properties of monkey somatosensory and motor cortex neurons activated during the control of force in precision grip. J Neuro-physiol 65:572-589.
82. Weinberg H, Cheyne D, Crisp D (1990): Electroencephalographic and magnetoencephalographic studies of motor function. Adv Neurol 54:193-205.
83. Yang TT, Gallen CC, Schwartz BJ, Bloom FE (1993): Noninvasive somatosensory homunculus mapping in humans by using a large-array biomagnetometer. Proc Nat Acad Sci USA 90:3098-3102.
84. Yeung SS, Au AL, Chow CC (1999): Effects of fatigue on the temporal neuromuscular control of vastus medialis muscle in humans. Eur J Appl Physiol 80:379-385.
85. Youell PD, Wise RG, Bentley DE, Dickinson MR, King TA, Tracey I, Jones AK (2004): Lateralization of nociceptive processing in the human brain: A functional magnetic resonance imaging study. Neuroimage 23:1068-1077.
86. Zhou S, McKenna MJ, Lawson DL, Morrison WE, Fairweather I (1996): Effects of fatigue and sprint training on electromechanical delay of knee extensor muscles. Eur J Appl Physiol 72:410-416.