Cortical and segmental excitability during fatiguing contractions of the soleus muscle in humans

Clinical Neurophysiology

Volumn 123, Issue 2, 2012, Pages 335-343

  Iguchi, Masaki ^a   Shields, Richard K ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

H reflex; Muscle fatigue; Soleus; Transcranial magnetic stimulation

Indexed keywords

ADULT; AMPLITUDE MODULATION; ARM; ARTICLE; BRAIN CORTEX; CLINICAL ARTICLE; ELECTROMYOGRAM; EVOKED MUSCLE RESPONSE; FLEXOR REFLEX; HOFFMANN REFLEX; HUMAN; MALE; MOTOR CORTEX; MOTOR PERFORMANCE; MUSCLE CONTRACTION; MUSCLE EXCITATION; MUSCLE FATIGUE; MUSCLE RELAXATION; PRIORITY JOURNAL; SOLEUS MUSCLE; TASK PERFORMANCE; TORQUE; TRANSCRANIAL MAGNETIC STIMULATION;

ADULT; EVOKED POTENTIALS, MOTOR; FEMALE; H-REFLEX; HUMANS; MALE; MOTOR CORTEX; MUSCLE CONTRACTION; MUSCLE FATIGUE; MUSCLE, SKELETAL; YOUNG ADULT;

EID: 84855528254     PISSN: 13882457     EISSN: 18728952     Source Type: Journal    
DOI: 10.1016/j.clinph.2011.06.031     Document Type: Article

References (58)

1. Amann M., Proctor L.T., Sebranek J.J., Pegelow D.F., Dempsey J.A. Opioid-mediated muscle afferents inhibit central motor drive and limit peripheral muscle fatigue development in humans. J Physiol 2009, 587:271-283.
2. Bawa P., Chalmers G.R., Stewart H., Eisen A.A. Responses of ankle extensor and flexor motoneurons to transcranial magnetic stimulation. J Neurophysiol 2002, 88:124-132.
3. Benwell N.M., Mastaglia F.L., Thickbroom G.W. Differential changes in long-interval intracortical inhibition and silent period duration during fatiguing hand exercise. Exp Brain Res 2007, 179:255-262.
4. Bigland-Ritchie B., Johansson R., Lippold O.C., Woods J.J. Contractile speed and EMG changes during fatigue of sustained maximal voluntary contractions. J Neurophysiol 1983, 50:313-324.
5. Bongiovanni L.G., Hagbarth K.E. Tonic vibration reflexes elicited during fatigue from maximal voluntary contractions in man. J Physiol 1990, 423:1-14.
6. Brasil-Neto J.P., Cammarota A., Valls-Sole J., Pascual-Leone A., Hallett M., Cohen L.G. Role of intracortical mechanisms in the late part of the silent period to transcranial stimulation of the human motor cortex. Acta Neurol Scand 1995, 92:383-386.
7. Burke D., Hicks R., Gandevia S.C., Stephen J., Woodforth I., Crawford M. Direct comparison of corticospinal volleys in human subjects to transcranial magnetic and electrical stimulation. J Physiol 1993, 470:383-393.
8. Burke D., Kiernan M., Mogyoros I., Bostock H. Susceptibility to conduction block: differences in the biophysical properties of cutaneous afferents and motor axons. Physiology of ALS and related diseases 1997, 43-53. Elsevier, Amsterdam. J. Kimura, R. Kaji (Eds.).
9. Butler J.E., Taylor J.L., Gandevia S.C. Responses of human motoneurons to corticospinal stimulation during maximal voluntary contractions and ischemia. J Neurosci 2003, 23:10224-10230.
10. Damron L.A., Dearth D.J., Hoffman R.L., Clark B.C. Quantification of the corticospinal silent period evoked via transcranial magnetic stimulation. J Neurosci Methods 2008, 173:121-128.
11. Darling W.G., Wolf S.L., Butler A.J. Variability of motor potentials evoked by transcranial magnetic stimulation depends on muscle activation. Exp Brain Res 2006, 174:376-385.
12. Daskalakis Z.J., Molnar G.F., Christensen B.K., Sailer A., Fitzgerald P.B., Chen R. An automated method to determine the transcranial magnetic stimulation-induced contralateral silent period. Clin Neurophysiol 2003, 114:938-944.
13. de Noordhout A.M., Rapisarda G., Bogacz D., Gerard P., De Pasqua V., Pennisi G., et al. Corticomotoneuronal synaptic connections in normal man: an electrophysiological study. Brain 1999, 122(Pt 7):1327-1340.
14. Eccles J. The physiology of synapses 1964, Springer, Berlin, Heidelberg, New York.
15. Enoka R.M., Hutton R.S., Eldred E. Changes in excitability of tendon tap and Hoffmann reflexes following voluntary contractions. Electroencephalogr Clin Neurophysiol 1980, 48:664-672.
16. Etnyre B.R., Kinugasa T., Abraham L.D. Post-contraction variations in motor pool excitability. Electromyogr Clin Neurophysiol 1990, 30:259-264.
17. Floeter M.K. Cutaneous silent periods. Muscle Nerve 2003, 28:391-401.
18. Fuhr P., Agostino R., Hallett M. Spinal motor neuron excitability during the silent period after cortical stimulation. Electroencephalogr Clin Neurophysiol 1991, 81:257-262.
19. Gandevia S.C. Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 2001, 81:1725-1789.
20. Garland S.J. Role of small diameter afferents in reflex inhibition during human muscle fatigue. J Physiol 1991, 435:547-558.
21. Garner S.H., Hicks A.L., McComas A.J. Prolongation of twitch potentiating mechanism throughout muscle fatigue and recovery. Exp Neurol 1989, 103:277-281.
22. Griffin L., Garland S.J., Ivanova T., Gossen E.R. Muscle vibration sustains motor unit firing rate during submaximal isometric fatigue in humans. J Physiol 2001, 535:929-936.
23. Hicks A.L., Kent-Braun J., Ditor D.S. Sex differences in human skeletal muscle fatigue. Exerc Sport Sci Rev 2001, 29:109-112.
24. Hoffman B.W., Oya T., Carroll T.J., Cresswell A.G. Increases in corticospinal responsiveness during a sustained submaximal plantar flexion. J Appl Physiol 2009, 107:112-120.
25. Hultborn H., Illert M., Nielsen J., Paul A., Ballegaard M., Wiese H. On the mechanism of the post-activation depression of the H-reflex in human subjects. Exp Brain Res 1996, 108:450-462.
26. Hunter S.K., Butler J.E., Todd G., Gandevia S.C., Taylor J.L. Supraspinal fatigue does not explain the sex difference in muscle fatigue of maximal contractions. J Appl Physiol 2006, 101:1036-1044.
27. Hutton R.S., Smith J.L., Eldred E. Post-contraction sensory discharge from muscle and its source. J Neurophysiol 1973, 36:1090-1103.
28. Inghilleri M., Berardelli A., Cruccu G., Manfredi M. Silent period evoked by transcranial stimulation of the human cortex and cervicomedullary junction. J Physiol 1993, 466:521-534.
29. Johnson M.A., Polgar J., Weightman D., Appleton D. Data on the distribution of fibre types in thirty-six human muscles. An autopsy study. J Neurol Sci 1973, 18:111-129.
30. Jovanovic K., Anastasijevic R., Vuco J. Reflex effects on gamma fusimotor neurones of chemically induced discharges in small-diameter muscle afferents in decerebrate cats. Brain Res 1990, 521:89-94.
31. Kawakami Y., Amemiya K., Kanehisa H., Ikegawa S., Fukunaga T. Fatigue responses of human triceps surae muscles during repetitive maximal isometric contractions. J Appl Physiol 2000, 88:1969-1975.
32. Kernell D., Monster A.W. Motoneurone properties and motor fatigue. An intracellular study of gastrocnemius motoneurones of the cat. Exp Brain Res 1982, 46:197-204.
33. Kernell D., Monster A.W. Time course and properties of late adaptation in spinal motoneurones of the cat. Exp Brain Res 1982, 46:191-196.
34. Kouzaki M., Shinohara M. Steadiness in plantar flexor muscles and its relation to postural sway in young and elderly adults. Muscle Nerve 2010, 42:78-87.
35. Kukulka C.G., Clamann H.P. Comparison of the recruitment and discharge properties of motor units in human brachial biceps and adductor pollicis during isometric contractions. Brain Res 1981, 219:45-55.
36. Levenez M., Garland S.J., Klass M., Duchateau J. Cortical and spinal modulation of antagonist coactivation during a submaximal fatiguing contraction in humans. J Neurophysiol 2008, 99:554-563.
37. Ljubisavljevic M., Jovanovic K., Anastasijevic R. Changes in discharge rate of fusimotor neurones provoked by fatiguing contractions of cat triceps surae muscles. J Physiol 1992, 445:499-513.
38. Macefield G., Hagbarth K.E., Gorman R., Gandevia S.C., Burke D. Decline in spindle support to alpha-motoneurones during sustained voluntary contractions. J Physiol 1991, 440:497-512.
39. Magladery J.W., Porter W.E., Park A.M., Teasdall R.D. Electrophysiological studies of nerve and reflex activity in normal man IV. The two-neurone reflex and identification of certain action potentials from spinal roots and cord. Bull Johns Hopkins Hosp 1951, 88:499-519.
40. Manca M., Cavazzini L., Cavazza S., Salvadori T., DeGrandis D., Basaglia N. H reflex excitability following voluntary muscle contraction of different duration. Electromyogr Clin Neurophysiol 1998, 38:381-384.
41. Martin P.G., Weerakkody N., Gandevia S.C., Taylor J.L. Group III and IV muscle afferents differentially affect the motor cortex and motoneurones in humans. J Physiol 2008, 586:1277-1289.
42. Nielsen J., Morita H., Baumgarten J., Petersen N., Christensen L.O. On the comparability of H-reflexes and MEPs. Electroencephalogr Clin Neurophysiol Suppl 1999, 51:93-101.
43. Nordlund M.M., Thorstensson A., Cresswell A.G. Central and peripheral contributions to fatigue in relation to level of activation during repeated maximal voluntary isometric plantar flexions. J Appl Physiol 2004, 96:218-225.
44. Oya T., Riek S., Cresswell A.G. Recruitment and rate coding organisation for soleus motor units across entire range of voluntary isometric plantar flexions. J Physiol 2009, 587:4737-4748.
45. Pettorossi V.E., Della Torre G., Bortolami R., Brunetti O. The role of capsaicin-sensitive muscle afferents in fatigue-induced modulation of the monosynaptic reflex in the rat. J Physiol 1999, 515(Pt 2):599-607.
46. Ridding M.C., Rothwell J.C. Reorganisation in human motor cortex. Can J Physiol Pharmacol 1995, 73:218-222.
47. Roick H., von Giesen H.J., Benecke R. On the origin of the postexcitatory inhibition seen after transcranial magnetic brain stimulation in awake human subjects. Exp Brain Res 1993, 94:489-498.
48. Rossi A., Decchi B., Ginanneschi F. Presynaptic excitability changes of group Ia fibres to muscle nociceptive stimulation in humans. Brain Res 1999, 818:12-22.
49. Rudomin P. Presynaptic selection of afferent inflow in the spinal cord. J Physiol Paris 1999, 93:329-347.
50. Sale D., Quinlan J., Marsh E., McComas A.J., Belanger A.Y. Influence of joint position on ankle plantarflexion in humans. J Appl Physiol 1982, 52:1636-1642.
51. Spielmann J.M., Laouris Y., Nordstrom M.A., Robinson G.A., Reinking R.M., Stuart D.G. Adaptation of cat motoneurons to sustained and intermittent extracellular activation. J Physiol 1993, 464:75-120.
52. Stein R.B., Estabrooks K.L., McGie S., Roth M.J., Jones K.E. Quantifying the effects of voluntary contraction and inter-stimulus interval on the human soleus H-reflex. Exp Brain Res 2007, 182:309-319.
53. Taylor J.L. Stimulation at the cervicomedullary junction in human subjects. J Electromyogr Kinesiol 2006, 16:215-223.
54. Taylor J.L., Gandevia S.C. A comparison of central aspects of fatigue in submaximal and maximal voluntary contractions. J Appl Physiol 2008, 104:542-550.
55. Taylor J.L., Todd G., Gandevia S.C. Evidence for a supraspinal contribution to human muscle fatigue. Clin Exp Pharmacol Physiol 2006, 33:400-405.
56. Vagg R., Mogyoros I., Kiernan M.C., Burke D. Activity-dependent hyperpolarization of human motor axons produced by natural activity. J Physiol 1998, 507(Pt 3):919-925.
57. Woods J.J., Furbush F., Bigland-Ritchie B. Evidence for a fatigue-induced reflex inhibition of motoneuron firing rates. J Neurophysiol 1987, 58:125-137.
58. Ziemann U., Netz J., Szelenyi A., Homberg V. Spinal and supraspinal mechanisms contribute to the silent period in the contracting soleus muscle after transcranial magnetic stimulation of human motor cortex. Neurosci Lett 1993, 156:167-171.