The origins of neuromuscular fatigue post-stroke

Experimental Brain Research

Volumn 214, Issue 2, 2011, Pages 303-315

  Knorr, S ^a   Ivanova, T D ^b   Doherty, T J ^a   Campbell, J A ^a   Garland, S J ^b  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Cortical silent period; Motor evoked potential; Neuromuscular fatigue; Stroke; Transcranial magnetic stimulation; Voluntary activation

Indexed keywords

ADULT; AGED; ANKLE; ARTICLE; CHRONIC DISEASE; CLINICAL ARTICLE; CONTROLLED STUDY; CORTICAL SILENT PERIOD; ELECTROMYOGRAPHY; EVOKED MUSCLE RESPONSE; FEMALE; HEMIPARESIS; HUMAN; ISOMETRICS; MALE; MAXIMAL VOLUNTARY CONTRACTION; MUSCLE CONTRACTION; MUSCLE ISOMETRIC CONTRACTION; MUSCLE WEAKNESS; NERVE STIMULATION; NERVOUS SYSTEM PARAMETERS; NEUROMUSCULAR BLOCKING; NEUROMUSCULAR FUNCTION; PERONEUS NERVE; PRIORITY JOURNAL; SELF REPORT; SOLEUS MUSCLE; STROKE; STROKE PATIENT; SURVIVOR; TIBIALIS ANTERIOR MUSCLE; TORQUE;

ADULT; AGED; ELECTRIC STIMULATION; FEMALE; HUMANS; MALE; MIDDLE AGED; MUSCLE CONTRACTION; MUSCLE FATIGUE; PARESIS; STROKE;

EID: 80053988607     PISSN: 00144819     EISSN: 14321106     Source Type: Journal    
DOI: 10.1007/s00221-011-2826-5     Document Type: Article

References (60)

1. A Adam CJ De Luca 2005 Firing rates of motor units in human vastus lateralis muscle during fatiguing isometric contractions J Appl Physiol 99 268 280 16036904 10.1152/japplphysiol.01344.2004 (Pubitemid 40934492)
2. GM Allen SC Gandevia DK McKenzie 1995 Reliability of measurements of muscle strength and voluntary activation using twitch interpolation Muscle Nerv 18 593 600 10.1002/mus.880180605 1:STN:280:DyaK2M3nt1KhsQ%3D%3D
3. AT Beekman DJ Deeg J Van Limbeek AW Braam MZ De Vries W Van Tilburg 1997 Criterion validity of the Center for Epidemiologic Studies Depression scale (CES-D): results from a community-based sample of older subjects in The Netherlands Psychol Med 27 231 235 9122304 10.1017/S0033291796003510 1:STN:280:DyaK2s7mvVansA%3D%3D (Pubitemid 27042735)
4. NM Benwell P Sacco GR Hammond ML Byrnes FL Mastaglia GW Thickbroom 2006 Short-interval cortical inhibition and corticomotor excitability with fatiguing hand exercise: a central adaptation to fatigue? Exp Brain Res 170 191 198 16328285 10.1007/s00221-005-0195-7
5. NM Benwell FL Mastaglia GW Thickbroom 2007 Differential changes in long-interval intracortical inhibition and silent period duration during fatiguing hand exercise Exp Brain Res 179 255 262 17464523 10.1007/s00221-006- 0790-2 (Pubitemid 46676149)
6. B Bigland-Ritchie JJ Woods 1984 Changes in muscle contractile properties and neural control during human muscular fatigue Muscle Nerv 7 691 699 10.1002/mus.880070902 1:STN:280:DyaL28%2FhsVWquw%3D%3D (Pubitemid 15209284)
7. B Bigland-Ritchie E Cafarelli NK Vollestad 1986 Fatigue of submaximal static contractions Acta Physiol Scand Suppl 556 137 148 3471051 1:STN:280:DyaL2s7otV2ltA%3D%3D (Pubitemid 17227029)
8. G Borg 1990 Psychophysical scaling with applications in physical work and the perception of exertion Scand J Work Environ Health 16 Suppl 1 55 58 2345867 (Pubitemid 20148982)
9. B Brouwer P Ashby 1990 Corticospinal projections to upper and lower limb spinal motoneurons in man Electroencephalogr Clin Neurophysiol 76 509 519 1701119 10.1016/0013-4694(90)90002-2 1:STN:280:DyaK3M%2FmsFajtw%3D%3D
10. ML Byrnes GW Thickbroom BA Phillips FL Mastaglia 2001 Long-term changes in motor cortical organisation after recovery from subcortical stroke Brain Res 889 278 287 11166720 10.1016/S0006-8993(00)03089-4 1:CAS:528: DC%2BD3MXpsFeqtQ%3D%3D (Pubitemid 32146298)
11. RG Carson S Riek N Shahbazpour 2002 Central and peripheral mediation of human force sensation following eccentric or concentric contractions J Physiol 539 913 925 11897860 10.1113/jphysiol.2001.013385 1:CAS:528:DC%2BD38Xjt1ejsL8%3D (Pubitemid 35175440)
12. Classen J, Schnitzler A, Binkofski F, Werhahn KJ, Kim YS, Kessler KR, Benecke R (1997) The motor syndrome associated with exaggerated inhibition within the primary motor cortex of patients with hemiparetic. Brain 120:605-619 (Pubitemid 27174096)
13. AG Crenshaw S Karlsson B Gerdle J Friden 1997 Differential responses in intramuscular pressure and EMG fatigue indicators during low- versus high-level isometric contractions to fatigue Acta Physiol Scand 160 353 361 9338516 10.1046/j.1365-201X.1997.00168.x 1:CAS:528:DyaK2sXlsVGmsL8%3D (Pubitemid 27342023)
14. Dattola R, Girlanda P, Vita G, Santoro M, Roberto ML, Toscano A, Venuto C, Baradello A, Messina C (1993) Muscle rearrangement in patients with hemiparesis after stroke: an electrophysiological and morphological study. Eur Neurol 33:109-114 (Pubitemid 23100533)
15. Di Lazzaro V, Restuccia D, Oliviero A, Profice P, Ferrara L, Insola A, Mazzone P, Tonali P, Rothwell JC (1998) Effects of voluntary contraction on descending volleys evoked by transcranial stimulation in conscious humans. J Physiol 508(Pt 2):625-633 (Pubitemid 28203974)
16. RM Enoka DG Stuart 1992 Neurobiology of muscle fatigue J Appl Physiol 72 1631 1648 1601767 10.1063/1.351680 1:STN:280:DyaK383ptV2nsg%3D%3D
17. SC Gandevia 1982 The perception of motor commands or effort during muscular paralysis Brain 105 151 159 6461386 10.1093/brain/105.1.151 1:STN:280:DyaL387mtF2iuw%3D%3D (Pubitemid 12001383)
18. SC Gandevia 2001 Spinal and supraspinal factors in human muscle fatigue Physiol Rev 81 1725 1789 11581501 1:STN:280:DC%2BD3MrjsV2isg%3D%3D (Pubitemid 32951808)
19. SC Gandevia DI McCloskey 1977 Changes in motor commands, as shown by changes in perceived heaviness, during partial curarization and peripheral anaesthesia in man J Physiol 272 673 689 592208 1:STN:280:DyaE1c%2FmvVyrtA%3D%3D (Pubitemid 8221844)
20. SC Gandevia GM Allen JE Butler JL Taylor 1996 Supraspinal factors in human muscle fatigue: evidence for suboptimal output from the motor cortex J Physiol 490 529 536 8821149 1:CAS:528:DyaK28XovVOlsg%3D%3D (Pubitemid 26032966)
21. SJ Garland 1991 Role of small diameter afferents in reflex inhibition during human muscle fatigue J Physiol 435 547 558 1770449 1:STN:280: DyaK387it1Wguw%3D%3D
22. SJ Garland AJ McComas 1990 Reflex inhibition of human soleus muscle during fatigue J Physiol 429 17 27 2277345 1:STN:280:DyaK3M7hs1Ggtg%3D%3D (Pubitemid 20327535)
23. Gowland C, Stratford P, Ward M, Moreland J, Torresin W, Van Hullenaar S, Sanford J, Barreca S, Vanspall B, Plews N (1993) Measuring physical impairment and disability with the Chedoke-McMaster Stroke Assessment. Stroke 24:58-63 (Pubitemid 23014383)
24. M Guette J Gondin A Martin 2005 Time-of-day effect on the torque and neuromuscular properties of dominant and non-dominant quadriceps femoris Chronobiol Int 22 541 558 16076653 10.1081/CBI-200062407 (Pubitemid 41140876)
25. Y Hara Y Masakado N Chino 2004 The physiological functional loss of single thenar motor units in the stroke patients: when does it occur? Does it progress? Clin Neurophysiol 115 97 103 14706475 10.1016/j.clinph.2003.08.002 (Pubitemid 38045601)
26. AM Holmback MM Porter D Downham JL Andersen J Lexell 2003 Structure and function of the ankle dorsiflexor muscles in young and moderately active men and women J Appl Physiol 95 2416 2424 12949015 (Pubitemid 37444987)
27. XL Hu KY Tong LK Hung 2006 Firing properties of motor units during fatigue in subjects after stroke J Electromyogr Kinesiol 16 469 476 16311042 10.1016/j.jelekin.2005.09.005 1:STN:280:DC%2BD28rhsVKktQ%3D%3D (Pubitemid 44287569)
28. M Inghilleri A Berardelli G Cruccu M Manfredi 1993 Silent period evoked by transcranial stimulation of the human cortex and cervicomedullary junction J Physiol 466 521 534 8410704 1:STN:280:DyaK2c%2FhsF2lug%3D%3D (Pubitemid 23225241)
29. LA Jones 1995 The senses of effort and force during fatiguing contractions Adv Exp Med Biol 384 305 313 8585460 1:STN:280:DyaK287mslaquw%3D%3D
30. JM Kalmar E Cafarelli 2004 Central fatigue and transcranial magnetic stimulation: effect of caffeine and the confound of peripheral transmission failure J Neurosci Method 138 15 26 10.1016/j.jneumeth.2004.03.006 1:CAS:528:DC%2BD2cXmvFWrtLw%3D (Pubitemid 39485972)
31. JM Kalmar E Cafarelli 2006 Central excitability does not limit postfatigue voluntary activation of quadriceps femoris J Appl Physiol 100 1757 1764 16424071 10.1152/japplphysiol.01347.2005 1:STN:280:DC%2BD283otlOlsw%3D%3D (Pubitemid 43845847)
32. DT Kirkendall 1990 Mechanisms of peripheral fatigue Med Sci Sports Exerc 22 444 449 2205780 1:STN:280:DyaK3czosVenug%3D%3D (Pubitemid 20241709)
33. S Knorr TJ Ivanova TJ Doherty SJ Garland 2009 The origins of fatigue post-stroke Appl Physiol Nutr Metab 34 S50
34. J Liepert 2006 Motor cortex excitability in stroke before and after constraint-induced movement therapy Cogn Behav Neurol 19 41 47 16633018 10.1097/00146965-200603000-00005
35. M Lukacs L Vecsei S Beniczky 2008 Large motor units are selectively affected following a stroke Clin Neurophysiol 119 2555 2558 18809353 10.1016/j.clinph.2008.08.005 1:STN:280:DC%2BD1cnptlOjsQ%3D%3D
36. G Mead J Lynch C Greig A Young S Lewis M Sharpe 2007 Evaluation of fatigue scales in stroke patients Stroke 38 2090 2095 17525397 10.1161/STROKEAHA.106.478941 (Pubitemid 47012273)
37. HJ Michielsen J De Vries GL Van Heck 2003 Psychometric qualities of a brief self-rated fatigue measure: The Fatigue Assessment Scale J Psychosom Res 54 345 352 12670612 10.1016/S0022-3999(02)00392-6 (Pubitemid 38365998)
38. DJ Newham SF Hsiao 2001 Knee muscle isometric strength, voluntary activation and antagonist co-contraction in the first six months after stroke Disabil Rehabil 23 379 386 11394588 10.1080/0963828001006656 1:STN:280:DC%2BD3Mzisleluw%3D%3D (Pubitemid 32492719)
39. Pennisi G, Alagona G, Rapisarda G, Nicoletti F, Costanzo E, Ferri R, Malaguarnera M, Bella R (2002) Transcranial magnetic stimulation after pure motor stroke. Clin Neurophysiol 113:1536-1543 (Pubitemid 35283940)
40. LS Radloff 1977 The CES-D scale: a self-report depression scale for research in the general population Appl Psychol Meas 1 385 401 10.1177/014662167700100306
41. NA Riley M Bilodeau 2002 Changes in upper limb joint torque patterns and EMG signals with fatigue following a stroke Disabil Rehabil 24 961 969 12523950 10.1080/0963828021000007932 1:STN:280:DC%2BD3s%2FhslKrtg%3D%3D (Pubitemid 36032859)
42. P Sacco GW Thickbroom ML Thompson FL Mastaglia 1997 Changes in corticomotor excitation and inhibition during prolonged submaximal muscle contractions Muscle Nerv 20 1158 1166 10.1002/(SICI)1097-4598(199709)20: 9<1158::AID-MUS11>3.0.CO;2-P 1:STN:280:DyaK2svhs1OhsQ%3D%3D (Pubitemid 27352100)
43. D Shinar CR Gross TR Price M Banko PL Bolduc RG Robinson 1986 Screening for depression in stroke patients: the reliability and validity of the Center for Epidemiologic Studies Depression Scale Stroke 17 241 245 3961834 10.1161/01.STR.17.2.241 1:STN:280:DyaL287otVOqsA%3D%3D (Pubitemid 16125247)
44. G Sjogaard B Kiens K Jorgensen B Saltin 1986 Intramuscular pressure, EMG and blood flow during low-level prolonged static contraction in man Acta Physiol Scand 128 475 484 3788624 10.1111/j.1748-1716.1986.tb08002.x 1:STN:280:DyaL2s%2Fnt1OntA%3D%3D (Pubitemid 17182749)
45. UT Slager JD Hsu C Jordan 1985 Histochemical and morphometric changes in muscles of stroke patients Clin Orthop Relat Res 199 159 168 4042473 (Pubitemid 16225192)
46. OR Smith KC Van den Broek M Renkens J Denollet 2008 Comparison of fatigue levels in patients with stroke and patients with end-stage heart failure: application of the fatigue assessment scale J Am Geriatr Soc 56 1915 1919 18771452 10.1111/j.1532-5415.2008.01925.x
47. K Sogaard SC Gandevia G Todd NT Petersen JL Taylor 2006 The effect of sustained low-intensity contractions on supraspinal fatigue in human elbow flexor muscles J Physiol 573 511 523 16556656 10.1113/jphysiol.2005.103598 (Pubitemid 43871063)
48. UM Svantesson KS Sunnerhagen US Carlsson G Grimby 1999 Development of fatigue during repeated eccentric-concentric muscle contractions of plantar flexors in patients with stroke Arch Phys Med Rehabil 80 1247 1252 10527082 10.1016/S0003-9993(99)90024-2 1:STN:280:DyaK1MvlsVajtA%3D%3D (Pubitemid 29474612)
49. JL Taylor SC Gandevia 2001 Transcranial magnetic stimulation and human muscle fatigue Muscle Nerv 24 18 29 10.1002/1097-4598(200101)24:1<18::AID- MUS2>3.0.CO;2-D 1:STN:280:DC%2BD3M%2FpsVCnsw%3D%3D (Pubitemid 32038023)
50. JL Taylor SC Gandevia 2008 A comparison of central aspects of fatigue in submaximal and maximal voluntary contractions J Appl Physiol 104 542 550 18032577 10.1152/japplphysiol.01053.2007 (Pubitemid 351231500)
51. JL Taylor JE Butler GM Allen SC Gandevia 1996 Changes in motor cortical excitability during human muscle fatigue J Physiol 490 519 528 8821148 1:CAS:528:DyaK28XovVOmuw%3D%3D (Pubitemid 26032965)
52. JL Taylor JE Butler SC Gandevia 1999 Altered responses of human elbow flexors to peripheral-nerve and cortical stimulation during a sustained maximal voluntary contraction Exp Brain Res 127 108 115 10424420 10.1007/s002210050779 1:STN:280:DyaK1MzltFOjtA%3D%3D (Pubitemid 29290563)
53. Tergau F, Wanschura V, Canelo M, Wischer S, Wassermann EM, Ziemann U, Paulus W (1999) Complete suppression of voluntary motor drive during the silent period after transcranial magnetic stimulation. Exp Brain Res 124:447-454 (Pubitemid 29132414)
54. GW Thickbroom ML Byrnes SA Archer FL Mastaglia 2002 Motor outcome after subcortical stroke: MEPs correlate with hand strength but not dexterity Clin Neurophysiol 113 2025 2029 12464343 10.1016/S1388-2457(02)00318-8 (Pubitemid 35441073)
55. ED Toffola D Sparpaglione A Pistorio M Buonocore 2001 Myoelectric manifestations of muscle changes in stroke patients Arch Phys Med Rehabil 82 661 665 11346844 10.1053/apmr.2001.22338 1:STN:280:DC%2BD3M3ltF2htQ%3D%3D (Pubitemid 32423583)
56. BJ Udby JF Nielsen 2009 Evidence of increased motoneuron excitability in stroke patients without clinical spasticity Neurorehabil Neural Repair 23 14 16
57. Y Ugawa Y Terao R Hanajima K Sakai I Kanazawa 1995 Facilitatory effect of tonic voluntary contraction on responses to motor cortex stimulation Electroencephalogr Clin Neurophysiol 97 451 454 8536598 10.1016/0924-980X(95) 00214-6 1:STN:280:DyaK287js1WnsA%3D%3D (Pubitemid 26019400)
58. KJ Werhahn E Kunesch S Noachtar R Benecke J Classen 1999 Differential effects on motorcortical inhibition induced by blockade of GABA uptake in humans J Physiol 517 Pt 2 591 597 10332104 10.1111/j.1469-7793.1999.0591t.x 1:CAS:528:DyaK1MXktVyktrc%3D (Pubitemid 29296371)
59. SA Wilson RJ Lockwood GW Thickbroom FL Mastaglia 1993 The muscle silent period following transcranial magnetic cortical stimulation J Neurol Sci 114 216 222 8445404 10.1016/0022-510X(93)90301-E 1:STN:280:DyaK3s7oslKmtQ%3D%3D (Pubitemid 23058620)
60. U Ziemann 2004 TMS and drugs Clin Neurophysiol 115 1717 1729 15261850 10.1016/j.clinph.2004.03.006 1:CAS:528:DC%2BD2cXlsl2lsLw%3D (Pubitemid 38952939)