Neural control of rhythmic arm cycling after stroke

Journal of Neurophysiology

Volumn 108, Issue 3, 2012, Pages 891-905

  Paul Zehr, E ^a,b   Loadman, Pamela M ^a   Hundza, Sandra R ^a,b  

^a UNIVERSITY OF VICTORIA   (Canada)

^b INTERNATIONAL COLLABORATION ON REPAIR DISCOVERIES   (Canada)

Author keywords

Cerebrovascular accident; Interlimb; Locomotion; Plasticity; Reflexes; Rehabilitation; Stroke

Indexed keywords

ADULT; AGED; ARM MOVEMENT; ARTICLE; CLINICAL ARTICLE; FEMALE; HUMAN; MALE; MOTOR CONTROL; MUSCLE REFLEX; NERVE CELL PLASTICITY; PRIORITY JOURNAL; RADIAL NERVE; REFLEX DISORDER; STROKE; TASK PERFORMANCE;

ADULT; AGED; AGED, 80 AND OVER; ARM; ELECTRIC STIMULATION; ELECTROMYOGRAPHY; FEMALE; HUMANS; MALE; MIDDLE AGED; MOVEMENT; PERIODICITY; RADIAL NERVE; REFLEX; STROKE;

EID: 84865640000     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01152.2011     Document Type: Article

References (75)

1. Alibiglou L, Brown DA. Impaired muscle phasing systematically adapts to varied relative angular relationships during locomotion in people poststroke. J Neurophysiol 105: 1660-1670, 2011.
2. Barbeau H, Visintin M. Optimal outcomes obtained with body-weight support combined with treadmill training in stroke subjects. Arch Phys Med Rehabil 84: 1458-1465, 2003.
3. Barthelemy D, Bo Nielsen JB. Corticospinal contribution to arm muscle activity during human walking. J Physiol 588: 967-979, 2010.
4. Barzi Y, Zehr EP. Rhythmic arm cycling suppresses hyperactive soleus H-reflex amplitude after stroke. Clin Neurophysiol 119: 1443-1452, 2008.
5. Beer RF, Dewald JP, Rymer WZ. Deficits in the coordination of multijoint arm movements in patients with hemiparesis: evidence for disturbed control of limb dynamics. Exp Brain Res 131: 305-319, 2000.
6. Bohannon R, Smith M. Interrater reliability on a modified Ashworth scale of muscle spasticity. Phys Ther 67: 206-207, 1987.
7. Bo Nielsen J. Motoneuronal drive during human walking. Brain Res Rev 40: 192-201, 2002.
8. Brown DA, Kautz SA. Increased workload enhances force output during pedaling exercise in persons with poststroke hemiplegia. Stroke 29: 598-606, 1998.
9. Brown DA, Kautz SA, Dairaghi CA. Muscle activity adapts to anti-gravity posture during pedalling in persons with post-stroke hemiplegia. Brain 120: 825-837, 1997.
10. Brunnstrom S. Motor testing procedures in hemiplegia: based on sequential recovery stages. Phys Ther 46: 357-375, 1966.
11. Burke RE. The use of state-dependent modulation of spinal reflexes as a tool to investigate the organization of spinal interneurons. Exp Brain Res 128: 263-277, 1999.
12. Burridge JH, Wood DE, Taylor PN, McLellan DL. Indices to describe different muscle activation patterns, identified during treadmill walking, in people with spastic drop-foot. Med Eng Phys 23: 427-434, 2001.
13. Canning CG, Ada L, O'Dwyer NJ. Abnormal muscle activation characteristics associated with loss of dexterity after stroke. J Neurol Sci 176: 45-56, 2000.
14. Carroll TJ, Baldwin ER, Collins DF, Zehr EP. Corticospinal excitability is lower during rhythmic arm movement than during tonic contraction. J Neurophysiol 95: 914-921, 2006.
15. Carroll TJ, Zehr EP, Collins DF. Modulation of cutaneous reflexes in human upper limb muscles during arm cycling is independent of activity in the contralateral arm. Exp Brain Res 161: 133-144, 2005.
16. Cauraugh JH, Lodha N, Naik SK, Summers JJ. Bilateral movement training and stroke motor recovery progress: a structured review and meta-analysis. Hum Move Sci 29: 853-870, 2010.
17. Cirstea MC, Levin MF. Compensatory strategies for reaching in stroke. Brain 123: 940-953, 2000.
18. Cramer SC, Sur M, Dobkin BH, O'Brien C, Sanger TD, Trojanowski JQ, Rumsey JM, Hicks R, Cameron J, Chen D, et al. Harnessing neuroplasticity for clinical applications. Brain 134: 1591-1609, 2011.
19. Diserens K, Perret N, Chatelain S, Bashir S, Ruegg D, Vuadens P, Vingerhoets F. The effect of repetitive arm cycling on post stroke spasticity and motor control: repetitive arm cycling and spasticity. J Neurol Sci 253: 18-24, 2007.
20. Dobkin BH. Rehabilitation after stroke. N Engl J Med 352: 1677-1684, 2005.
21. Dobkin BH, Firestine A, West M, Saremi K, Woods R. Ankle dorsiflexion as an fMRI paradigm to assay motor control for walking during rehabilitation. NeuroImage 23: 370-381, 2004.
22. Dragert K, Zehr EP. Rhythmic arm cycling modulates Hoffmann reflex excitability differentially in the ankle flexor and extensor muscles. Neurosci Lett 450: 235-238, 2009.
23. Duysens J. From cat to man: basic aspects of locomotion relevant to motor rehabilitation of SCI. Neurorehabilitation 10: 107-118, 1998.
24. Duysens J, Van de Crommert HW. Neural control of locomotion. Part 1: The central pattern generator from cats to humans. Gait Posture 7: 131-141, 1998.
25. Ferris DP, Huang HJ, Kao P-C. Moving the arms to activate the legs. Exerc Sport Sci Rev 34: 113-120, 2006.
26. Frigon A, Collins DF, Zehr EP. Effect of rhythmic arm movement on reflexes in the legs: modulation of soleus H-reflexes and somatosensory conditioning. J Neurophysiol 91: 1516-1523, 2004.
27. Grefkes C, Fink GR. Reorganization of cerebral networks after stroke: new insights from neuroimaging with connectivity approaches. Brain 134: 1264-1276, 2011.
28. Hage JJ, van der Steen LP, de Groot PJ. Difference in sensibility between the dominant and nondominant index finger as tested using the Semmes-Weinstein monofilaments pressure aesthesiometer. J Hand Surg Am 20: 227-229, 1995.
29. Haridas C, Zehr EP. Coordinated interlimb compensatory responses to electrical stimulation of cutaneous nerves in the hand and foot during walking. J Neurophysiol 90: 2850-2861, 2003.
30. Hundza S, Zehr E. Cutaneous reflexes during rhythmic arm cycling are insensitive to asymmetrical changes in crank length. Exp Brain Res 168: 165-177, 2006.
31. Hundza SR, Zehr EP. Suppression of soleus H-reflex amplitude is graded with frequency of rhythmic arm cycling. Exp Brain Res 193: 297-306, 2009.
32. Jankowska E, Hammar I. Spinal interneurones; how can studies in animals contribute to the understanding of spinal interneuronal systems in man? Brain Res Rev 40: 19-28, 2002.
33. Jones CA, Yang JF. Reflex behavior during walking in incomplete spinalcord-injured subjects. Exp Neurol 128: 239-248, 1994.
34. Kautz SA, Patten C. Interlimb influences on paretic leg function in poststroke hemiparesis. J Neurophysiol 93: 2460-2473, 2005.
35. Kautz SA, Patten C, Neptune RR. Does unilateral pedaling activate a rhythmic locomotor pattern in the nonpedaling leg in post-stroke hemiparesis? J Neurophysiol 95: 3154-3163, 2006.
36. Kim CM, Eng JJ. Magnitude and pattern of 3D kinematic and kinetic gait profiles in persons with stroke: relationship to walking speed. Gait Posture 20: 140-146, 2004.
37. Klimstra MD, Thomas E, Zehr PE. Biomechanical outcomes and neural correlates of cutaneous reflexes evoked during rhythmic arm cycling. J Biomech 44: 802-809, 2011.
38. Lewis GN, Byblow WD. Bimanual coordination dynamics in poststroke hemiparetics. J Mot Behav 36: 174-188, 2004a.
39. Lewis GN, Byblow WD. The effects of repetitive proprioceptive stimulation on corticomotor representation in intact and hemiplegic individuals. Clin Neurophysiol 115: 765-773, 2004b.
40. Lewis GN, Byblow WD. Neurophysiological and behavioural adaptations to a bilateral training intervention in individuals following stroke. Clin Rehabil 18: 48-59, 2004c.
41. Loadman PM, Zehr EP. Rhythmic arm cycling produces a non-specific signal that suppresses soleus H-reflex amplitude in stationary legs. Exp Brain Res 179: 199-208, 2007.
42. Luft A, McCombe-Waller S, Whitall J, Forrester L, Macko R, Sorkin J, Schulz J, Goldberg A, Hanley D. Repetitive bilateral arm training and motor cortex activation in chronic stroke: a randomized controlled trial. J Am Med Assoc 292: 1853-1861, 2004.
43. Matthews PBC. Observations on the automatic compensation of reflex gain on varying the pre-existing level of motor discharge in man. J Physiol 374: 73-90, 1986.
44. McCrea DA, Rybak IA. Organization of mammalian locomotor rhythm and pattern generation. Brain Res Rev 57: 134-146, 2008.
45. Mirbagheri MM, Alibiglou L, Thajchayapong M, Rymer WZ. Muscle and reflex changes with varying joint angle in hemiparetic stroke. J Neuroeng Rehabil 5: Art. 6, 2008.
46. Moseley AM, Stark A, Cameron ID, Pollock A. Treadmill training and body weight support for walking after stroke. Cochrane Database of Systematic Reviews 1: CD002840, 2005.
47. Olney SJ, Richards C. Hemiparetic gait following stroke. Part I: Characteristics. Gait Posture 4: 136-148, 2001.
48. Richards C, Olney SJ. Hemiparetic gait following stroke. Part II: Recovery and physical therapy. Gait Posture 4: 149-162, 2001.
49. Rymer WZ, Dewald J, Given PTJ, Beer R. Abnormal muscle synergies in hemiparetic stroke: origins and implications for movement control. In: Progress in Motor Control: Berstein's Traditions in Movement Studies, edited by Latash ML. Champaign, IL: Human Kinetics, 1998, vol. 1, p. 191-202.
50. Schindler-Ivens S, Brown DA, Brooke JD. Direction-dependent phasing of locomotor muscle activity is altered post-stroke. J Neurophysiol 92: 2207-2216, 2004.
51. Senesac CR, Davis S, Richards L. Generalization of a modified form of repetitive rhythmic bilateral training in stroke. Hum Move Sci 29: 137-148, 2010.
52. Shiavi R, Bugle HJ, Limbird T. Electromyographic gait assessment, Part 2: Preliminary assessment of hemiparetic synergy patterns. J Rehabil Res Dev 24: 24-30, 1987.
53. Stinear JW, Byblow WD. The contribution of cervical propriospinal premotoneurons in recovering hemiparetic stroke patients. J Clin Neurophysiol 21: 426-434, 2004a.
54. Stinear JW, Byblow WD. Modulation of human cervical premotoneurons during bilateral voluntary contraction of upper-limb muscles. Muscle Nerve 29: 506-514, 2004b.
55. Stinear JW, Byblow WD. Rhythmic bilateral movement training modulates corticomotor excitability and enhances upper limb motricity poststroke: a pilot study. J Clin Neurophysiol 21: 124-131, 2004c.
56. Thilmann AF, Fellows SJ, Garms E. Pathological stretch reflexes on the "good" side of hemiparetic patients. J Neurol Neurosurg Psychiatry 53: 208-214, 1990.
57. Whitall J, McCombe Waller S, Silver KH, Macko RF. Repetitive bilateral arm training with rhythmic auditory cueing improves motor function in chronic hemiparetic stroke. Stroke 31: 2390-2395, 2000.
58. Whitlock JA. Neurophysiology of spasticity. In: The Practical Management of Spasticity in Children and Adults, edited by Glen MB, Whyte J. Philadelphia: Lea & Febiger, 1990, p. 8-33.
59. Wolpaw JR. What can the spinal cord teach us about learning and memory? Neuroscientist 16: 532-549, 2010.
60. Zehr EP. Neural control of rhythmic human movement: the common core hypothesis. Exerc Sport Sci Rev 33: 54-60, 2005.
61. Zehr EP. Evidence-based risk assessment and recommendations for physical activity clearance: stroke and spinal cord injury. Appl Physiol Nutr Metab 36: S214-S231, 2011.
62. Zehr EP, Balter JE, Ferris DP, Hundza SR, Loadman PM, Stoloff RH. Neural regulation of rhythmic arm and leg movement is conserved across human locomotor tasks. J Physiol 582: 209-227, 2007a.
63. Zehr EP, Carroll TJ, Chua R, Collins DF, Frigon A, Haridas C, Hundza SR, Kido A. Possible contributions of spinal CPG activity to rhythmic human arm movement. Can J Physiol Pharmacol 82: 556-568, 2004a.
64. Zehr EP, Chua R. Modulation of human cutaneous reflexes during rhythmic cyclical arm movement. Exp Brain Res 135: 241-250, 2000.
65. Zehr EP, Collins DF, Chua R. Human interlimb reflexes evoked by electrical stimulation of cutaneous nerves innervating the hand and foot. Exp Brain Res 140: 495-504, 2001.
66. Zehr EP, Collins DF, Frigon A, Hoogenboom N. Neural control of rhythmic human arm movement: phase dependence and task modulation of Hoffmann reflexes in forearm muscles. J Neurophysiol 89: 12-21, 2003.
67. Zehr EP, Duysens J. Regulation of arm and leg movement during human locomotion. Neuroscientist 10: 347-361, 2004.
68. Zehr EP, Fujita K, Stein RB. Reflexes from the superficial peroneal nerve during walking in stroke subjects. J Neurophysiol 79: 848-858, 1998.
69. Zehr EP, Haridas C. Modulation of cutaneous reflexes in arm muscles during walking: further evidence of similar control mechanisms for rhythmic human arm and leg movements. Exp Brain Res 149: 260-266, 2003.
70. Zehr EP, Hoogenboom N, Frigon A, Collins DF. Facilitation of soleus H-reflex amplitude evoked by cutaneous nerve stimulation at the wrist is not suppressed by rhythmic arm movement. Exp Brain Res 159: 382-388, 2004b.
71. Zehr EP, Hundza SR. Forward and backward arm cycling are regulated by equivalent neural mechanisms. J Neurophysiol 93: 633-640, 2005.
72. Zehr EP, Hundza SR, Vasudevan EV. The quadrupedal nature of human bipedal locomotion. Exerc Sport Sci Rev 37: 102-108, 2009.
73. Zehr EP, Kido A. Neural control of rhythmic, cyclical human arm movement: task dependency, nerve specificity and phase modulation of cutaneous reflexes. J Physiol 537: 1033-1045, 2001.
74. Zehr EP, Klimstra M, Dragert K, Barzi Y, Bowden MG, Javan B, Phadke C. Enhancement of arm and leg locomotor coupling with augmented cutaneous feedback from the hand. J Neurophysiol 98: 1810-1814, 2007b.
75. Zehr EP, Loadman PM. Persistence of locomotor-related interlimb reflex networks during walking after stroke. Clin Neurophysiol 123: 96-807, 2012.