Impairment in Task-Specific Modulation of Muscle Coordination Correlates with the Severity of Hand Impairment following Stroke

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Lee, Sang Wook ^a,b   Triandafilou, Kristen ^c   Lock, Blair A ^c   Kamper, Derek G ^c,d  

^a Catholic University of America   (United States)

^b NATIONAL REHABILITATION HOSPITAL   (United States)

^c REHABILITATION INSTITUTE OF CHICAGO   (United States)

^d Illinois Institute of Technology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGED; ARTICLE; CEREBROVASCULAR ACCIDENT; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; ELECTROMYOGRAPHY; FEMALE; FUNCTIONAL STATUS; HAND DISEASE; HAND FUNCTION; HAND MUSCLE; HUMAN; MALE; MOTOR COORDINATION; MOTOR PERFORMANCE; MUSCLE DISEASE; MUSCLE EXCITATION; MUSCLE ISOMETRIC CONTRACTION; NEUROMODULATION; SURVIVOR; TASK PERFORMANCE; WRIST MUSCLE;

ADULT; AGED; AGED, 80 AND OVER; ELECTROMYOGRAPHY; FEMALE; HAND; HUMANS; MALE; MIDDLE AGED; MODELS, THEORETICAL; MUSCLE CONTRACTION; MUSCLE, SKELETAL; STROKE;

EID: 84880501019     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068745     Document Type: Article

References (93)

1. Roger VL, Go AS, Lloyd-Jones DM, Benjamin EJ, Berry JD, et al. (2012) Heart disease and stroke statistics-2012 update: a report from the American Heart Association. Circulation 125; e2- e220.
2. Trombly CA (1989) Stroke. In: Trombly CA, Ed Occupational therapy for physical dysfunction. Baltimore, MD: Williams and Wilkins: 454-71.
3. Bohannon RW, Smith MB, (1987) Assessment of strength deficits in eight paretic upper extremity muscle groups of stroke patients with hemiplegia. Phys Ther 67: 522-525.
4. Cruz EG, Waldinger HC, Kamper DG, (2005) Kinetic and kinematic workspace of the index finger following stroke. Brain 128: 1112-1121.
5. Triandafilou K, Fischer HC, Towles JD, Kamper DG, Rymer WZ, (2011) Diminished capacity to modulate motor activation patterns according to task contributes to thumb deficits following stroke. J Neurophysiol 106: 1644-1651.
6. Sukai TM, Ellis MD, Dewald JPA, (2007) Shoulder abduction-induced reductions in reaching work area following hemiparetic stroke: neuroscientific implications. Exp Brain Res 183: 215-223.
7. Beebe JA, Lang CE, (2009) Active range of motion predicts upper extremity function 3 months after stroke. Stroke 40: 1772-1779.
8. Kamper DG, Cruz EG, Siegel MP, (2003) Stereotypical fingertip trajectories during grasp, J Neurophysiol. 90: 3702-3710.
9. Beer RF, Dewald JPA, Dawson ML, Rymer WZ, (2004) Target-dependent differences between free and constrained arm movements in chronic hemiparesis. Exp Brain Res 156: 458-470.
10. Seo NJ, Rymer WZ, Kamper DG, (2010) Altered digit force direction during pinch grip following stroke, Exp Brain Res. 202: 891-901.
11. O'Dwyer NJ, Ada L, Neilson PD, (1996) Spasticity and muscle contracture following stroke, Brain. 119: 1737-1749.
12. Given JD, Dewald JPA, Rymer WZ, (1995) Joint dependent passive stiffness in paretic and contralateral limbs of spastic patients with hemiparetic stroke. J Neurol Neurosurg Psychiatry 59: 271-279.
13. Dattola R, Girlanda P, Vita G, Santoro M, Roberto ML, et al. (1993) Muscle Rearrangement in Patients with Hemiparesis after Stroke: An Electrophysiological and Morphological Study, Eur Neurol. 33: 109-114.
14. McPherson JG, Ellis MD, Heckman CJ, Dewald JPA, (2008) Evidence for increased activation of persistent inward currents in individuals with chronic hemiparetic stroke, J Neurophysiol. 100: 3236-324.
15. Lance JW (1980) Symposium synopsis. In: Feldman RG, Young RR, Koella WP, Eds. Spasticity: disordered motor control. Miami: Symposia Specialists: 485-94.
16. Schmit BD, Dewald JPA, Rymer WZ, (2000) Stretch reflex adaptation in elbow flexors during repeated passive movements in unilateral brain-injured patients. Arch Phys Med Rehabil 81: 269-278.
17. Sommerfeld DK, Eek EU, Svensson AK, Holmqvist LW, von Arbin MH, (2004) Spasticity after stroke: its occurrence and association with motor impairments and activity limitations, Stroke. 35: 134-139.
18. Canning CG, Ada L, O'Dwyer NJ, (2000) Abnormal muscle activation characteristics associated with loss of dexterity after stroke. J Neurol Sci 176: 45-56.
19. Kamper DG, Rymer WZ, (2001) Impairment of voluntary control of finger motion following stroke: role of inappropriate muscle coactivation. Muscle Nerve 24: 673-681.
20. Seo NJ, Rymer WZ, Kamper DG, (2009) Delays in Grip Initiation and Termination in Persons with Stroke: Effects of Arm Support and Active Muscle Stretch Exercise, J Neurophysiol. 101: 3108-3115.
21. Gemperline JJ, Allen S, Walk D, Rymer WZ, (1995) Characteristics of motor unit discharge in subjects with hemiparesis, Muscle Nerve. 18: 1101-1114.
22. Zhou P, Suresh NL, Rymer WZ, (2007) Model based sensitivity analysis of EMG- force relation with respect to motor unit properties: applications to muscle paresis in stroke, Ann Biomed Eng. 35: 1521-1531.
23. Gowland C, deBruin H, Basmajian JV, Plews N, Burcea I, (1992) Agonist and antagonist activity during voluntary upper-limb movement in patients with stroke, Phys Ther. 72: 624-633.
24. Patten C, Lexell J, Brown HE, (2004) Weakness and strength training in persons with poststroke hemiplegia: Rationale, method, and efficacy, J Rehabil Res Dev. 41: 293-312.
25. Klein CS, Brooks D, Richardson D, McIlroy WE, Bayley MT, (2010) Voluntary activation failure contributes more to plantar flexor weakness than antagonist coactivation and muscle atrophy in chronic stroke survivors, J App Physiol. 109: 1337-1346.
26. Brunnstrom S (1970) Movement therapy in hemiplegia: a neurophysiological approach. New York: Harper and Row.
27. Beer RF, Given JD, Dewald JP, (1999) Task-dependent weakness at the elbow in patients with hemiparesis, Arch Phys Med Rehabil. 80: 766-772.
28. Cirstea MC, Levin MF, (2000) Compensatory strategies for reaching in stroke, Brain. 123: 940-953.
29. Dewald JPA, Sheshadri V, Dawson ML, Beer RF, (2001) Upper limb discoordination in hemiparetic stroke: implication for neurorehabilitation, Top Stroke Rehabil. 8: 1-12.
30. Lum PS, Burgar CG, Shor PC, (2003) Evidence for strength imbalances as a significant contributor to abnormal synergies in hemiparetic subjects, Muscle Nerve. 27: 211-221.
31. Ellis MD, Holubar BG, Acosta AM, Beer RF, Dewald JPA, (2005) Modifiability of abnormal isometric elbow and shoulder joint torque coupling after stroke, Muscle Nerve. 32: 170-178.
32. Welmer AK, Holmqvist LW, Sommerfeld DK, (2006) Hemiplegic limb synergies in stroke patients, Am J Phys Med Rehabil. 85: 112-119.
33. Dipietro L, Krebs HI, Fasoli SE, Volpe BT, Stein J, et al. (2007) Changing motor synergies in chronic stroke, J Neurophysiol. 98: 757-768.
34. Dewald JPA, Pope PS, Given JD, Buchanan TS, Rymer WZ, (1995) Abnormal muscle coactivation patterns during isometric torque generation at the elbow and shoulder in hemiparetic subjects, Brain. 118: 495-510.
35. Iwamuro BT, Cruz EG, Connelly LL, Fischer HC, Kamper DG, (2008) Effect of a gravity-compensating orthosis on reaching after stroke: evaluation of the therapy assistant WREX, Arch Phys Med Rehabil. 89: 2121-2128.
36. Schieber MH, Santello M, (2004) Hand function: peripheral and central constraints on performance. J App Physiol 96: 2293-2300.
37. An KN, Chao EY, Cooney WP, Linscheid RL, (1985) Forces in the normal and abnormal hand, J Orthop Res. 3: 202-211.
38. Cole KJ, Abbs JH, (1986) Coordination of three-joint digit movements for rapid finger-thumb grasp, J Neurophysiol. 55: 1407-1423.
39. Dennerlein JT, Diao E, Mote CD Jr, Rempel DM, (1998) Tensions of the flexor digitorum superficialis are higher than a current model predicts, J Biomech. 31: 295-301.
40. Valero-Cuevas FJ, Zajac FE, Burgar CG, (1998) Large index-fingertip forces are produced by subject-independent patterns of muscle excitation, J Biomech. 31: 693-703.
41. Lee SW, Chen H, Towles JD, Kamper DG, (2008) Estimation of the effective static moment arms of the tendons in the index finger extensor mechanism, J Biomech. 41: 1467-1573.
42. Napier JR, (1956) The prehensile movements of the human hand, J Bone Joint Surg. 38B: 902-913.
43. Elliot JM, Connolly KJ, (1984) A classification of manipulative hand movements, Dev Med Child Neurol. 26: 283-296.
44. Maier MA, Hepp-Reymond MC, (1995) EMG activation patterns during force production in precision grip. I. Contribution of 15 finger muscles to isometric force, Exp Brain Res 103: 108-122.
45. Valero-Cuevas FJ, (2000) Predictive modulation of muscle coordination pattern magnitude scales fingertip force magnitude over the voluntary range, J Neurophysiol. 83: 1469-1479.
46. Kutch JJ, Kuo AD, Bloch AM, Rymer WZ, (2008) Endpoint force fluctuations reveal flexible rather than synergistic patterns of muscle cooperation, J Neurophysiol. 100: 2455-2471.
47. Rearick MP, Casares A, Santello M, (2003) Task-dependent modulation of multi-digit force coordination patterns, J Neurophysiol. 89: 1317-26.
48. Weiss EJ, Flanders M, (2004) Muscular and postural synergies of the human hand, J Neurophysiol. 92: 523-535.
49. Raghavan P, Krakauer JW, Gordon AM, (2006) Impaired anticipatory control of fingertip forces in patients with a pure motor or sensorimotor lacunar syndrome, Brain. 129: 1415-1425.
50. Takahashi CD, Reinkensmeyer DJ, (2003) Hemiparetic stroke impairs anticipatory control of arm movement, Exp Brain Res. 149: 131-140.
51. Raghavan P, Santello M, Gorden AM, Krakauer JW, (2010) Compensatory motor control after stroke: an alternative joint strategy for object-dependent shaping of hand posture, J Neurophysiol. 103: 3034-3043.
52. Holdefer RN, Miller LE, (2002) Primary motor cortical neurons encode functional muscle synergies, Exp Brain Res. 146: 233-243.
53. Clark DJ, Ting LH, Zajac FE, Neptune RR, Kautz SA, (2010) Merging of healthy motor modules predicts reduced locomotor performance and muscle coordination complexity post-stroke, J Neurophysiol. 103: 844-857.
54. Cheung VCK, Piron L, Agostin M, Silvoni S, Turolla A, et al. (2009) Stability of muscle synergies for voluntary actions after cortical stroke in humans, PNAS. 106: 19563-19568.
55. Cheung VCK, Turolla A, Agostini M, Silvoni S, Bennis C, et al. (2012) Muscle synergy patterns as physiological markers of motor cortical damage, PNAS. 109: 14652-14656.
56. Roh J, Rymer WZ, Perreault EJ, Yoo SB, Beer RF, (2012) Alterations in upper limb muscle synergy structure in chronic stroke survivors, J Neurophysiol. 109: 768-781.
57. Roh J, Rymer WZ, Beer BF, (2012) Robustness of muscle synergies underlying three-dimensional force generation at the hand in healthy humans, J Neurophysiol. 107: 2123-2142.
58. Gowland CA (1990) Staging motor impairment after stroke, Stroke 21 (suppl. II): 19-21.
59. Johnston JA, Bobichb LR, Santello M, (2010) Coordination of intrinsic and extrinsic hand muscle activity as a function of wrist joint angle during two-digit grasping, Neurosci Letters. 474: 104-108.
60. Lindeman RH, Merenda PF, Gold RZ (1979) Introduction to Bivariate and Multivariate Analyses, Scott Foresman & Co, Glenview, IL.
61. Lee SW, Wilson K, Lock BA, Kamper DG, (2011) Subject-specific myoelectric pattern classification for stroke survivors, IEEE Trans Neural Syst Rehabil Eng. 19: 558-566.
62. Tresch MC, Saltiel P, Bizzi E, (1999) The construction of movement by the spinal cord, Nat Neurosci. 2: 162-167.
63. Ting LH, Macpherson JM, (2005) A limited set of muscle synergies for force control during a postural task, J Neurophysiol. 93: 609-613.
64. d'Avella A, Bizzi E, (2004) Shared and specific muscle synergies in natural motor behaviors, Proc Natl Acad Sci USA. 102: 3076-3081.
65. Torres-Oviedo G, Ting LH, (2007) Muscle synergies characterizing human postural responses, J Neurophysiol. 98: 2144-2156.
66. Lee DD, Seung HS, (1999) Learning the parts of objects by non-negative matrix factorization, Nature. 401: 276-308.
67. Bowden MG, Clark DJ, Kautz SA, (2010) Evaluation of abnormal synergy patterns poststroke: relationship of the Fugl-Meyer assessment to hemiparetic locomotion, Neurorehabil Neural Repair. 24: 328-337.
68. Frere J, Hug F, (2012) Between-subject variability of muscle synergies during a complex motor skill, Front Comput Neurosci. 6: 99.
69. Zajac FE, Neptune RR, Kautz SA, (2002) Biomechanics and muscle coordination of human walking. Part I: Introduction to concepts, power transfer, dynamics and simulations, Gait Posture 16: 215-232.
70. Traversa R, Cicinelli P, Bassi A, Rossini PM, Bernardi G, (1997) Mapping of motor cortical reorganization after stroke. A brain stimulation study with focal magnetic pulses, Stroke 28: 110-117.
71. Lang CE, Schieber MH, (2004) Reduced muscle selectivity during individuated finger movements in humans after damage to the motor cortex or corticospinal tract, J Neurophysiol. 91: 1722-1733.
72. Baker SN (2011) The primate reticulospinal tract, hand function and functional recovery, J Physiol 589; 5603-5612.
73. Valero-Cuevas FJ, Venkadesan M, Todorov E, (2009) Structured variability of muscle activations supports the minimum intervention principle of motor control, J Neurophysiol. 102: 59-68.
74. Scholz JP, Schoner G, (1999) The uncontrolled manifold concept: identifying control variables for a functional task, Exp Brain Res. 126: 289-306.
75. Kamper DG, Rymer WZ, (2000) Quantitative features of the stretch response of extrinsic finger muscles in hemiparetic stroke, Muscle Nerve. 23: 954-961.
76. Patten C, Srisethnil J, Asakawa D, Wright GA, Gold G (2002) Imaging activation impairment in post-stroke hemiparesis, Proc Intl Soc Magn Reson Med 10th Annu Meet, Honolulu, HI.
77. Hoffmann G, Kamper DG, Kahn JH, Rymer WZ, Schmit BD, (2009) Modulation of stretch reflexes of the finger flexors by sensory feedback from the proximal upper limb poststroke, J Neurophysiol. 102: 1420-1429.
78. Galganski ME, Fuglevand AJ, Enoka RM, (1993) Reduced control of motor output in a human hand muscle of elderly subjects during submaximal contractions. J Neurophysiol 69: 2108-2115.
79. Spiegel KM, Stratton J, Burke JR, Glendinning DS, Enoka RM, (1996) The influence of age on the assessment ofz motor unit activation in a human hand muscle, Exp Physiol. 81: 805-819.
80. Laidlaw DH, Bilodeau M, Enoka RM, (2000) Steadiness is reduced and motor unit discharge is more variable in old adults. Muscle Nerve 23: 600-612.
81. Ranganathan VK, Siemionow V, Sahgal V, Yue GH, (2001) Effects of aging on hand function, J Am Geriatr Soc. 49: 1478-1484.
82. Burnett RA, Laidlaw DH, Enoka RM, (2000) Coactivation of the antagonist muscle does not covary with steadiness in old adults, J Appl Physiol. 89: 61-71.
83. Jesunathadas M, Marmon AR, Gibb JM, Enoka RM, (2010) Recruitment and derecruitment characteristics of motor units in a hand muscle of young and old adults, J Appl Physiol. 108: 1659-1667.
84. Johnston JA, Bobichb LR, Santello M, (2010) Coordination of intrinsic and extrinsic hand muscle activity as a function of wrist joint angle during two-digit grasping, Neurosci Letters. 474: 104-108.
85. Lawrence DG, Kuypers HG, (1968) The functional organization of the motor system in the monkey, II. The effects of lesions of the descending brain-stem pathways, Brain 91: 15-36.
86. Bourbonnais D, Vanden Noven S, Carey KM, Rymer WZ, (1989) Abnormal spatial patterns of elbow muscle activation in hemiparetic human subject, Brain. 112: 85-102.
87. Conrad MO, Kamper DG, Lee SW (2011) Common cortical drive to hand muscles altered following stroke, Society for Neuroscience Annual Meeting, Washington, DC.
88. Ellis MD, Acosta AM, Yao J, Dewald JPA, (2007) Position-dependent torque coupling and associated muscle activation in the hemiparetic upper extremity, Exp Brain Res. 176: 594-602.
89. Schwerin S, Dewald JPA, Haztl M, Jovanovich S, Nickeas M, et al. (2008) Ipsilateral versus contralateral cortical motor projections to a shoulder adductor in chronic hemiparetic stroke: implications for the expression of arm synergies, Exp Brain Res 185; 509-519.
90. Davidson AG, Bufford JA, (2006) Bilateral actions of the reticulospinal tract on arm and shoulder muscles in the monkey: stimulus triggered averaging, Exp Brain Res. 173: 25-39.
91. Reinkensmeyer DJ, Cole AM, Kahn LE, Kamper DG, (2002) Directional control of reaching is preserved following mild/moderate stroke and stochastically constrained following severe stroke, Exp Brain Res. 143: 525-530.
92. Seo NJ, Fischer HW, Bogey RO, Rymer WZ, Kamper DG, (2011) Use of visual force feedback to improve digit force direction during pinch grip in persons with stroke: A pilot study, Arch Phys Med Rehabil. 92: 24-30.
93. Shah PK, Gerasimenko Y, Shyu A, Lavrov I, Zhong H, et al. (2012) Variability in step training enhances locomotor recovery after a spinal cord injury. Eur J Neurosci 36: 2054-2062.