[Abstract+References] Upper Limb Coordination in Individuals With Stroke: Poorly Defined and Poorly Quantified.

Abstract

Background. The identification of deficits in interjoint coordination is important in order to better focus upper limb rehabilitative treatment after stroke. The majority of standardized clinical measures characterize endpoint performance, such as accuracy, speed, and smoothness, based on the assumption that endpoint performance reflects interjoint coordination, without measuring the underlying temporal and spatial sequences of joint recruitment directly. However, this assumption is questioned since improvements of endpoint performance can be achieved through different degrees of restitution or compensation of upper limb motor impairments based on the available kinematic redundancy of the system. Confusion about adequate measurement may stem from a lack a definition of interjoint coordination during reaching. Methods and Results. We suggest an operational definition of interjoint coordination during reaching as a goal-oriented process in which joint degrees of freedom are organized in both spatial and temporal domains such that the endpoint reaches a desired location in a context-dependent manner. Conclusions. In this point-of-view article, we consider how current approaches to laboratory and clinical measures of coordination comply with our definition. We propose future study directions and specific research strategies to develop clinical measures of interjoint coordination with better construct and content validity than those currently in use.

References

1.	Chen, SY, Winstein, CJ. A systematic review of voluntary arm recovery in hemiparetic stroke: critical predictors for meaningful outcomes using the international classification of functioning, disability, and health. J Neurol Phys Ther. 2009;33:2–13. Google Scholar, Crossref, Medline
2.	Stinear, CM, Byblow, WD. Predicting and accelerating motor recovery after stroke. Curr Opin Neurol. 2014;27:624–630. Google Scholar, Medline
3.	Jolkkonen, J, Kwakkel, G. Translational hurdles in stroke recovery studies. Transl Stroke Res. 2016;7:331–342. Google Scholar, Crossref, Medline
4.	Levin, MF, Kleim, JA, Wolf, SL. What do motor “recovery” and “compensation” mean in patients following stroke? Neurorehabil Neural Repair. 2009;23:313–319. Google Scholar, Link
5.	Schmidt, R, Lee, T. Motor Control and Learning— A Behavioral Emphasis. 5th ed. Champaign, IL: Human Kinetics; 2011. Google Scholar
6.	Brunnstrom, S. Movement Therapy in Hemiplegia: A Neurophysiological Approach. New York, NY: Harper & Row; 1970. Google Scholar
7.	Fugl-Meyer, AR, Jääskö, L, Leyman, I, Olsson, S, Steglind, S. The post-stroke hemiplegic patient 1. A method for evaluation of physical performance. Scand J Rehabil Med. 1975;7:13–31. Google Scholar, Medline
8.	Gowland, C, Stratford, P, Ward, M. Measuring physical impairment and disability with the Chedoke-McMaster Stroke Assessment. Stroke. 1993;24:58–63. Google Scholar, Crossref, Medline
9.	Latash, ML. Fundamentals of Motor Control. Oxford, England: Academic Press; 2012. Google Scholar
10.	Bernstein, NA. The Coordination and Regulation of Movements. Oxford, England: Pergamon Press; 1967. Google Scholar
11.	Levin, MF, Michaelsen, SM, Cirstea, CM, Roby-Brami, A. Use of the trunk for reaching targets placed within and beyond the reach in adult hemiparesis. Exp Brain Res. 2002;143:171–180. Google Scholar, Crossref, Medline
12.	Shaikh, T, Goussev, V, Feldman, AG, Levin, MF. Arm-trunk coordination for beyond-the-reach movements in adults with stroke. Neurorehabil Neural Repair. 2014;28:355–366. Google Scholar, Link
13.	Levin, MF. Interjoint coordination during pointing movements is disrupted in spastic hemiparesis. Brain. 1996;119:281–293. Google Scholar, Crossref, Medline
14.	van Kordelaar, J, van Wegen, EE, Nijland, RH, Daffertshofer, A, Kwakkel, G. Understanding adaptive motor control of the paretic upper limb early poststroke: the EXPLICIT-stroke program. Neurorehabil Neural Repair. 2013;27:854–863. Google Scholar, Link
15.	Levin, MF, Liebermann, DG, Parmet, Y, Berman, S. Compensatory versus noncompensatory shoulder movements used for reaching in stroke. Neurorehabil Neural Repair. 2016;30:635–646. Google Scholar, Link
16.	Reisman, DS, Scholz, JP. Aspects of joint coordination are preserved during pointing in persons with post-stroke hemiparesis. Brain. 2003;126(pt 11):2510–2527. Google Scholar, Crossref, Medline
17.	Cirstea, CM, Ptito, A, Levin, MF. Feedback and cognition in arm motor skill reacquisition after stroke. Stroke. 2006;37:1237–1242. Google Scholar, Crossref, Medline
18.	Chen, HL, Lin, KC, Liing, RJ, Wu, CY, Chen, CL. Kinematic measures of arm-trunk movements during unilateral and bilateral reaching predict clinically important change in perceived arm use in daily activities after intensive stroke rehabilitation. J Neuroeng Rehabil. 2015;12:84. Google Scholar, Crossref, Medline
19.	Wee, SK, Hughes, AM, Warner, M, Burridge, JH. Trunk restraint to promote upper extremity recovery in stroke patients: a systematic review and meta-analysis. Neurorehabil Neural Repair. 2014;28:660–677. Google Scholar, Link
20.	Higgins, J, Mayo, NE, Desrosiers, J, Salbach, NM, Ahmed, S. Upper-limb function and recovery in the acute phase poststroke. J Rehabil Res Dev. 2005;42:65–76. Google Scholar, Crossref, Medline
21.	Desrosiers, J, Bravo, G, Hébert, R, Dutil, E, Mercier, L. Validation of the Box and Block Test as a measure of dexterity of elderly people: reliability, validity, and norms studies. Arch Phys Med Rehabil. 1994;75:751–755. Google Scholar, Medline
22.	Rodrigues, MRM, Slimovitch, M, Blanchette, AK, Levin, MF. Temporal and spatial upper-limb interjoint coordination in chronic stroke subjects versus healthy individuals when reaching, American Society for Neurorehabilitation Annual Meeting, Chicago, IL. Neurorehabil Neural Repair. 2016;30:NP1–NP44. doi:10.1177/1545968315625245. Google Scholar, Crossref
23.	Johansson, GM, Grip, H, Levin, MF, Häger, CK. The added value of kinematic evaluation of the timed finger-to-nose test in persons post-stroke. J Neuroeng Rehabil. 2017;14:11. Google Scholar, Crossref, Medline
24.	Krasovsky, T, Levin, MF. Review: toward a better understanding of coordination in healthy and poststroke gait. Neurorehabil Neural Repair. 2010;24:213–224. Google Scholar, Link
25.	Rau, G, Disselhorst-Klug, C, Schmidt, R. Movement biomechanics goes upwards: from the leg to the arm. J Biomech. 2000;33:1207–1216. Google Scholar, Crossref, Medline
26.	Abend, W, Bizzi, E, Morasso, P. Human arm trajectory formation. Brain. 1982;105(pt 2):331–348. Google Scholar, Crossref, Medline
27.	Von Hofsten, C. Development of visually directed reaching: the approach phase. J Hum Mov Stud. 1979;5:160–178. Google Scholar
28.	Fagg, AH, Varto, AG, Houk, JC. Learning to reach via corrective movements. Paper presented at: Proceedings of the Tenth Yale Workshop on Adaptive and Learning Systems; June 10-12, 1988; New Haven, CT. http://www.gbv.de/dms/tib-ub-hannover/251755754.pdf. Accessed October 13, 2017. Google Scholar
29.	World Health Organization. International Classification of Functioning, Disability and Health. Geneva, Switzerland: World Health Organization; 2001. Google Scholar
30.	Krakauer, JW, Carmichael, ST, Corbett, D, Wittenberg, GF. Getting neurorehabilitation right: what can be learned from animal models? Neurorehabil Neural Repair. 2012;26:923–931. Google Scholar, Link
31.	Michaelsen, SM, Luta, A, Roby-Brami, A, Levin, MF. Effect of trunk restraint on the recovery of reaching movements in hemiparetic patients. Stroke. 2001;32:1875–1883. Google Scholar, Crossref, Medline
32.	Swaine, BR, Sullivan, SJ. Reliability of the scores for the finger-to-nose test in adults with traumatic brain injury. Phys Ther. 1993;73:71–78. Google Scholar, Crossref, Medline
33.	Gagnon, C, Mathieu, J, Desrosiers, J. Standardized finger-nose test validity for coordination assessment in an ataxic disorder. Can J Neurol Sci. 2004;31:484–489. Google Scholar, Crossref, Medline
34.	Nijland, R, van Wegen, E, Verbunt, J, van Wijk, R, van Kordelaar, J, Kwakkel, G. A comparison of two validated tests for upper limb function after stroke: the Wolf Motor Function Test and the Action Research Arm Test. J Rehabil Med. 2010;42:694–696. Google Scholar, Crossref, Medline
35.	Hsueh, IP, Hsu, MJ, Sheu, CF, Lee, S, Hsieh, CL, Lin, JH. Psychometric comparisons of 2 versions of the Fugl-Meyer Motor Scale and 2 versions of the Stroke Rehabilitation Assessment of Movement. Neurorehabil Neural Repair. 2008;22:737–744. Google Scholar, Link
36.	Daley, K, Mayo, N, Wood-Dauphinée, S. Reliability of scores on the Stroke Rehabilitation Assessment of Movement (STREAM) measure. Phys Ther. 1999;79:8–19. Google Scholar, Medline
37.	Hsueh, IP, Wang, CH, Sheu, CF, Hsieh, CL. Comparison of psychometric properties of three mobility measures for patients with stroke. Stroke. 2003;34:1741–1745. Google Scholar, Crossref, Medline
38.	van der Lee, JH, De Groot, V, Beckerman, H, Wagenaar, RC, Lankhorst, GJ, Bouter, LM. The intra- and interrater reliability of the action research arm test: a practical test of upper extremity function in patients with stroke. Arch Phys Med Rehabil. 2001;82:14–19. Google Scholar, Crossref, Medline
39.	Platz, T, Pinkowski, C, van Wijck, F, Kim, IH, di Bella, P, Johnson, G. Reliability and validity of arm function assessment with standardized guidelines for the Fugl-Meyer Test, Action Research Arm Test and Box and Block Test: a multicentre study. Clin Rehabil. 2005;19:404–411. Google Scholar, Link
40.	Van de Winckel, A, Feys, H, van der Knaap, S. Can quality of movement be measured? Rasch analysis and inter-rater reliability of the Motor Evaluation Scale for upper extremity in stroke patients (MESUPES). Clin Rehabil. 2006;20:871–884. Google Scholar, Link
41.	Johansson, GM, Häger, CK. Measurement properties of the Motor Evaluation Scale for upper extremity in stroke patients (MESUPES). Disabil Rehabil. 2012;34:288–294. Google Scholar, Crossref, Medline
42.	Mathiowetz, V, Volland, G, Kashman, N, Weber, K. Adult norms for the Box and Block Test of manual dexterity. Am J Occup Ther. 1985;39:386–391. Google Scholar, Crossref, Medline
43.	Heller, A, Wade, DT, Wood, VA, Sunderland, A, Hewer, RL, Ward, E. Arm function after stroke: measurement and recovery over the first three months. J Neurol Neurosurg Psychiatry. 1987;50:714–719. Google Scholar, Crossref, Medline
44.	Parker, VM, Wade, DT, Langton Hewer, R. Loss of arm function after stroke: measurement, frequency, and recovery. Int Rehabil Med. 1986;8:69–73. Google Scholar, Crossref, Medline
45.	Morris, DM, Uswatte, G, Crago, JE, Cook, EW, Taub, E. The reliability of the Wolf Motor Function Test for assessing upper extremity function after stroke. Arch Phys Med Rehabil. 2001;82:750–755. Google Scholar, Crossref, Medline
46.	Whitall, J, Savin, DN, Harris-Love, M, Waller, SM. Psychometric properties of a modified Wolf Motor Function Test for people with mild and moderate upper-extremity hemiparesis. Arch Phys Med Rehabil. 2006;87:656–660. Google Scholar, Crossref, Medline
47.	Levin, MF, Desrosiers, J, Beauchemin, D, Bergeron, N, Rochette, A. Development and validation of a scale for rating motor compensations used for reaching in patients with hemiparesis: the Reaching Performance Scale. Phys Ther. 2004;84:8–22. Google Scholar, Medline
48.	Miyamoto, S, Kondo, T, Suzukamo, Y, Michimata, A, Izumi, S. Reliability and validity of the Manual Function Test in patients with stroke. Am J Phys Med Rehabil. 2009;88:247–255. Google Scholar, Crossref, Medline
49.	Kurtaiş, Y, Küçükdeveci, A, Elhan, A. Psychometric properties of the Rivermead Motor Assessment: its utility in stroke. J Rehabil Med. 2009;41:1055–1061. Google Scholar, Crossref, Medline
50.	Collin, C, Wade, D. Assessing motor impairment after stroke: a pilot reliability study. J Neurol Neurosurg Psychiatry. 1990;53:576–579. Google Scholar, Crossref, Medline
51.	Kopp, B, Kunkel, A, Flor, H. The Arm Motor Ability Test: reliability, validity, and sensitivity to change of an instrument for assessing disabilities in activities of daily living. Arch Phys Med Rehabil. 1997;78:615–620. Google Scholar, Crossref, Medline
52.	O’Dell, MW, Kim, G, Rivera, L. A psychometric evaluation of the Arm Motor Ability Test. J Rehabil Med. 2013;45:519–527. Google Scholar, Crossref, Medline
53.	Chae, J, Labatia, I, Yang, G. Upper limb motor function in hemiparesis: concurrent validity of the Arm Motor Ability Test. Am J Phys Med Rehabil. 2003;82:1–8. Google Scholar, Crossref, Medline
54.	Wagner, JM, Rhodes, JA, Patten, C. Reproducibility and minimal detectable change of three-dimensional kinematic analysis of reaching tasks in people with hemiparesis after stroke. Phys Ther. 2008;88:652–663. Google Scholar, Crossref, Medline
55.	Alt Murphy, M, Willén, C, Sunnerhagen, KS. Kinematic variables quantifying upper-extremity performance after stroke during reaching and drinking from a glass. Neurorehabil Neural Repair. 2011;25:71–80. Google Scholar, Link
56.	Silfies, SP, Bhattacharya, A, Biely, S, Smith, SS, Giszter, S. Trunk control during standing reach: a dynamical system analysis of movement strategies in patients with mechanical low back pain. Gait Posture. 2009;29:370–376. Google Scholar, Crossref, Medline
57.	Cirstea, MC, Mitnitski, AB, Feldman, AG, Levin, MF. Interjoint coordination dynamics during reaching in stroke. Exp Brain Res. 2003;151:289–300. Google Scholar, Crossref, Medline
58.	Petrarca, M, Zanelli, G, Patanè, F, Frascarelli, F, Cappa, P, Castelli, E. Reach-to-grasp interjoint coordination for moving object in children with hemiplegia. J Rehabil Med. 2009;41:995–1000. Google Scholar, Crossref, Medline
59.	Merdler, T, Liebermann, DG, Levin, MF, Berman, S. Arm-plane representation of shoulder compensation during pointing movements in patients with stroke. J Electromyogr Kinesiol. 2013;23:938–947. Google Scholar, Crossref, Medline
60.	Reisman, DS, Scholz, JP. Workspace location influences joint coordination during reaching in post-stroke hemiparesis. Exp Brain Res. 2006;170:265–276. Google Scholar, Crossref, Medline
61.	Park, J, Lewis, MM, Huang, X, Latash, ML. Dopaminergic modulation of motor coordination in Parkinson’s disease. Parkinsonism Relat Disord. 2014;20:64–68. Google Scholar, Crossref, Medline
62.	Steenbergen, B, vanThiel, E, Hulstijn, W, Meulenbroek, RGJ. The coordination of reaching and grasping in spastic hemiparesis. Hum Mov Sci. 2000;19:75–105. Google Scholar, Crossref
63.	Kelso, JA. Phase transitions and critical behavior in human bimanual coordination. Am J Physiol. 1984;246(6 pt 2):R1000–R1004. Google Scholar, Medline
64.	van de Winckel, A, Feys, H. Effects of walking velocity on relative phase dynamics in the trunk in human walking. J Biomech. 1996;29:1175–1184. Google Scholar, Crossref, Medline
65.	Kaminski, TR, Bock, C, Gentile, AM. The coordination between trunk and arm motion during pointing movements. Exp Brain Res. 1995;106:457–466. Google Scholar, Crossref, Medline
66.	Kukke, SN, Curatalo, LA, de Campos, AC, Hallett, M, Alter, KE, Damiano, DL. Coordination of reach-to-grasp kinematics in individuals with childhood-onset dystonia due to hemiplegic cerebral palsy. IEEE Trans Neural Syst Rehabil Eng. 2016;24:582–590. Google Scholar, Crossref, Medline
67.	Jaspers, E, Desloovere, K, Bruyninckx, H. Three-dimensional upper limb movement characteristics in children with hemiplegic cerebral palsy and typically developing children. Res Dev Disabil. 2011;32:2283–2294. Google Scholar, Crossref, Medline
68.	Newell, KM, Vaillancourt, DE. Dimensional change in motor learning. Hum Mov Sci. 2001;20:695–715. Google Scholar, Crossref, Medline
69.	Berret, B, Bonnetblanc, F, Papaxanthis, C, Pozzo, T. Modular control of pointing beyond arm’s length. J Neurosci. 2009;29:191–205. Google Scholar, Crossref, Medline
70.	Tagliabue, M, Ferrigno, G, Horak, F. Effects of Parkinson’s disease on proprioceptive control of posture and reaching while standing. Neuroscience. 2009;158:1206–1214. Google Scholar, Crossref, Medline
71.	Daffertshofer, A, Lamoth, CJ, Meijer, OG, Beek, PJ. PCA in studying coordination and variability: a tutorial. Clin Biomech (Bristol, Avon). 2004;19:415–428. Google Scholar, Crossref, Medline
72.	Ivanenko, YP, Cappellini, G, Dominici, N, Poppele, RE, Lacquaniti, F. Modular control of limb movements during human locomotion. J Neurosci. 2007;27:11149–1161. Google Scholar, Crossref, Medline
73.	Cheron, G, Bengoetxea, A, Bouillot, E, Lacquaniti, F, Dan, B. Early emergence of temporal co-ordination of lower limb segments elevation angles in human locomotion. Neurosci Lett. 2001;308:123–127. Google Scholar, Crossref, Medline
74.	Degelean, M, De Borre, L, Salvia, P. Effect of ankle-foot orthoses on trunk sway and lower limb intersegmental coordination in children with bilateral cerebral palsy. J Pediatr Rehabil Med. 2012;5:171–179. Google Scholar, Medline
75.	Ivanenko, YP, d’Avella, A, Poppele, RE, Lacquaniti, F. On the origin of planar covariation of elevation angles during human locomotion. J Neurophysiol. 2008;99:1890–1898. Google Scholar, Crossref, Medline
76.	Wang, X. Three-dimensional kinematic analysis of influence of hand orientation and joint limits on the control of arm postures and movements. Biol Cybern. 1999;80:449–463. Google Scholar, Crossref, Medline
77.	Scholz, JP, Schöner, G. The uncontrolled manifold concept: identifying control variables for a functional task. Exp Brain Res. 1999;126:289–306. Google Scholar, Crossref, Medline
78.	Latash, ML, Scholz, JP, Schöner, G. Toward a new theory of motor synergies. Motor Control. 2007;11:276–308. Google Scholar, Crossref, Medline
79.	Knorr, B, Hughes, R, Sherrill, D, Stein, J, Akay, M, Bonato, P. Quantitative measures of functional upper limb movement in persons after stroke. Paper presented at: Conference Proceedings. 2nd International IEEE EMBS Conference on Neural Engineering, 2005; March 16-19, 2005; Arlington, VA. http://ieeexplore.ieee.org/document/1419604. Accessed October 13, 2017. Google Scholar
80.	Archambault, P, Pigeon, P, Feldman, AG, Levin, MF. Recruitment and sequencing of different degrees of freedom during pointing movements involving the trunk in healthy and hemiparetic subjects. Exp Brain Res. 1999;126:55–67. Google Scholar, Crossref, Medline
81.	Sveistrup, H. Motor rehabilitation using virtual reality. J Neuroeng Rehabil. 2004;1:10. Google Scholar, Crossref, Medline
82.	Tao, G, Archambault, PS, Levin, MF. Evaluation of Kinect skeletal tracking in a virtual reality rehabilitation system for upper limb hemiparesis. Presented at: The 2013 International Conference on Virtual Rehabilitation (ICVR); August 26-19, 2013; Philadelphia, PA. http://ieeexplore.ieee.org/document/6662084/. Accessed October 13, 2017. Google Scholar
83.	Liebermann, DG, Berman, S, Weiss, PL, Levin, MF. Kinematics of reaching movements in a 2-D virtual environment in adults with and without stroke. IEEE Trans Neural Syst Rehabil Eng. 2012;20:778–787. Google Scholar, Crossref, Medline

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