Advertisement

Experimental Brain Research

, Volume 237, Issue 12, pp 3391–3408 | Cite as

Effects of arm weight support on neuromuscular activation during reaching in chronic stroke patients

  • Keith D. Runnalls
  • Pablo Ortega-Auriol
  • Angus J. C. McMorland
  • Greg Anson
  • Winston D. ByblowEmail author
Research Article

Abstract

To better understand how arm weight support (WS) can be used to alleviate upper limb impairment after stroke, we investigated the effects of WS on muscle activity, muscle synergy expression, and corticomotor excitability (CME) in 13 chronic stroke patients and 6 age-similar healthy controls. For patients, lesion location and corticospinal tract integrity were assessed using magnetic resonance imaging. Upper limb impairment was assessed using the Fugl-Meyer upper extremity assessment with patients categorised as either mild or moderate–severe. Three levels of WS were examined: low = 0, medium = 50 and high = 100% of full support. Surface EMG was recorded from 8 upper limb muscles, and muscle synergies were decomposed using non-negative matrix factorisation from data obtained during reaching movements to an array of 14 targets using the paretic or dominant arm. Interactions between impairment level and WS were found for the number of targets hit, and EMG measures. Overall, greater WS resulted in lower EMG levels, although the degree of modulation between WS levels was less for patients with moderate–severe compared to mild impairment. Healthy controls expressed more synergies than patients with moderate–severe impairment. Healthy controls and patients with mild impairment showed more synergies with high compared to low weight support. Transcranial magnetic stimulation was used to elicit motor-evoked potentials (MEPs) to which stimulus–response curves were fitted as a measure of corticomotor excitability (CME). The effect of WS on CME varied between muscles and across impairment level. These preliminary findings demonstrate that WS has direct and indirect effects on muscle activity, synergies, and CME and warrants further study in order to reduce upper limb impairment after stroke.

Keywords

Human Stroke Upper limb Muscle synergy Reaching Transcranial magnetic stimulation 

Notes

Acknowledgements

The authors acknowledge assistance provided by April Ren, Terry Corin, Fiona Doolan, and support from Saebo Inc. for supplying the SaeboMAS. WB received funding from the Health Research Council of New Zealand (Grant No. 14/136).

Supplementary material

221_2019_5687_MOESM1_ESM.docx (16 kb)
Supplementary material 1 (DOCX 16 kb)
221_2019_5687_MOESM2_ESM.pdf (1.9 mb)
Supplementary Fig. 1 Anatomical T1-weighted images in the transverse plane at the level of the lesion for each patient. Patient numbers correspond with Table 1 (PDF 1958 kb)

References

  1. Andersson JLR, Sotiropoulos SN (2016) An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging. Neuroimage 125:1063–1078PubMedPubMedCentralGoogle Scholar
  2. Bates D, Mächler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48Google Scholar
  3. Beer RF, Dewald JPA, Dawson ML, Rymer WZ (2004) Target-dependent differences between free and constrained arm movements in chronic hemiparesis. Exp Brain Res 156:458–470PubMedGoogle Scholar
  4. Beer RF, Ellis MD, Holubar BG, Dewald JPA (2007) Impact of gravity loading on post-stroke reaching and its relationship to weakness. Muscle Nerve 36:242–250PubMedPubMedCentralGoogle Scholar
  5. Bizzi E, Cheung VCK (2013) The neural origin of muscle synergies. Front Comput Neurosci 7:1–6Google Scholar
  6. Bradnam LV, Stinear CM, Barber PA, Byblow WD (2012) Contralesional hemisphere control of the proximal paretic upper limb following stroke. Cereb Cortex 22:2662–2671PubMedGoogle Scholar
  7. Cheung VCK, Piron L, Agostini M, Silvoni S, Turolla A, Bizzi E (2009) Stability of muscle synergies for voluntary actions after cortical stroke in humans. Proc Natl Acad Sci USA 106:19563–19568PubMedGoogle Scholar
  8. Cheung VCK, Turolla A, Agostini M, Silvoni S, Bennis C, Kasi P, Paganoni S, Bonato P, Bizzi E (2012) Muscle synergy patterns as physiological markers of motor cortical damage. Proc Natl Acad Sci USA 109:14652–14656PubMedGoogle Scholar
  9. 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 103:844–857PubMedGoogle Scholar
  10. Coscia M, Cheung VCK, Tropea P, Koenig A, Monaco V, Bennis C, Micera S, Bonato P (2014) The effect of arm weight support on upper limb muscle synergies during reaching movements. J NeuroEng Rehabil 11:1–15Google Scholar
  11. Cramer SC, Nelles G, Benson RR, Kaplan JD, Parker RA, Kwong KK, Kennedy DN, Finklestein SP, Rosen BR (1997) A functional MRI study of subjects recovered from hemiparetic stroke. Stroke 28:2518–2527PubMedGoogle Scholar
  12. Devanne H, Lavoie BA, Capaday C (1997) Input-output properties and gain changes in the human corticospinal pathway. Exp Brain Res 114:329–338PubMedGoogle Scholar
  13. Devanne H, Cohen LG, Kouchtir-Devanne N, Capaday C (2002) Integrated motor cortical control of task-related muscles during pointing in humans. J Neurophysiol 87:3006–3017PubMedGoogle Scholar
  14. Devanne H, Cassim F, Ethier C, Brizzi L, Thevenon A, Capaday C (2006) The comparable size and overlapping nature of upper limb distal and proximal muscle representations in the human motor cortex. Eur J Neurosci 23:2467–2476PubMedGoogle Scholar
  15. Dewald JPA, Beer RF (2001) Abnormal joint torque patterns in the paretic upper limb of subjects with hemiparesis. Muscle Nerve 24:273–283PubMedGoogle Scholar
  16. Dominici F, Popa T, Ginanneschi F, Mazzocchio R, Rossi A (2005) Cortico-motoneuronal output to intrinsic hand muscles is differentially influenced by static changes in shoulder positions. Exp Brain Res 164:500–504PubMedGoogle Scholar
  17. Ellis MD, Schut I, Dewald JPA (2017) Flexion synergy overshadows flexor spasticity during reaching in chronic moderate to severe hemiparetic stroke. Clin Neurophysiol 128(7):1308–1314PubMedPubMedCentralGoogle Scholar
  18. Ellis MD, Carmona C, Drogos J, Dewald JPA (2018) Progressive abduction loading therapy with horizontal-plane viscous resistance targeting weakness and flexion synergy to treat upper limb function in chronic hemiparetic stroke: a randomized clinical trial. Front Neurol 9:71PubMedPubMedCentralGoogle Scholar
  19. Feigin VL, Barker-Collo S, Parag V, Senior H, Lawes CMM, Ratnasabapathy Y, Glen E, ASTRO study group (2010) Auckland Stroke Outcomes Study. Part 1: gender, stroke types, ethnicity, and functional outcomes 5 years poststroke. Neurology 75:1597–1607PubMedGoogle Scholar
  20. Flanders M, Herrmann U (1992) Two components of muscle activation: scaling with the speed of arm movement. J Neurophysiol 67:931–943PubMedGoogle Scholar
  21. Fox J, Weisberg S (2010) An R companion to applied regression, 2nd edn. SAGE, Thousand OaksGoogle Scholar
  22. Fridman EA, Hanakawa T, Chung M, Hummel F, Leiguarda RC, Cohen LG (2004) Reorganization of the human ipsilesional premotor cortex after stroke. Brain 127:747–758PubMedPubMedCentralGoogle Scholar
  23. Frost SB, Barbay S, Friel KM, Plautz EJ, Nudo RJ (2003) Reorganization of remote cortical regions after ischemic brain injury: a potential substrate for stroke recovery. J Neurophysiol 89:3205–3214PubMedGoogle Scholar
  24. Ginanneschi F, Santo F, Dominici F, Gelli F, Mazzocchio R, Rossi A (2005) Changes in corticomotor excitability of hand muscles in relation to static shoulder positions. Exp Brain Res 161:374–382PubMedGoogle Scholar
  25. Ginanneschi F, Dominici F, Biasella A, Gelli F, Rossi A (2006) Changes in corticomotor excitability of forearm muscles in relation to static shoulder positions. Brain Res 1073–1074:332–338PubMedGoogle Scholar
  26. Grefkes C, Fink GR (2011) Reorganization of cerebral networks after stroke: new insights from neuroimaging with connectivity approaches. Brain 134:1264–1276PubMedPubMedCentralGoogle Scholar
  27. Herbert WJ, Powell K, Buford JA (2015) Evidence for a role of the reticulospinal system in recovery of skilled reaching after cortical stroke: initial results from a model of ischemic cortical injury. Exp Brain Res 233(11):3231–3251PubMedGoogle Scholar
  28. Israely S, Leisman G, Machluf CC, Carmeli E (2018) Muscle synergies control during hand-reaching tasks in multiple directions post-stroke. Front Comput Neurosci 12:10PubMedPubMedCentralGoogle Scholar
  29. Jenkinson M, Smith S (2001) A global optimisation method for robust affine registration of brain images. Med Image Anal 5:143–156PubMedGoogle Scholar
  30. Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17:825–841PubMedPubMedCentralGoogle Scholar
  31. Jenkinson M, Beckmann CF, Behrens TEJ, Woolrich MW, Smith SM (2012) FSL. Neuroimage 62:782–790PubMedGoogle Scholar
  32. Johansen-Berg H, Rushworth MFS, Bogdanovic MD, Kischka U, Wimalaratna S, Matthews PM (2002) The role of ipsilateral premotor cortex in hand movement after stroke. Proc Natl Acad Sci USA 99:14518–14523PubMedGoogle Scholar
  33. Johnson MJ (2006) Recent trends in robot-assisted therapy environments to improve real-life functional performance after stroke. J NeuroEng Rehabil 3:29PubMedPubMedCentralGoogle Scholar
  34. Kantak SS, Wittenberg GF, Liao W-W, Magder LS, Rogers MW, Waller SM (2013) Posture-related modulations in motor cortical excitability of the proximal and distal arm muscles. Neurosci Lett 533:65–70PubMedGoogle Scholar
  35. Karbasforoushan H, Cohen-Adad J, Dewald JPA (2019) Brainstem and spinal cord MRI identifies altered sensorimotor pathways post-stroke. Nat Commun 10(1):3524PubMedPubMedCentralGoogle Scholar
  36. Kieliba P, Tropea P, Pirondini E, Coscia M, Micera S, Artoni F (2018) How are muscle synergies affected by electromyography pre-processing? IEEE Trans Neural Syst Rehabil Eng 26:882–893PubMedGoogle Scholar
  37. Krabben T, Prange GB, Molier BI, Stienen AHA, Jannink MJA, Buurke JH, Rietman JS (2011) Influence of gravity compensation training on synergistic movement patterns of the upper extremity after stroke, a pilot study. J NeuroEng Rehabil 9:44Google Scholar
  38. Kwakkel G, Meskers CGM (2014) Effects of robotic therapy of the arm after stroke. Lancet Neurol 13:132–133PubMedGoogle Scholar
  39. Kwakkel G, Wagenaar RC, Kollen BJ, Lankhorst GJ (1996) Predicting disability in stroke—a critical review of the literature. Age Ageing 25:479–489PubMedGoogle Scholar
  40. Kwakkel G, van Peppen R, Wagenaar RC, Wood Dauphinee S, Richards C, Ashburn A, Miller K, Lincoln N, Partridge C, Wellwood I, Langhorne P (2004) Effects of augmented exercise therapy time after stroke: a meta-analysis. Stroke 35:2529–2539PubMedGoogle Scholar
  41. Lan Y, Yao J, Dewald JPA (2017) The impact of shoulder abduction loading on volitional hand opening and grasping in chronic hemiparetic stroke. NNR 31(6):521–529Google Scholar
  42. Lang CE, Macdonald JR, Reisman DS, Boyd L, Jacobson Kimberley T, Schindler-Ivens SM, Hornby TG, Ross SA, Scheets PL (2009) Observation of amounts of movement practice provided during stroke rehabilitation. Arch Phys Med Rehabil 90:1692–1698PubMedPubMedCentralGoogle Scholar
  43. Loureiro RCV, Harwin WS, Nagai K, Johnson M (2011) Advances in upper limb stroke rehabilitation: a technology push. Med Biol Eng Comput 49:1103–1118PubMedGoogle Scholar
  44. Luo D, Ganesh S, Koolaard J (2014) Predictmeans: calculate predicted means for linear models. http://cran.r-project.org/web/packages/predictmeans/index.html. Accessed 1 Dec 2016
  45. MATLAB (2016). Version 9.1 (R2016b) In: The Mathworks Inc, Natick, MassachusettsGoogle Scholar
  46. McKiernan BJ, Marcario JK, Karrer JH, Cheney PD (1998) Corticomotoneuronal postspike effects in shoulder, elbow, wrist, digit, and intrinsic hand muscles during a reach and prehension task. J Neurophysiol 80:1961–1980PubMedGoogle Scholar
  47. McMorland AJC, Runnalls KD, Byblow WD (2015) A neuroanatomical framework for upper limb synergies after stroke. Front Hum Neurosci 9:305Google Scholar
  48. McPherson JG, Chen A, Ellis MD, Yao J, Heckman CJ, Dewald JPA (2018a) Progressive recruitment of contralesional cortico-reticulospinal pathways drives motor impairment post stroke. J Physiol 596(7):1211–1225PubMedPubMedCentralGoogle Scholar
  49. McPherson JG, Ellis MD, Harden RN, Carmona C, Heckman CJ, Dewald JPA (2018b) Neuromodulatory inputs to motoneurons contribute to the loss of independent joint control in chronic moderate to severe hemiparetic stroke. Front Neurol 9:470PubMedPubMedCentralGoogle Scholar
  50. Meijer R, Ihnenfeldt DS, de Groot IJM, van Limbeek J, Vermeulen M, de Haan RJ (2003) Prognostic factors for ambulation and activities of daily living in the subacute phase after stroke. A systematic review of the literature. Clin Rehabil 17:119–129PubMedGoogle Scholar
  51. Mendis S (2013) Stroke disability and rehabilitation of stroke: world Health Organization perspective. Int J Stroke 8:3–4PubMedGoogle Scholar
  52. Miller LC, Dewald JPA (2012) Involuntary paretic wrist/finger flexion forces and EMG increase with shoulder abduction load in individuals with chronic stroke. Clin Neurophysiol 123(6):1216–1225PubMedPubMedCentralGoogle Scholar
  53. Ortega-Auriol PA, Besier TF, Byblow WD, McMorland AJC (2018) Fatigue influences the recruitment, but not structure, of muscle synergies. Front Hum Neurosci 12:217.   https://doi.org/10.3389/fnhum.2018.00217 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Park H-S, Jun C-H (2009) A simple and fast algorithm for K-medoids clustering. Expert Syst Appl 36:3336–3341Google Scholar
  55. Patel AT, Duncan PW, Lai SM, Studenski S (2000) The relation between impairments and functional outcomes poststroke. Arch Phys Med Rehabil 81:1357–1363PubMedGoogle Scholar
  56. Pauvert V, Pierrot-Deseilligny E, Rothwell JC (1998) Role of spinal premotoneurones in mediating corticospinal input to forearm motoneurones in man. J Physiol (Lond) 508(Pt 1):301–312Google Scholar
  57. Pierrot-Deseilligny E (2002) Propriospinal transmission of part of the corticospinal excitation in humans. Muscle Nerve 26:155–172PubMedGoogle Scholar
  58. Prange GB, Jannink MJA, Stienen AHA, van der Kooij H, IJzerman MJ, Hermens HJ (2009a) Influence of gravity compensation on muscle activation patterns during different temporal phases of arm movements of stroke patients. NNR 23:478–485Google Scholar
  59. Prange GB, Kallenberg LAC, Jannink MJA, Stienen AHA, van der Kooij H, IJzerman MJ, Hermens HJ (2009b) Influence of gravity compensation on muscle activity during reach and retrieval in healthy elderly. J Electromyogr Kinesiol 19:e40–e49PubMedGoogle Scholar
  60. Roh J, Rymer WZ, Beer RF (2012) Robustness of muscle synergies underlying three-dimensional force generation at the hand in healthy humans. J Neurophysiol 107:2123–2142PubMedPubMedCentralGoogle Scholar
  61. Roh J, Rymer WZ, Perreault EJ, Yoo SB, Beer RF (2013) Alterations in upper limb muscle synergy structure in chronic stroke survivors. J Neurophysiol 109:768–781PubMedGoogle Scholar
  62. Roh J, Rymer WZ, Beer RF (2015) Evidence for altered upper extremity muscle synergies in chronic stroke survivors with mild and moderate impairment. Front Hum Neurosci 9:6PubMedPubMedCentralGoogle Scholar
  63. Runnalls KD, Anson G, Wolf SL, Byblow WD (2014) Partial weight support differentially affects corticomotor excitability across muscles of the upper limb. Physiol Rep 2:e12183PubMedPubMedCentralGoogle Scholar
  64. Runnalls KD, Anson G, Byblow WD (2015) Partial weight support of the arm affects corticomotor selectivity of biceps brachii. J NeuroEng Rehabil 12:1–10Google Scholar
  65. Runnalls KD, Anson G, Byblow WD (2017) Posture interacts with arm weight support to modulate corticomotor excitability to the upper limb. Exp Brain Res 235:97–107PubMedGoogle Scholar
  66. Sabatini AM (2002) Identification of neuromuscular synergies in natural upper-arm movements. Biol Cybern 86:253–262PubMedGoogle Scholar
  67. Sanes JN, Donoghue JP, Thangaraj V, Edelman RR, Warach S (1995) Shared neural substrates controlling hand movements in human motor cortex. Science 268:1775–1777PubMedGoogle Scholar
  68. Smith SM (2002) Fast robust automated brain extraction. Hum Brain Mapp 17:143–155PubMedGoogle Scholar
  69. Stinear CM, Barber PA, Smale PR, Coxon JP, Fleming MK, Byblow WD (2007) Functional potential in chronic stroke patients depends on corticospinal tract integrity. Brain 130:170–180PubMedGoogle Scholar
  70. Sukal TM, Ellis MD, Dewald JPA (2007) Shoulder abduction-induced reductions in reaching work area following hemiparetic stroke: neuroscientific implications. Exp Brain Res 183:215–223PubMedPubMedCentralGoogle Scholar
  71. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R-project.org/. Accessed 1 Dec 2016
  72. Turton A, Wroe S, Trepte N, Fraser C, Lemon RN (1996) Contralateral and ipsilateral EMG responses to transcranial magnetic stimulation during recovery of arm and hand function after stroke. Electroencephalogr Clin Neurophysiol 101:316–328PubMedGoogle Scholar
  73. Veerbeek JM, Kwakkel G, van Wegen EEH, Ket JCF, Heymans MW (2011) Early prediction of outcome of activities of daily living after stroke: a systematic review. Stroke 42:1482–1488PubMedGoogle Scholar
  74. Veerbeek JM, van Wegen E, van Peppen R, van der Wees PJ, Hendriks E, Rietberg M, Kwakkel G (2014) What is the evidence for physical therapy poststroke? a systematic review and meta-analysis. PLoS One 9:e87987-33Google Scholar
  75. Ward NS, Newton JM, Swayne OBC, Lee L, Thompson AJ, Greenwood RJ, Rothwell JC, Frackowiak RSJ (2006) Motor system activation after subcortical stroke depends on corticospinal system integrity. Brain 129:809–819PubMedPubMedCentralGoogle Scholar
  76. Welham S, Cullis B, Gogel B, Gilmour A, Thompson R (2004) Prediction in linear mixed models. Aust NZ J Stat 46:325–347Google Scholar
  77. Yao J, Dewald JPA (2018) The increase in overlap of cortical activity preceding static elbow/shoulder motor tasks is associated with limb synergies in severe stroke. NNR 32(6–7):624–634Google Scholar
  78. Zaaimi B, Edgley SA, Soteropoulos DS, Baker SN (2012) Changes in descending motor pathway connectivity after corticospinal tract lesion in macaque monkey. Brain 135(7):2277–2289PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Movement Neuroscience Laboratory, Department of Exercise SciencesUniversity of AucklandAucklandNew Zealand
  2. 2.Centre for Brain Research, University of AucklandAucklandNew Zealand
  3. 3.Auckland Bioengineering Institute, University of AucklandAucklandNew Zealand

Personalised recommendations