Normal and Impaired Cooperative Hand Movements: Role of Neural Coupling

Chapter
First Online:

Abstract

Recent research indicates that a task-specific, interhemispheric neural coupling is involved in the control of cooperative hand movements required for activities of daily living. This neural coupling is manifested in bilateral electromyographic reflex responses in the arm muscles to unilateral arm nerve stimulation. In addition, fMRI recordings show a bilateral task-specific activation and functional coupling of the secondary somatosensory cortical areas (S2) during the cooperative, but not during bimanual control tasks. This activation is suggested to reflect processing of shared cutaneous input during the cooperative task in both cortical areas. In chronic poststroke patients, arm nerve stimulation of the unaffected arm also leads to bilateral electromyographic responses, similar to those seen in healthy subjects in the cooperative task. However, stimulation of the affected side is frequently followed only by ipsilateral responses. The presence/absence of contralateral electromyographic responses correlates with the clinical motor impairment measured by the Fugl-Meyer score. The observations suggest impaired processing of afferent input from the affected side leading to defective neural coupling during cooperative hand movements after stroke. In moderately affected patients, movement execution seems to rely on the involvement of the ipsilateral corticospinal tract arising in the non-damaged hemisphere. According to these results, hand rehabilitation of stroke patients, currently focused on reach and grasp movements of the affected side, should be supplemented with the training of cooperative hand movements required during activities of daily living.

Keywords

Stroke Hand function Rehabilitation Neural limb coupling Reflex activity fMRI recordings 
This is a preview of subscription content, log in to check access.

References

  1. 1.
    Jenny AB. Commissural projections of the cortical hand motor area in monkeys. J Comp Neurol. 1979;188(1):137–45.CrossRefPubMedGoogle Scholar
  2. 2.
    Rouiller EM, Babalian A, Kazennikov O, Moret V, Yu XH, et al. Transcallosal connections of the distal forelimb representations of the primary and supplementary motor cortical areas in macaque monkeys. Exp Brain Res. 1994;102(2):227–43.CrossRefPubMedGoogle Scholar
  3. 3.
    Donchin O, Gribova A, Steinberg O, Bergman H, Vaadia E. Primary motor cortex is involved in bimanual coordination. Nature. 1998;395(6699):274–8.CrossRefPubMedGoogle Scholar
  4. 4.
    Kermadi I, Liu Y, Tempini A, Calciati E, Rouiller EM. Neuronal activity in the primate supplementary motor area and the primary motor cortex in relation to spatio-temporal bimanual coordination. Somatosens Mot Res. 1998;15(4):287–308.CrossRefPubMedGoogle Scholar
  5. 5.
    Tanji J, Okano K, Sato KC. Relation of neurons in the nonprimary motor cortex to bilateral hand movement. Nature. 1987;327(6123):618–20.CrossRefPubMedGoogle Scholar
  6. 6.
    Theorin A, Johansson RS. Selection of prime actor in humans during bimanual object manipulation. J Neurosci. 2010;30(31):10448–59.CrossRefPubMedGoogle Scholar
  7. 7.
    Debaere F, Swinnen SP, Beatse E, Sunaert S, Van Hecke P, et al. Brain areas involved in interlimb coordination: a distributed network. Neuroimage. 2001;14:947–58.CrossRefPubMedGoogle Scholar
  8. 8.
    Kazennikov O, Hyland B, Corboz M, Babalian A, Rouiller EM, et al. Neural activity of supplementary and primary motor areas in monkeys and its relation to bimanual and unimanual movement sequences. Neuroscience. 1999;89:661–74.CrossRefPubMedGoogle Scholar
  9. 9.
    Kermadi I, Liu Y, Rouiller EM. Do bimanual motor actions involve the dorsal premotor (PMd), cingulate (CMA) and posterior parietal (PPC) cortices? Comparison with primary and supplementary motor cortical areas. Somatosens Mot Res. 2000;17(3):255–71.CrossRefPubMedGoogle Scholar
  10. 10.
    Stephan KM, Binkofski F, Halsband U, Dohle C, Wunderlich G, et al. The role of ventral medial wall motor areas in bimanual co-ordination. A combined lesion and activation study. Brain. 1999;122(Pt 2):351–68.CrossRefPubMedGoogle Scholar
  11. 11.
    Swinnen SP. Intermanual coordination: from behavioural principles to neural-network interactions. Nat Rev Neurosci. 2002;3:348–59.CrossRefPubMedGoogle Scholar
  12. 12.
    Wiesendanger M, Serrien DJ. The quest to understand bimanual coordination. Prog Brain Res. 2004;143:491–505.CrossRefPubMedGoogle Scholar
  13. 13.
    Liuzzi G, Horniss V, Zimerman M, Gerloff C, Hummel FC. Coordination of uncoupled bimanual movements by strictly timed interhemispheric connectivity. J Neurosci. 2011;31(25):9111–7.CrossRefPubMedGoogle Scholar
  14. 14.
    Ohki Y, Johansson RS. Sensorimotor interactions between pairs of fingers in bimanual and unimanual manipulative tasks. Exp Brain Res. 1999;127(1):43–53.CrossRefPubMedGoogle Scholar
  15. 15.
    White O, Dowling N, Bracewell RM, Diedrichsen J. Hand interactions in rapid grip force adjustments are independent of object dynamics. J Neurophysiol. 2008;100:2738–45.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Lum PS, Reinkensmeyer DJ, Lehman SL. A Bimanual reflex during two hand grasp. Conference proceedings IEEE, Med Biol Soc, San Diego, 1993. p. 1163–4.Google Scholar
  17. 17.
    Obhi SS. Bimanual coordination: an unbalanced field of research. Motor Control. 2004;8(2):111–20.PubMedGoogle Scholar
  18. 18.
    Dietz V, Macauda G, Schrafl-Altermatt M, Wirz M, Kloter E, et al. Neural coupling of cooperative hand movements: a reflex and FMRI study. Cereb Cortex. 2015;25(4):948–58.CrossRefPubMedGoogle Scholar
  19. 19.
    Datta AK, Harrison LM, Stephens JA. Task-dependent changes in the size of response to magnetic brain stimulation in human first dorsal interosseous muscle. J Physiol. 1989;418:13–23.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Zehr EP, Kido A. Neural control of rhythmic, cyclical human arm movement: task dependency, nerve specificity and phase modulation of cutaneous reflexes. J Physiol. 2001;537(Pt 3):1033–45.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Michel J, van Hedel HJ, Dietz V. Obstacle stepping involves spinal anticipatory activity associated with quadrupedal limb coordination. Eur J Neurosci. 2008;27(7):1867–75.CrossRefPubMedGoogle Scholar
  22. 22.
    Dietz V, Fouad K, Bastiaanse CM. Neuronal coordination of arm and leg movements during human locomotion. Eur J Neurosci. 2001;14(11):1906–14.CrossRefPubMedGoogle Scholar
  23. 23.
    Disbrow E, Roberts T, Poeppel D, Krubitzer L. Evidence for interhemispheric processing of inputs from the hands in human S2 and PV. J Neurophysiol. 2001;85(5):2236–44.PubMedGoogle Scholar
  24. 24.
    Whitsel BL, Petrucelli LM, Werner G. Symmetry and connectivity in the map of the body surface in somatosensory area II of primates. J Neurophysiol. 1969;32(2):170–83.PubMedGoogle Scholar
  25. 25.
    Lin YY, Forss N. Functional characterization of human second somatosensory cortex by magnetoencephalography. Behav Brain Res. 2002;135(1–2):141–5.CrossRefPubMedGoogle Scholar
  26. 26.
    Hari R, Hanninen R, Makinen T, Jousmaki V, Forss N, et al. Three hands: fragmentation of human bodily awareness. Neurosci Lett. 1998;240(3):131–4.CrossRefPubMedGoogle Scholar
  27. 27.
    Schrafl-Altermatt M, Dietz V. Task-specific role of ipsilateral pathways: somatosensory evoked potentials during cooperative hand movements. Neuroreport. 2014;25(18):1429–32.CrossRefPubMedGoogle Scholar
  28. 28.
    Massion J, Ioffe M, Schmitz C, Viallet F, Gantcheva R. Acquisition of anticipatory postural adjustments in a bimanual load-lifting task: normal and pathological aspects. Exp Brain Res. 1999;128(1–2):229–35.CrossRefPubMedGoogle Scholar
  29. 29.
    Torre K, Hammami N, Metrot J, van Dokkum L, Coroian F, et al. Somatosensory-related limitations for bimanual coordination after stroke. Neurorehabil Neural Repair. 2013;27(6):507–15.CrossRefPubMedGoogle Scholar
  30. 30.
    Schrafl-Altermatt M, Dietz V. Cooperative hand movements in stroke patients: neural reorganization. Under revision. 2016.Google Scholar
  31. 31.
    Lemon RN. Descending pathways in motor control. Annu Rev Neurosci. 2008;31:195–218.CrossRefPubMedGoogle Scholar
  32. 32.
    Kloter E, Wirz M, Dietz V. Locomotion in stroke subjects: interactions between unaffected and affected sides. Brain. 2011;134(Pt 3):721–31.CrossRefPubMedGoogle Scholar
  33. 33.
    Edgerton VR, Tillakaratne NJ, Bigbee AJ, de Leon RD, Roy RR. Plasticity of the spinal neural circuitry after injury. Annu Rev Neurosci. 2004;27:145–67.CrossRefPubMedGoogle Scholar
  34. 34.
    Bradnam LV, Stinear CM, Byblow WD. Theta burst stimulation of human primary motor cortex degrades selective muscle activation in the ipsilateral arm. J Neurophysiol. 2010;104(5):2594–602.CrossRefPubMedGoogle Scholar
  35. 35.
    Howatson G, Taylor MB, Rider P, Motawar BR, McNally MP, et al. Ipsilateral motor cortical responses to TMS during lengthening and shortening of the contralateral wrist flexors. Eur J Neurosci. 2011;33(5):978–90.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Baker SN. The primate reticulospinal tract, hand function and functional recovery. J Physiol. 2011;589(Pt 23):5603–12.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Edwards JD, Meehan SK, Linsdell MA, Borich MR, Anbarani K, et al. Changes in thresholds for intracortical excitability in chronic stroke: more than just altered intracortical inhibition. Restor Neurol Neurosci. 2013;31:693.PubMedGoogle Scholar
  38. 38.
    Teasell R, Bayona NA, Bitensky J. Plasticity and reorganization of the brain post stroke. Top Stroke Rehabil. 2005;12(3):11–26.CrossRefPubMedGoogle Scholar
  39. 39.
    Schaefer SY, Haaland KY, Sainburg RL. Ipsilesional motor deficits following stroke reflect hemispheric specializations for movement control. Brain. 2007;130(Pt 8):2146–58.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Taub E, Uswatte G, Mark VW, Morris DM. The learned nonuse phenomenon: implications for rehabilitation. Eura Medicophys. 2006;42:241–56.PubMedGoogle Scholar
  41. 41.
    Taub E, Uswatte G, Pidikiti R. Constraint-induced movement therapy: a new family of techniques with broad application to physical rehabilitation – a clinical review. J Rehabil Res Dev. 1999;36(3):237–51.PubMedGoogle Scholar
  42. 42.
    Stoykov ME, Lewis GN, Corcos DM. Comparison of bilateral and unilateral training for upper extremity hemiparesis in stroke. Neurorehabil Neural Repair. 2009;23:945–53.CrossRefPubMedGoogle Scholar
  43. 43.
    van Delden AL, Peper CL, Beek PJ, Kwakkel G. Match and mismatch between objective and subjective improvements in upper limb function after stroke. Disabil Rehabil. 2013;35(23):1961–7.CrossRefPubMedGoogle Scholar
  44. 44.
    Lin KC, Chen YA, Chen CL, Wu CY, Chang YF. The effects of bilateral arm training on motor control and functional performance in chronic stroke: a randomized controlled study. Neurorehabil Neural Repair. 2010;24(1):42–51.CrossRefPubMedGoogle Scholar
  45. 45.
    Mudie MH, Matyas TA. Can simultaneous bilateral movement involve the undamaged hemisphere in reconstruction of neural networks damaged by stroke? Disabil Rehabil. 2000;22(1–2):23–37.CrossRefPubMedGoogle Scholar
  46. 46.
    Jung R, Dietz V. Delayed initiation of voluntary movements after pyramidal lesions in man (author’s transl). Arch Psychiatr Nervenkr. 1975 Dec 31;221(2):87–109.Google Scholar
  47. 47.
    Carr LJ, Harrison LM, Evans AL, Stephens JA. Patterns of central motor reorganization in hemiplegic cerebral palsy. Brain. 1993;116(Pt 5):1223–47.CrossRefPubMedGoogle Scholar
  48. 48.
    Mayston MJ, Harrison LM, Stephens JA. A neurophysiological study of mirror movements in adults and children. Ann Neurol. 1999;45(5):583–94.CrossRefPubMedGoogle Scholar
  49. 49.
    Buma F, Kwakkel G, Ramsey N. Understanding upper limb recovery after stroke. Restor Neurol Neurosci. 2013;31(6):707–22.PubMedGoogle Scholar
  50. 50.
    Schrafl-Altermatt M, Dietz V. Effect of cooperative hand movement training in post-stroke subjects: a single case study. Under review. 2016.Google Scholar
  51. 51.
    Sleimen-Malkoun R, Temprado JJ, Berton E. A dynamic systems approach to bimanual coordination in stroke: implications for rehabilitation and research. Medicina. 2010;46(6):374–81.PubMedGoogle Scholar
  52. 52.
    Laffont I, Bakhti K, Coroian F, van Dokkum L, Mottet D, et al. Innovative technologies applied to sensorimotor rehabilitation after stroke. Ann Phys Rehabil Med. 2014;57(8):543–51.CrossRefPubMedGoogle Scholar
  53. 53.
    Lum PS, Burgar CG, Shor PC, Majmundar M, Van der Loos M. Robot-assisted movement training compared with conventional therapy techniques for the rehabilitation of upper-limb motor function after stroke. Arch Phys Med Rehabil. 2002;83:952–9.CrossRefPubMedGoogle Scholar
  54. 54.
    Klamroth-Marganska V, Blanco J, Campen K, Curt A, Dietz V, et al. Three-dimensional, task-specific robot therapy of the arm after stroke: a multicentre, parallel-group randomised trial. Lancet Neurol. 2014;13(2):159–66.CrossRefPubMedGoogle Scholar
  55. 55.
    Sale P, Lombardi V, Franceschini M. Hand robotics rehabilitation: feasibility and preliminary results of a robotic treatment in patients with hemiparesis. Stroke Res Treat. 2012;2012:820931.PubMedPubMedCentralGoogle Scholar
  56. 56.
    Guidali M, Duschau-Wicke A, Broggi S, Klamroth-Marganska V, Nef T, et al. A robotic system to train activities of daily living in a virtual environment. Med Biol Eng Comput. 2011;49(10):1213–23.CrossRefPubMedGoogle Scholar
  57. 57.
    Ang KK, Chua KS, Phua KS, Wang C, Chin ZY, et al. A Randomized controlled trial of EEG-based motor imagery brain-computer interface robotic rehabilitation for stroke. Clin EEG Neurosci. 2015;46(4):310–20.Google Scholar
  58. 58.
    Formaggio E, Storti SF, Boscolo Galazzo I, Gandolfi M, Geroin C, et al. Modulation of event-related desynchronization in robot-assisted hand performance: brain oscillatory changes in active, passive and imagined movements. J Neuroeng Rehabil. 2013;10:24.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Lum PS, Burgar CG, Shor PC. Evidence for improved muscle activation patterns after retraining of reaching movements with the MIME robotic system in subjects with post-stroke hemiparesis. IEEE Trans Neural Syst Rehabil Eng. 2004;12(2):186–94.CrossRefPubMedGoogle Scholar
  60. 60.
    Basteris A, Nijenhuis SM, Stienen AH, Buurke JH, Prange GB, et al. Training modalities in robot-mediated upper limb rehabilitation in stroke: a framework for classification based on a systematic review. J Neuroeng Rehabil. 2014;11:111.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing 2016

Authors and Affiliations

  1. 1.Spinal Cord Injury CenterBalgrist University HospitalZurichSwitzerland

Personalised recommendations