Advertisement

Experimental Brain Research

, Volume 236, Issue 5, pp 1263–1272 | Cite as

A “matched” sensory reference can guide goal-directed movements of the affected hand in central post-stroke sensory ataxia

  • Michihiro OsumiEmail author
  • Masahiko Sumitani
  • Yuko Otake
  • Shu Morioka
Research Article

Abstract

Patients with central post-stroke sensory ataxia (CPSA) suffer from not only somatosensory dysfunction but also the ataxic movement disorder of the affected limb. These sensory and motor impairments possibly interfere each other, but such interference is still unclear. We evaluated smoothness of grasp movements in CPSA patients using a kinematic analysis, and verified the effect of somatosensory reference from the intact hand on grasp movements. Eight CPSA patients were enrolled. We recorded their reach-and-pinch movements of both affected and intact hands toward the tip of the 3-cm-diameter vertical bar, using a three-dimensional measurement system. When executing these movements of one hand, the patients simultaneously pinched the same diameter bar as the goal tip (matched-reference condition: Matched-Ref) or the 5-cm-diameter thicker bar (mismatched-reference condition: Mismatched-Ref) by the other hand. The normalized jerk index (i.e., movement smoothness) of the affected hand was disturbed compared with the intact hand. The kinematic data of the finger opening and closing phases were also disturbed. These disturbances were partially improved with Matched-Ref but not Mismatched-Ref of the intact hand. We successfully evaluated the features of CPSA, indicating that the somatosensory reference method could be useful for rehabilitation in sensory ataxia.

Keywords

Sensory ataxia Motor control Bimanual coupling 

Notes

Acknowledgements

This study was supported by a grant from JSPS KAKENHI Grant numbers 17K13080 and 17H05915.

Compliance with ethical standards

Conflicts of interest

The authors have no conflicts of interest to declare.

References

  1. Bogousslavsky J, Regli F, Ghika J, Feldmeyer JJ (1984) Painful ataxic hemiparesis. Arch Neurol 41:892–893CrossRefPubMedGoogle Scholar
  2. Cambier DC, De Corte E, Danneels LA, Witvrouw EE (2003) Treating sensory impairments in the post-stroke upper limb with intermittent pneumatic compression. Results of a preliminary trial. Clin Rehabil 17:14–20CrossRefPubMedGoogle Scholar
  3. Caplan LR (2012) Ataxia in patients with brain infarcts and hemorrhages. Handb Clin Neuro 103:147–160CrossRefGoogle Scholar
  4. Chen JC, Liang CC, Shaw FZ (2005) Facilitation of sensory and motor recovery by thermal intervention for the hemiplegic upper limb in acute stroke patients: a single-blind randomized clinical trial. Stroke 36:2665–2669CrossRefPubMedGoogle Scholar
  5. Chhetri SK, Gow D, Shaunak S, Varma A (2014) Clinical assessment of the sensory ataxias: diagnostic algorithm with illustrative cases. Pract Neurol 14:242–251CrossRefPubMedGoogle Scholar
  6. Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. Routledge Academic, New YorkGoogle Scholar
  7. Cuypers K, Levin O, Thijs H, Swinnen SP, Meesen RL (2010) Long-term TENS treatment improves tactile sensitivity in MS patients. Neurorehabil Neural Repair 24:420–427CrossRefPubMedGoogle Scholar
  8. Dempsey-Jones H, Harrar V, Oliver J, Johansen-Berg H, Spence C, Makin TR (2016) Transfer of tactile perceptual learning to untrained neighboring fingers reflects natural use relationships. J Neurophysiol 115:1088–1097CrossRefPubMedGoogle Scholar
  9. Desmurget M, Prablanc C, Rossetti Y, Arzi M, Paulignan Y, Urquizar C, Mignot JC (1995) Postural and synergic control for three-dimensional movements of reaching and grasping. J Neurophysiol 74(2):905–910CrossRefPubMedGoogle Scholar
  10. Dobato JL, Villanueva JA, Giménez-Roldán S (1990) Sensory ataxic hemiparesis in thalamic hemorrhage. Stroke 21:1749–1753CrossRefPubMedGoogle Scholar
  11. Dworkin RH, Turk DC, Revicki DA, Harding G, Coyne KS, Peirce-Sandner S, Bhagwat D, Everton D, Burke LB, Cowan P, Farrar JT, Hertz S, Max MB, Rappaport BA, Melzack R (2009) Development and initial validation of an expanded and revised version of the Short-form McGill Pain Questionnaire (SF-MPQ-2). Pain 144:35–42CrossRefPubMedGoogle Scholar
  12. Fujisaki W (2012) Effects of delayed visual feedback on grooved pegboard test performance. Front Psychol 8:61Google Scholar
  13. Gaveau V, Pisella L, Priot AE, Fukui T, Rossetti Y, Pélisson D, Prablanc C (2014) Automatic online control of motor adjustments in reaching and grasping. Neuropsychologia 55:25–40CrossRefPubMedGoogle Scholar
  14. Gentilucci M, Toni I, Chieffi S, Pavesi G (1994) The role of proprioception in the control of prehension movements: a kinematic study in a peripherally deafferented patient and in normal subjects. Exp Brain Res 99:483–500CrossRefPubMedGoogle Scholar
  15. Gentilucci M, Toni I, Daprati E, Gangitano M (1997) Tactile input of the hand and the control of reaching to grasp movements. Exp Brain Res 114:130–137CrossRefPubMedGoogle Scholar
  16. Gentilucci M, Daprati E, Gangitano M (1998) Haptic information differentially interferes with visual analysis in reaching-grasping control and in perceptual processes. Neuroreport 9:887–891CrossRefPubMedGoogle Scholar
  17. Ghika J, Bogousslavsky J, Henderson J, Maeder P, Regli F (1994) The “jerky dystonic unsteady hand”: a delayed motor syndrome in posterior thalamic infarctions. J Neurol 241:537–542CrossRefPubMedGoogle Scholar
  18. Gordon AM, Forssberg H, Iwasaki N (1994) Formation and lateralization of internal representations underlying motor commands during precision grip. Neuropsychologia 32:555–568CrossRefPubMedGoogle Scholar
  19. Gross D (1984) Contralateral local anesthesia in stump, phantom and post-traumatic pain. Reg Anaesth 7:65–73PubMedGoogle Scholar
  20. Heldmann B, Kerkhoff G, Struppler A, Havel P, Jahn T (2000) Repetitive peripheral magnetic stimulation alleviates tactile extinction. Neuroreport 11:3193–3198CrossRefPubMedGoogle Scholar
  21. Hogan N, Sternad D (2009) Sensitivity of smoothness measures to movement duration, amplitude, and arrests. J Mot Behav 41:529–534CrossRefPubMedPubMedCentralGoogle Scholar
  22. Iwamura Y, Iriki A, Tanaka M (1994) Bilateral hand representation in the postcentral somatosensory cortex. Nature 369:554–556CrossRefPubMedGoogle Scholar
  23. Jeannerod M (1984) The timing of natural prehension movements. J Mot Behav 16:235–254CrossRefPubMedGoogle Scholar
  24. Jeannerod M, Arbib MA, Rizzolatti G, Sakata H (1995) Grasping objects: the cortical mechanisms of visuomotor transformation. Trends Neurosci 18:314–320CrossRefPubMedGoogle Scholar
  25. Jones SA, Fiehler K, Henriques DY (2012) A task-dependent effect of memory and hand-target on proprioceptive localization. Neuropsychologia 50:1462–1470CrossRefPubMedGoogle Scholar
  26. Kammers MP, Kootker JA, Hogendoorn H, Dijkerman HC (2010) How many motoric body representations can we grasp? Exp Brain Res 202:203–212CrossRefPubMedGoogle Scholar
  27. Kim JW, Kim SH, Cha JK (1999) Pseudochoreoathetosis in four patients with hypesthetic ataxic hemiparesis in a thalamic lesion. J Neurol 246:1075–1079CrossRefPubMedGoogle Scholar
  28. Kuehn E, De Havas J, Silkoset E, Gomi H, Haggard P (2015) On the bimanual integration of proprioceptive information. Exp Brain Res 233:1273–1288CrossRefPubMedGoogle Scholar
  29. Kuntzer T, Antoine JC, Steck AJ (2004) Clinical features and pathophysiological basis of sensory neuronopathies (ganglionopathies). Muscle Nerve 30:255–268CrossRefPubMedGoogle Scholar
  30. Langhorne P, Bernhardt J, Kwakkel G (2011) Stroke rehabilitation. Lancet 377:1693–1702CrossRefPubMedGoogle Scholar
  31. Lemmens RJ, Timmermans AA, Janssen-Potten YJ, Smeets RJ, Seelen HA (2012) Valid and reliable instruments for arm-hand assessment at ICF activity level in persons with hemiplegia: a systematic review. BMC Neuro 12:21CrossRefGoogle Scholar
  32. Liu M, Chino N, Tuji T, Masakado Y, Hase K, Kimura A (2002) Psychometric properties of the stroke impairment assessment set (SIAS). Neurorehabil Neural Repair 16:339–351CrossRefPubMedGoogle Scholar
  33. Mann GE, Burridge JH, Malone LJ, Strike PW (2005) A pilot study to investigate the effects of electrical stimulation on recovery of hand function and sensation in subacute stroke patients. Neuromodulation 8:193–202CrossRefPubMedGoogle Scholar
  34. McCrea PH, Eng JJ (2005) Consequences of increased neuromotor noise for reaching movements in persons with stroke. Exp Brain Res 162:70–77CrossRefPubMedGoogle Scholar
  35. Melo TP, Bogousslavsky J (1992) Hemiataxia-hypesthesia: a thalamic stroke syndrome. J Neurol Neurosurg Psychiatry 55:581–584CrossRefPubMedPubMedCentralGoogle Scholar
  36. Nowak DA, Glasauer S, Hermsdorfer J (2004) How predictive is grip force control in the complete absence of somatosensory feedback? Brain 127:182–192CrossRefPubMedGoogle Scholar
  37. Patchay S, Castiello U, Haggard P (2003) A cross-modal interference effect in grasping objects. Psychon Bull Rev 10:924–931CrossRefPubMedGoogle Scholar
  38. Patchay S, Haggard P, Castiello U (2006) An object-centred reference frame for control of grasping: effects of grasping a distractor object on visuomotor control. Exp Brain Res 170:532–542CrossRefPubMedGoogle Scholar
  39. Reichenbach A, Thielscher A, Peer A, Bülthoff HH, Bresciani JP (2014) A key region in the human parietal cortex for processing proprioceptive hand feedback during reaching movements. Neuroimage 84:615–625CrossRefPubMedGoogle Scholar
  40. Rice MS, Newell KM (2001) Interlimb coupling and left hemiplegia because of right cerebral vascular accident. Occup Ther J Res 21:12–28CrossRefGoogle Scholar
  41. Richards L, Senesac C, McGuirk T, Woodbury M, Howland D, Davis S, Patterson T (2008) Response to intensive upper extremity therapy by individuals with ataxia from stroke. Top Stroke Rehabil 15:262–271CrossRefPubMedGoogle Scholar
  42. Rohrer B, Fasoli S, Krebs HI, Hughes R, Volpe B, Frontera WR, Stein J, Hogan N (2002) Movement smoothness changes during stroke recovery. J Neurosci 22:8297–8304CrossRefPubMedGoogle Scholar
  43. Rothwell JC, Traub MM, Day BL, Obeso JA, Thomas PK, Marsden CD (1982) Manual motor performance in a deafferented man. Brain 105:515–542CrossRefPubMedGoogle Scholar
  44. Seki M, Hase K, Takahashi H, Liu M (2014) Comparison of three instruments to assess changes of motor impairment in acute hemispheric stroke: the Stroke Impairment Assessment Set (SIAS), the National Institute of Health Stroke Scale (NIHSS) and the Canadian Neurological Scale (CNS). Disabil Rehabil 36:1549–1554CrossRefPubMedGoogle Scholar
  45. Sumitani M, Yozu A, Tomioka T, Yamada Y, Miyauchi S (2010) Using the intact hand for objective assessment of phantom hand-perception. Eur J Pain 14:261–265CrossRefPubMedGoogle Scholar
  46. Topka H, Konczak J, Dichgans J (1998) Coordination of multi-joint arm movements in cerebellar ataxia: analysis of hand and angular kinematics. Exp Brain Res 119:483–492CrossRefPubMedGoogle Scholar
  47. Torre K, Hammami N, Metrot J, van Dokkum L, Coroian F, Mottet D, Amri M, Laffont I (2013) Somatosensory-related limitations for bimanual coordination after stroke. Neurorehabil Neural Repair 27:507–515CrossRefPubMedGoogle Scholar
  48. van Dokkum L, Hauret I, Mottet D, Froger J, Métrot J, Laffont I (2014) The contribution of kinematics in the assessment of upper limb motor recovery early after stroke. Neurorehabil Neural Repair 28:4–12CrossRefPubMedGoogle Scholar
  49. van Kordelaar J, van Wegen E, Kwakkel G (2014) Impact of time on quality of motor control of the paretic upper limb after stroke. Arch Phys Med Rehabil 95:338–344CrossRefPubMedGoogle Scholar
  50. Wolpert DM, Ghahramani Z, Jordan MI (1995) An internal model for sensorimotor integration. Science 269:1880–1882CrossRefPubMedGoogle Scholar
  51. Wong JD, Wilson ET, Kistemaker DA, Gribble PL (2014) Bimanual proprioception: are two hands better than one? J Neurophysiol 111:1362–1368CrossRefPubMedGoogle Scholar
  52. Yozbatiran N, Donmez B, Kayak N, Bozan O (2006) Electrical stimulation of wrist and fingers for sensory and functional recovery in acute hemiplegia. Clin Rehabil 20:4–11CrossRefPubMedGoogle Scholar
  53. Zopf R, Truong S, Finkbeiner M, Friedman J, Williams MA (2011) Viewing and feeling touch modulates hand position for reaching. Neuropsychologia 49:1287–1293CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Michihiro Osumi
    • 1
    • 2
    Email author
  • Masahiko Sumitani
    • 3
  • Yuko Otake
    • 3
  • Shu Morioka
    • 1
    • 2
  1. 1.Graduate School of Health ScienceKio UniversityNaraJapan
  2. 2.Neurorehabilitation Research CenterKio UniversityNaraJapan
  3. 3.Department of Pain and Palliative MedicineThe University of Tokyo HospitalTokyoJapan

Personalised recommendations