Vision does not always help stroke survivors compensate for impaired limb position sense

Journal of NeuroEngineering and Rehabilitation - Tập 16 - Trang 1-12 - 2019
Troy M. Herter1, Stephen H. Scott2,3,4, Sean P. Dukelow5,6
1Department of Exercise Science, University of South Carolina, Columbia, USA
2Centre for Neuroscience Studies, Queen’s University, Kingston, Canada
3Department of Anatomy and Cell Biology, Queen's University, Kingston, Canada
4School of Medicine, Queen’s University, Kingston, Canada
5Hotchkiss Brain Institute, University of Calgary, Calgary, Canada
6Department of Clinical Neurosciences, University of Calgary, Calgary, Canada

Tóm tắt

Position sense is commonly impaired after stroke. Traditional rehabilitation methods instruct patients to visualize their limbs to compensate for impaired position sense. Our goal was to evaluate how the use of vision influences impaired position sense. We examined 177 stroke survivors, an average of 12.7 days (+/− 10 days (SD)) post-stroke, and 133 neurologically-intact controls with a robotic assessment of position sense. The robot positioned one limb (affected) and subjects attempted to mirror-match the position using the opposite limb (unaffected). Subjects completed the test without, then with vision of their limbs. We examined three measures of position sense: variability (Var), contraction/expansion (C/E) and systematic shift (Shift). We classified stroke survivors as having full compensation if they performed the robotic task abnormally without vision but corrected performance within the range of normal with vision. Stroke survivors were deemed to have partial compensation if they performed the task outside the range of normal without and with vision, but improved significantly with vision. Those with absent compensation performed the task abnormally in both conditions and did not improve with vision. Many stroke survivors demonstrated impaired position sense with vision occluded [Var: 116 (66%), C/E: 91 (51%), Shift: 52 (29%)]. Of those stroke survivors with impaired position sense, some exhibited full compensation with vision [Var: 23 (20%), C/E: 42 (46%), Shift: 32 (62%)], others showed partial compensation [Var: 37 (32%), C/E: 8 (9%), Shift: 3 (6%)] and many displayed absent compensation (Var: 56 (48%), C/E: 41 (45%), Shift: 17 (33%)]. Stroke survivors with an affected left arm, visuospatial neglect and/or visual field defects were less likely to compensate for impaired position sense using vision. Our results indicate that vision does not help many stroke survivors compensate for impaired position sense, at least within the current paradigm. This contrasts with historical reports that vision helps compensate for proprioceptive loss following neurologic injuries.

Tài liệu tham khảo

de Weerdt W, Lincoln NB, Harrison MA. Prediction of arm and hand function recovery in stroke patients. Int J Rehabil Res. 1987;10:110–2. Kusoffsky A, Wadell I, Nilsson BY. The relationship between sensory impairment and motor recovery in patients with hemiplegia. Scand J Rehabil Med. 1982;14:27–32. Medical M's. Nursing & Allied Health Dictionary. 6th ed. Elsevier Health Sciences: St. Louis, Missouri; 2002. Sarlegna FR, Sainburg RL. The roles of vision and proprioception in the planning of reaching movements. Adv Exp Med Biol. 2009;629:317–35. Scott SH. A functional taxonomy of bottom-up sensory feedback processing for motor actions. Trends Neurosci. 2016;39:512–26. Shadmehr R, Smith MA, Krakauer JW. Error correction, sensory prediction, and adaptation in motor control. Annu Rev Neurosci. 2010;33:89–108. Wolpert DM, Diedrichsen J, Flanagan JR. Principles of sensorimotor learning. Nat Rev Neurosci. 2011;12:739–51. Sherrington CS. On the proprio-ceptive system, especially in its reflex aspect. Brain. 1907;29:467–82. Sullivan JE, Hedman LD. Sensory dysfunction following stroke: incidence, significance, examination, and intervention. Top Stroke Rehabil. 2008;15:200–17. Schabrun SM, Hillier S. Evidence for the retraining of sensation after stroke: a systematic review. Clin Rehabil. 2009;23:27–39. Dukelow SP, Herter TM, Moore KD, Demers MJ, Glasgow JI, Bagg SD, et al. Quantitative assessment of limb position sense following stroke. Neurorehabil Neural Repair. 2010;24:178–87. Semrau JA, Herter TM, Scott SH, Dukelow SP. Robotic identification of kinesthetic deficits after stroke. Stroke. 2013;44:3414–21. Dukelow SP, Herter TM, Bagg SD, Scott SH. The independence of deficits in position sense and visually guided reaching following stroke. J Neuroeng Rehabil. 2012;9:72. Semrau JA, Herter TM, Scott SH, Dukelow SP. Examining differences in patterns of sensory and motor recovery after stroke with robotics. Stroke. 2015;46:3459–69. Yekutiel M, Guttman E. A controlled trial of the retraining of the sensory function of the hand in stroke patients. J Neurol Neurosurg Psychiatry. 1993;56:241–4. http://www.stroke-rehab.com/. 2014 [cited 2015 Jan. 5, 2015]; Available from: http://www.stroke-rehab.com/sensory-re-education.html. Lederman E. CGD, Donatelli R. The Science and Practice of Manual Therapy. 2nd ed. Elsevier Health Sciences: St. Louis, MO; 2005. Wynn Parry C.B. SM, Miller D. Rehabilitation of the Hand. London: Butterworth; 1981. Newport R, Hindle JV, Jackson SR. Links between vision and somatosensation. Vision can improve the felt position of the unseen hand. Curr Biol. 2001;11:975–80. van Beers RJ, Sittig AC. Denier van der Gon JJ. The precision of proprioceptive position sense. Exp Brain Res. 1998;122:367–77. Sober SJ, Sabes PN. Multisensory integration during motor planning. J Neurosci. 2003;23:6982–92. Crevecoeur F, Munoz DP, Scott SH. Dynamic multisensory integration: somatosensory speed trumps visual accuracy during feedback control. J Neurosci. 2016;36:8598–611. van Beers RJ, Wolpert DM, Haggard P. When feeling is more important than seeing in sensorimotor adaptation. Curr Biol. 2002;12:834–7. Robin C, Toussaint L, Blandin Y, Vinter A. Sensory integration in the learning of aiming toward "self-defined" targets. Res Q Exerc Sport. 2004 Dec;75:381–7. Casadio M, Morasso P, Sanguineti V, Giannoni P. Minimally assistive robot training for proprioception enhancement. Exp Brain Res. 2009;194:219–31. Wong JD, Wilson ET, Gribble PL. Spatially selective enhancement of proprioceptive acuity following motor learning. J Neurophysiol. 2011;105:2512–21. Cusmano I, Sterpi I, Mazzone A, Ramat S, Delconte C, Pisano F, et al. Evaluation of upper limb sense of position in healthy individuals and patients after stroke. J Healthc Eng. 2014;5:145–62. Simo L, Botzer L, Ghez C, Scheidt RA. A robotic test of proprioception within the hemiparetic arm post-stroke. J Neuroeng Rehabil. 2014;11:77. Scott SH. Apparatus for measuring and perturbing shoulder and elbow joint positions and torques during reaching. J Neurosci Methods. 1999;89:119–27. Debert CT, Herter TM, Scott SH, Dukelow S. Robotic assessment of sensorimotor deficits after traumatic brain injury. J Neurol Phys Ther. 2012;36:58–67. Kenzie JM, Semrau JA, Findlater SE, Herter TM, Hill MD, Scott SH, et al. Anatomical correlates of proprioceptive impairments following acute stroke: a case series. J Neurol Sci. 2014;342:52–61. Herter TM, Scott SH, Dukelow SP. Systematic changes in position sense accompany normal aging across adulthood. J Neuroeng Rehabil. 2014;11:43. Keith RA, Granger CV, Hamilton BB, Sherwin FS. The functional independence measure: a new tool for rehabilitation. Adv Clin Rehabil. 1987;1:6–18. Hirayama K, Fukutake T, Kawamura M. 'Thumb localizing test' for detecting a lesion in the posterior column-medial lemniscal system. J Neurol Sci. 1999;167:45–9. Bickley LS. Bates' guide to physical examination and history taking. 11th ed. Lippincott, WIlliams & Wilkins: Hagerstown, MD; 2012. Wilson B, Cockburn J, Halligan P. Development of a behavioral test of visuospatial neglect. Arch Phys Med Rehabil. 1987;68:98–102. Gowland C, Stratford P, Ward M, Moreland J, Torresin W, Van Hullenaar S, et al. Measuring physical impairment and disability with the Chedoke-McMaster stroke assessment. Stroke. 1993;24:58–63. Bohannon RW, Smith MB. Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys Ther. 1987;67:206–7. Nasreddine ZS, Phillips NA, Bedirian V, Charbonneau S, Whitehead V, Collin I, et al. The Montreal cognitive assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc. 2005;53:695–9. Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971;9:97–113. Cohen J. A power primer. Psychol Bull. 1992;112:155–9. Singh T, Perry CM, Herter TM. A geometric method for computing ocular kinematics and classifying gaze events using monocular remote eye tracking in a robotic environment. J Neuroeng Rehabil. 2016;13:10. Singh T, Fridriksson J, Perry CM, Tryon SC, Ross A, Fritz S, Herter TM. A novel computational model to probe visual search deficits during motor performance. J Neurophysiol. 2017;117:79–92. Singh T, Perry CM, Fritz SL, Fridriksson J, Herter TM. Eye movements interfere with limb motor control in stroke survivors. Neurorehabil Neural Repair. 2018;32:724–34. Kenzie JM, Findlater SE, Pittman DJ, Goodyear BG, Dukelow SP. Errors in proprioceptive matching post-stroke are associated with impaired recruitment of parietal, supplementary motor, and temporal cortices. Brain Imaging Behav. 2019 Jun 20. https://doi.org/10.1007/s11682-019-00149-w. Marini F, Zenzeri J, Pippo V, Morasso P, Campus C. Neural correlates of proprioception in upper limb position matching. Hum Brain Mapp. https://doi.org/10.1002/hbm.24739. Findlater SE, Desai JA, Semrau JA, Kenzie JM, Rorden C, Herter TM, Scott SH, Dukelow SP. Central perception of position sense involves a distributed neural network - evidence from lesion-behavior analyses. Cortex. 2016;79:42–56. Findlater SE, Hawe RL, Mazerolle EL, Al Sultan AS, Cassidy JM, Scott SH, Pike GB, Dukelow SP. Comparing CST Lesion metrics as biomarkers for recovery of motor and proprioceptive impairments after stroke. Neurorehabil Neural Repair. 2019. https://doi.org/10.1177/1545968319868714. Kenzie JM, Semrau JA, Findlater SE, Yu AY, Desai JA, Herter TM, Hill MD, Scott SH, Dukelow SP. Localization of impaired kinesthetic processing post-stroke. Front Hum Neurosci. 2016;10:505. Wolpert DM, Goodbody SJ, Husain M. Maintaining internal representations: the role of the human superior parietal lobe. Nat Neurosci. 1998;1:529–33. Corbetta M, Miezin FM, Shulman GL, Petersen SE. A PET study of visuospatial attention. J Neurosci. 1993;13:1202–26. Posner MI, Walker JA, Friedrich FJ, Rafal RD. Effects of parietal injury on covert orienting of attention. J Neurosci. 1984;4:1863–74. Coull JT, Frith CD, Frackowiak RS, Grasby PM. A fronto-parietal network for rapid visual information processing: a PET study of sustained attention and working memory. Neuropsychologia. 1996;34:1085–95. Hagura N, Takei T, Hirose S, Aramaki Y, Matsumura M, Sadato N, et al. Activity in the posterior parietal cortex mediates visual dominance over kinesthesia. J Neurosci. 2007;27:7047–53. Naito E, Roland PE, Grefkes C, Choi HJ, Eickhoff S, Geyer S, et al. Dominance of the right hemisphere and role of area 2 in human kinesthesia. J Neurophysiol. 2005;93:1020–34. Shi Y, Apker G, Buneo CA. Multimodal representation of limb endpoint position in the posterior parietal cortex. J Neurophysiol. 2013;109:2097–107. Andersen RA, Bracewell RM, Barash S, Gnadt JW, Fogassi L. Eye position effects on visual, memory, and saccade-related activity in areas LIP and 7a of macaque. J Neurosci. 1990;10:1176–96. Thura D, Hadj-Bouziane F, Meunier M, Boussaoud D. Hand position modulates saccadic activity in the frontal eye field. Behav Brain Res. 2008;186:148–53. Wang X, Zhang M, Cohen IS, Goldberg ME. The proprioceptive representation of eye position in monkey primary somatosensory cortex. Nat Neurosci. 2007;10:640–6. Cohen YE, Andersen RA. A common reference frame for movement plans in the posterior parietal cortex. Nat Rev Neurosci. 2002;3:553–62. Vegaro E, Casadio M, Squeri V, Giannoni P, Morasso P, Sanguinti V. Self-adaptive robot training of stroke aptients for continuous tracking movements. J Neuroengineering and Rehabilitation. 2010;7:13. De Santis D, Zenzeri J, Casadio M, Masia L, Riva A, Morasso P, Squeri V. Robot-assisted training of kinesthetic sense: enhance proprioception after stroke. Front Hum Neurosci. 2015;8:1037. https://doi.org/10.3389/fnhum.2014.01037. Squeri V, Zenzeri J, Morasso P, Basteris A, Giannoni P. Integrating proprioceptive assessment with proprioceptive training of stroke patients. In: IEEE 12th international conference on rehabilitation robotics. Zurich, ETH Zurich Science City, Switzerland: Rehab Week; 2011. p. 1059–64. Smania N, Montagnana B, Faccioli S, Fiaschi A, Aglioti SM. Rehabilitation of somatic sensation and related deficit of motor control in patients with pure sensory stroke. Arch Phys Med Rehabil. 2003;84:1692–702. Cuppone AV, Squeri V, Semprini M, Masia L, Konczak J. Robot-assisted proprioceptive training with added Vibro-tactile feedback enhances somatosensory and motor performance. PLoS One. 2016;11(10):e0164511. Koopman B, van Asseldonk EH, van der Kooij H. Selective control of gait subtasks in robotic gait training: foot clearance support in stroke survivors with a powered exoskeleton. J Neuroeng Rehabil. 2013;10:3. Apker GA, Karimi CP, Buneo CA. Contributions of vision and proprioception to arm movement planning in the vertical plane. Neurosci Lett. 2011;503:186–90. Soechting JF, Lacquaniti F. Quantitative evaluation of the electromyographic responses to multidirectional load perturbations of the human arm. J Neurophysiol. 1988;59:1296–313. Mennie N, Hayhoe M, Sullivan B. Look-ahead fixations: anticipatory eye movements in natural tasks. Exp Brain Res. 2007;179:427–42.