Effects of a robot-aided somatosensory training on proprioception and motor function in stroke survivors
I-Ling Yeh, Jessica Holst-Wolf, Naveen Elangovan, Anna Vera Cuppone, Kamakshi Lakshminarayan, Leonardo Cappello, Lorenzo Masia, Jürgen Konczak, I-Ling Yeh, Jessica Holst-Wolf, Naveen Elangovan, Anna Vera Cuppone, Kamakshi Lakshminarayan, Leonardo Cappello, Lorenzo Masia, Jürgen Konczak
Abstract
Background: Proprioceptive deficits after stroke are associated with poor upper limb function, slower motor recovery, and decreased self-care ability. Improving proprioception should enhance motor control in stroke survivors, but current evidence is inconclusive. Thus, this study examined whether a robot-aided somatosensory-based training requiring increasingly accurate active wrist movements improves proprioceptive acuity as well as motor performance in chronic stroke.
Methods: Twelve adults with chronic stroke completed a 2-day training (age range: 42-74 years; median time-after-stroke: 12 months; median Fugl-Meyer UE: 65). Retention was assessed at Day 5. Grasping the handle of a wrist-robotic exoskeleton, participants trained to roll a virtual ball to a target through continuous wrist adduction/abduction movements. During training vision was occluded, but participants received real-time, vibro-tactile feedback on their forearm about ball position and speed. Primary outcome was the just-noticeable-difference (JND) wrist position sense threshold as a measure of proprioceptive acuity. Secondary outcomes were spatial error in an untrained wrist tracing task and somatosensory-evoked potentials (SEP) as a neural correlate of proprioceptive function. Ten neurologically-intact adults were recruited to serve as non-stroke controls for matched age, gender and hand dominance (age range: 44 to 79 years; 6 women, 4 men).
Results: Participants significantly reduced JND thresholds at posttest and retention (Stroke group: pretest: mean: 1.77° [SD: 0.54°] to posttest mean: 1.38° [0.34°]; Control group: 1.50° [0.46°] to posttest mean: 1.45° [SD: 0.54°]; F[2,37] = 4.54, p = 0.017, ηp2 = 0.20) in both groups. A higher pretest JND threshold was associated with a higher threshold reduction at posttest and retention (r = - 0.86, - 0.90, p ≤ 0.001) among the stroke participants. Error in the untrained tracing task was reduced by 22 % at posttest, yielding an effect size of w = 0.13. Stroke participants exhibited significantly reduced P27-N30 peak-to-peak SEP amplitude at pretest (U = 11, p = 0.03) compared to the non-stroke group. SEP measures did not change systematically with training.
Conclusions: This study provides proof-of-concept that non-visual, proprioceptive training can induce fast, measurable improvements in proprioceptive function in chronic stroke survivors. There is encouraging but inconclusive evidence that such somatosensory learning transfers to untrained motor tasks. Trial registration Clinicaltrials.gov; Registration ID: NCT02565407; Date of registration: 01/10/2015; URL: https://ichgcp.net/clinical-trials-registry/NCT02565407 .
Keywords: Cerebrovascular disease/stroke; Human; Rehabilitation; Somatosensation; Upper limb.
Conflict of interest statement
The authors declare that they have no competing interests.
Figures
References
- Kessner SS, Bingel U, Thomalla G. Somatosensory deficits after stroke: a scoping review. Top Stroke Rehabil. 2016;23(2):136–46. doi: 10.1080/10749357.2015.1116822.
- Connell L, Lincoln N, Radford K. Somatosensory impairment after stroke: frequency of different deficits and their recovery. Clin Rehabil. 2008;22(8):758–67. doi: 10.1177/0269215508090674.
- Sommerfeld DK, von Arbin MH. The impact of somatosensory function on activity performance and length of hospital stay in geriatric patients with stroke. Clin Rehabil. 2004;18(2):149–55. doi: 10.1191/0269215504cr710oa.
- Tyson SF, Hanley M, Chillala J, Selley AB, Tallis RC. Sensory loss in hospital-admitted people with stroke: characteristics, associated factors, and relationship with function. Neurorehabil Neural Repair. 2008;22(2):166–72. doi: 10.1177/1545968307305523.
- Coupar F, Pollock A, Rowe P, Weir C, Langhorne P. Predictors of upper limb recovery after stroke: a systematic review and meta-analysis. Clin Rehabil. 2012;26(4):291–313. doi: 10.1177/0269215511420305.
- Meyer S, Karttunen AH, Thijs V, Feys H, Verheyden G. How do somatosensory deficits in the arm and hand relate to upper limb impairment, activity, and participation problems after stroke? A systematic review. Phys Ther. 2014;94(9):1220–31. doi: 10.2522/ptj.20130271.
- Ingemanson ML, Rowe JR, Chan V, Wolbrecht ET, Reinkensmeyer DJ, Cramer SC. Somatosensory system integrity explains differences in treatment response after stroke. Neurology. 2019;92(10):e1098-e108. doi: 10.1212/WNL.0000000000007041.
- Miall RC, Rosenthal O, Ørstavik K, Cole JD, Sarlegna FR. Loss of haptic feedback impairs control of hand posture: a study in chronically deafferented individuals when grasping and lifting objects. Exp Brain Res. 2019;237(9):2167–84. doi: 10.1007/s00221-019-05583-2.
- Miall RC, Kitchen NM, Nam SH, Lefumat H, Renault AG, Ørstavik K, et al. Proprioceptive loss and the perception, control and learning of arm movements in humans: evidence from sensory neuronopathy. Exp Brain Res. 2018;236(8):2137–55. doi: 10.1007/s00221-018-5289-0.
- Timm F, Kuehn E. A Mechanical Stimulation Glove to Induce Hebbian Plasticity at the Fingertip. Front Hum Neurosci. 2020;14:177. doi: 10.3389/fnhum.2020.00177.
- Kattenstroth JC, Kalisch T, Sczesny-Kaiser M, Greulich W, Tegenthoff M, Dinse HR. Daily repetitive sensory stimulation of the paretic hand for the treatment of sensorimotor deficits in patients with subacute stroke: RESET, a randomized, sham-controlled trial. BMC Neurol. 2018;18(1):2. doi: 10.1186/s12883-017-1006-z.
- Dechaumont-Palacin S, Marque P, De Boissezon X, Castel-Lacanal E, Carel C, Berry I, et al. Neural correlates of proprioceptive integration in the contralesional hemisphere of very impaired patients shortly after a subcortical stroke: an FMRI study. Neurorehabil Neural Repair. 2008;22(2):154–65. doi: 10.1177/1545968307307118.
- Vahdat S, Darainy M, Thiel A, Ostry DJ. A single session of robot-controlled proprioceptive training modulates functional connectivity of sensory motor networks and improves reaching accuracy in chronic stroke. Neurorehabil Neural Repair. 2019;33(1):70–81. doi: 10.1177/1545968318818902.
- De Santis D, Zenzeri J, Casadio M, Masia L, Riva A, Morasso P, et al. Robot-assisted training of the kinesthetic sense: enhancing proprioception after stroke. Front Hum Neurosci. 2014;8:1037.
- Rowe JB, Chan V, Ingemanson ML, Cramer SC, Wolbrecht ET, Reinkensmeyer DJ. Robotic assistance for training finger movement using a Hebbian model: a randomized controlled trial. Neurorehabil Neural Repair. 2017;31(8):769–80. doi: 10.1177/1545968317721975.
- Chiyohara S, Furukawa JI, Noda T, Morimoto J, Imamizu H. Passive training with upper extremity exoskeleton robot affects proprioceptive acuity and performance of motor learning. Scientific reports. 2020;10(1):11820. doi: 10.1038/s41598-020-68711-x.
- Vahdat S, Darainy M, Ostry DJ. Structure of plasticity in human sensory and motor networks due to perceptual learning. J Neurosci. 2014;34(7):2451–63. doi: 10.1523/JNEUROSCI.4291-13.2014.
- Aman JE, Elangovan N, Yeh IL, Konczak J. The effectiveness of proprioceptive training for improving motor function: a systematic review. Front Hum Neurosci. 2014;8:1075.
- Sigrist R, Rauter G, Riener R, Wolf P. Augmented visual, auditory, haptic, and multimodal feedback in motor learning: a review. Psychon Bull Rev. 2013;20(1):21–53. doi: 10.3758/s13423-012-0333-8.
- Krueger AR, Giannoni P, Shah V, Casadio M, Scheidt RA. Supplemental vibrotactile feedback control of stabilization and reaching actions of the arm using limb state and position error encodings. J Neuroeng Rehabil. 2017;14(1):36. doi: 10.1186/s12984-017-0248-8.
- Risi N, Shah V, Mrotek LA, Casadio M, Scheidt RA. Supplemental vibrotactile feedback of real-time limb position enhances precision of goal-directed reaching. J Neurophysiol. 2019;122(1):22–38. doi: 10.1152/jn.00337.2018.
- 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. doi: 10.1371/journal.pone.0164511.
- Yamada T, Kimura J, Wilkinson JT, Kayamori R. Short-and long-latency median somatosensory evoked potentials: findings in patients with localized neurological lesions. Arch Neurol. 1983;40(4):215–20. doi: 10.1001/archneur.1983.04050040045007.
- Meyer S, De Bruyn N, Lafosse C, Van Dijk M, Michielsen M, Thijs L, et al. Somatosensory impairments in the upper limb poststroke: distribution and sssociation with motor function and visuospatial neglect. Neurorehabil Neural Repair. 2016;30(8):731–42. doi: 10.1177/1545968315624779.
- Peurala SH, Pitkänen K, Sivenius J, Tarkka IM. Cutaneous electrical stimulation may enhance sensorimotor recovery in chronic stroke. Clin Rehabil. 2002;16(7):709–16. doi: 10.1191/0269215502cr543oa.
- Kattenstroth JC, Kalisch T, Peters S, Tegenthoff M, Dinse HR. Long-term sensory stimulation therapy improves hand function and restores cortical responsiveness in patients with chronic cerebral lesions. Three single case studies. Front Hum Neurosci. 2012;6:244. doi: 10.3389/fnhum.2012.00244.
- Hislop H, Avers D, Brown M. Daniels and Worthingham’s muscle testing-e-book: techniques of manual examination and performance testing. Elsevier Health Sciences; 2013.
- Folstein MF, Folstein SE, McHugh PR. Mini-Mental State: a practical method for grading the cognitive state of patients for the clinician: Pergamon Press; 1975.
- Bohannon RW, Smith MB. Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys Ther. 1987;67(2):206–7. doi: 10.1093/ptj/67.2.206.
- Masia L, Casadio M, Giannoni P, Sandini G, Morasso P. Performance adaptive training control strategy for recovering wrist movements in stroke patients: a preliminary, feasibility study. J Neuroeng Rehabil. 2009;6(1):1–11. doi: 10.1186/1743-0003-6-44.
- Masia L, Casadio M, Sandini G, Morasso P. Eye-hand coordination during dynamic visuomotor rotations. PloS One. 2009;4(9):e7004. doi: 10.1371/journal.pone.0007004.
- Cappello L, Elangovan N, Contu S, Khosravani S, Konczak J, Masia L. Robot-aided assessment of wrist proprioception. Front Hum Neurosci. 2015;9:198. doi: 10.3389/fnhum.2015.00198.
- Calota A, Feldman AG, Levin MF. Spasticity measurement based on tonic stretch reflex threshold in stroke using a portable device. Clin Neurophysiol. 2008;119(10):2329–37. doi: 10.1016/j.clinph.2008.07.215.
- Prins N. The psi-marginal adaptive method: How to give nuisance parameters the attention they deserve (no more, no less) J Vis. 2013;13(7):3. doi: 10.1167/13.7.3.
- Elangovan N, Herrmann A, Konczak J. Assessing proprioceptive function: evaluating joint position matching methods against psychophysical thresholds. Phys Ther. 2014;94(4):553–61. doi: 10.2522/ptj.20130103.
- Herter TM, Scott SH, Dukelow SP. Vision does not always help stroke survivors compensate for impaired limb position sense. J Neuroeng Rehabil. 2019;16(1):129. doi: 10.1186/s12984-019-0596-7.
- Delorme A, Makeig S. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods. 2004;134(1):9–21. doi: 10.1016/j.jneumeth.2003.10.009.
- Lopez-Calderon J, Luck SJ. ERPLAB: an open-source toolbox for the analysis of event-related potentials. Front Hum Neurosci. 2014;8:213. doi: 10.3389/fnhum.2014.00213.
- Cruccu G, Aminoff M, Curio G, Guerit J, Kakigi R, Mauguiere F, et al. Recommendations for the clinical use of somatosensory-evoked potentials. Clin Neurophysiol. 2008;119(8):1705–19. doi: 10.1016/j.clinph.2008.03.016.
- Longo MR, Pernigo S, Haggard P. Vision of the body modulates processing in primary somatosensory cortex. Neurosci Lett. 2011;489(3):159–63. doi: 10.1016/j.neulet.2010.12.007.
- Tomczak M, Tomczak E. The need to report effect size estimates revisited. An overview of some recommended measures of effect size. Trends Sport Sci. 2014;21(1).
- Carey LM, Matyas TA, Oke LE. Sensory loss in stroke patients: effective training of tactile and proprioceptive discrimination. Arch Phys Med Rehabil. 1993;74(6):602–11. doi: 10.1016/0003-9993(93)90158-7.
- Carey LM, Matyas TA. Training of somatosensory discrimination after stroke: facilitation of stimulus generalization. Am J Phys Med Rehabil. 2005;84(6):428–42. doi: 10.1097/01.PHM.0000159971.12096.7F.
- Byl N, Roderick J, Mohamed O, Hanny M, Kotler J, Smith A, et al. Effectiveness of sensory and motor rehabilitation of the upper limb following the principles of neuroplasticity: patients stable poststroke. Neurorehabil Neural Repair. 2003;17(3):176–91. doi: 10.1177/0888439003257137.
- Borstad AL, Bird T, Choi S, Goodman L, Schmalbrock P, Nichols-Larsen DS. Sensorimotor training and neural reorganization after stroke: a case series. J Neurol Phys Ther. 2013;37(1):27–36. doi: 10.1097/NPT.0b013e318283de0d.
- Turville M, Carey LM, Matyas TA, Blennerhassett J. Change in functional arm use is associated with somatosensory skills after sensory retraining poststroke. Am J Occup Ther. 2017;71(3):7103190070p1-p9. doi: 10.5014/ajot.2017.024950.
- Restuccia D, Valeriani M, Insola A, Lo Monaco M, Grassi E, Barba C, et al. Modality-related scalp responses after electrical stimulation of cutaneous and muscular upper limb afferents in humans. Muscle Nerve. 2002;26(1):44–54. doi: 10.1002/mus.10163.
Source: PubMed