After stroke, ankle proprioceptive deficits are common and do not typically correlate with ankle weakness. Some studies report that these deficits correlate with gait function, supporting the importance of somatosensory input for gait control. Others have not found a relationship, possibly due to use of coarse proprioception measures. Robotic assessments of proprioception offer improved consistency and sensitivity.
Objective:
To establish relationships between ankle proprioception, gait function, and ankle motor in stroke survivors.
Methods:
We studied 39 individuals in the chronic phase of stroke using 2 robotic tests, Crisscross and Joint Position Reproduction (JPR), to quantify ankle proprioception. We examined associations of these measures with gait speed (10-meter walk test) and gait endurance (6-minute walk test). We also analyzed correlations with lower extremity motor impairment, including robotic measures of ankle strength (MVC) and active range of motion (AROM), and the lower extremity Fugl-Meyer exam (LEFM).
Results:
Impaired ankle proprioception was present in 87% of participants. Crisscross error weakly correlated with the 10mWT gait speed (ρ = −0.20, P = 0.23) and 6MWT distance (ρ = −0.28, P = .089). JPR error weakly correlated with 10mWT gait speed (ρ = −0.29, P = .092) and significantly correlated with 6MWT distance (ρ = −0.34, P = .04). No significant correlations were observed between ankle proprioceptive error and MVC, AROM, or LEFM (P > 0.2).
Conclusion:
These results confirm the presence of a weak relationship between ankle proprioception and gait after stroke that is independent of several common measures of motor impairment.
MentiplayBFAdairBBowerKJWilliamsGToleGClarkRA.Associations between lower limb strength and gait velocity following stroke: a systematic review. Brain Inj. 2015;29(4):409-422. doi:10.3109/02699052.2014.995231
2.
HussainSJamwalPKGhayeshMH.State-of-the-art robotic devices for ankle rehabilitation: mechanism and control review. Proc Inst Mech Eng H. 2017;231(12):1224-1234. doi:10.1177/09544119177375
3.
LinSIHsuLJWangHC.Effects of ankle proprioceptive interference on locomotion after stroke. Arch Phys Med Rehabil. 2012;93(6):1027-1033. doi:10.1016/J.APMR.2012.01.019
4.
LinPYYangYRChengSJWangRY.The relation between ankle impairments and gait velocity and symmetry in people with stroke. Arch Phys Med Rehabil. 2006;87(4):562-568. doi:10.1016/J.APMR.2005.12.042
5.
ChisholmAEPerrySDMcilroyWE.Correlations between ankle-foot impairments and dropped foot gait deviations among stroke survivors. Clin Biomech. 2013;28(9-10):1049-1054. doi:10.1016/j.clinbiomech.2013.09.007
6.
AriesAMDowningPSimJHunterSM.Effectiveness of somatosensory stimulation for the lower limb and foot to improve balance and gait after stroke: a systematic review. Brain Sci. 2022;12(8):1102. doi:10.3390/brainsci12081102
LinSI.Motor function and joint position sense in relation to gait performance in chronic stroke patients. Arch Phys Med Rehabil. 2005;86(2):197-203. doi:10.1016/J.APMR.2004.05.009
9.
HsuALTangPFJanMH.Analysis of impairments influencing gait velocity and asymmetry of hemiplegic patients after mild to moderate stroke. Arch Phys Med Rehabil. 2003;84(8):1185-1193. doi:10.1016/S0003-9993(03)00030-3
10.
HillierSImminkMThewlisD.Assessing proprioception: a systematic review of possibilities. Neurorehabil Neural Repair. 2015;29(10):933-949. doi:10.1177/1545968315573055
11.
ProskeUGandeviaSC.The proprioceptive senses: their roles in signaling body shape, body position and movement, and muscle force. Physiol Rev. 2012;92(4):1651-1697. doi:10.1152/physrev.00048.2011
12.
GandeviaSCHallLAMcCloskeyDIPotterEK.Proprioceptive sensation at the terminal joint of the middle finger. J Physiol. 1983;335(1):507-517. doi:10.1113/jphysiol.1983.sp014547
13.
AmanJEElangovanNYehILKonczakJ.The effectiveness of proprioceptive training for improving motor function: a systematic review. Front Hum Neurosci. 2015;8:119864. doi:10.3389/FNHUM.2014.01075/ABSTRACT
14.
EdgertonVRLeonRDHarkemaSJ, et al. Retraining the injured spinal cord. J Physiol. 2001;533(Pt 1):15. doi:10.1111/J.1469-7793.2001.0015B.X
15.
FujitaTOhashiYKuritaM, et al. Functions necessary for gait independence in patients with stroke: a study using decision tree. J Stroke Cerebrovasc Dis. 2020;29(8):104998. doi:10.1016/j.jstrokecerebrovasdis.2020.104998
16.
ChiaFSFKuysSLow ChoyN. Sensory retraining of the leg after stroke: systematic review and meta-analysis. Clin Rehabil. 2019;33(6):964-979. doi:10.1177/0269215519836461
17.
WutzkeCMercerVLewekM.Influence of lower extremity sensory function on locomotor adaptation following stroke: a review. Top Stroke Rehabil. 2013;20(3):233-240. doi:10.1310/TSR2003-233
18.
ShadmehrRSmithMAKrakauerJW.Error correction, sensory prediction, and adaptation in motor control. Annu Rev Neurosci. 2010;33(1):89-108. doi:10.1146/annurev-neuro-060909-153135
19.
SeoHGYunSJFarrensAJJohnsonCAReinkensmeyerDJ.A systematic review of the learning dynamics of proprioception training: specificity, acquisition, retention, and transfer. Neurorehabil Neural Repair. 2023;37(10):744-757. doi:10.1177/15459683231207354
20.
ParkSWWolfSLBlantonSWinsteinCNichols-LarsenDS.The EXCITE trial: predicting a clinically meaningful motor activity log outcome. Neurorehabil Neural Repair. 2008;22(5):486-493. doi:10.1177/1545968308316906
21.
RoweJBChanVIngemansonMLCramerSCWolbrechtETReinkensmeyerDJ.Robotic assistance for training finger movement using a hebbian model: a randomized controlled trial. Neurorehabil Neural Repair. 2017;31(8):769-780. doi:10.1177/1545968317721975
22.
IngemansonMLRoweJRChanVWolbrechtETReinkensmeyerDJCramerSC.Somatosensory system integrity explains differences in treatment response after stroke. Neurology. 2019;92(10):E1098-E1108. doi:10.1212/WNL.0000000000007041
23.
IngemansonMLRoweJRChanV, et al. Neural correlates of passive position finger sense after stroke. Neurorehabil Neural Repair. 2019;33(9):740-750. doi:10.1177/1545968319862556
24.
GorstTRogersAMorrisonSC, et al. The prevalence, distribution, and functional importance of lower limb somatosensory impairments in chronic stroke survivors: a cross sectional observational study. Disabil Rehabil. 2019;41(20):2443-2450. doi:10.1080/09638288.2018.1468932
25.
GorstTFreemanJYarrowKMarsdenJ.Assessing lower limb position sense in stroke using the gradient discrimination test (GradDTTM) and step-height discrimination test (StepDTTM): a reliability and validity study. Disabil Rehabil. 2020;42(15):2215-2223. doi:10.1080/09638288.2018.1554008
26.
ChoJEKimH.Ankle proprioception deficit is the strongest factor predicting balance impairment in patients with chronic stroke. Arch Rehabil Res Clin Transl. 2021;3(4):100165. doi:10.1016/J.ARRCT.2021.100165
27.
LeeMJKilbreathSLRefshaugeKM.Movement detection at the ankle following stroke is poor. Aust J Physiother. 2005;51(1):19-24. doi:10.1016/S0004-9514(05)70049-0
28.
HuangQZhongBElangovanNZhangMKonczakJ.A robotic device for measuring human ankle motion sense. IEEE Trans Neural Syst Rehabil Eng. 2023;31:2822-2830. doi:10.1109/TNSRE.2023.3288550
29.
HorváthÁFerentziESchwartzKJacobsNMeynsPKötelesF. The measurement of proprioceptive accuracy: a systematic literature review. J Sport Health Sci. 2023;12(2):219-225. doi:10.1016/J.JSHS.2022.04.001
30.
HanJWaddingtonGAdamsRAnsonJLiuY.Assessing proprioception: a critical review of methods. J Sport Health Sci. 2016;5(1):80-90. doi:10.1016/j.jshs.2014.10.004
31.
ZbytniewskaMKanzlerCMJordanL, et al. Reliable and valid robot-assisted assessments of hand proprioceptive, motor and sensorimotor impairments after stroke. J NeuroEng Rehabil. 2021;18(1):1-20. doi:10.1186/S12984-021-00904-5
32.
RiemannBLLephartSM.The sensorimotor system, part I: the physiologic basis of functional joint stability. J Athl Train. 2002;37(1):71-79.
33.
KoSUSimonsickEMDeshpandeNStudenskiSFerrucciL.Ankle proprioception-associated gait patterns in older adults. Med Sci Sports Exerc. 2016;48(11):2190-2194. doi:10.1249/MSS.0000000000001017
34.
TakahashiAKawanaHFurukawaK.Test–retest reliability and validity in lower limb proprioception tests using image capture technique in healthy adults. Bull Fac Phys Ther. 2024;29(1):58. doi:10.1186/s43161-024-00225-3
35.
BuschABangerterCMayerFBaurH.Reliability of the active knee joint position sense test and influence of limb dominance and sex. Sci Rep. 2023;13(1):152. doi:10.1038/s41598-022-26932-2
36.
IngemansonMLRoweJBChanVWolbrechtETCramerSCReinkensmeyerDJ.Use of a robotic device to measure age-related decline in finger proprioception. Exp Brain Res. 2016;234(1):83-93. doi:10.1007/s00221-015-4440-4
37.
BiswasPDodakianLWangPT, et al. A single-center, assessor-blinded, randomized controlled clinical trial to test the safety and efficacy of a novel brain-computer interface controlled functional electrical stimulation (BCI-FES) intervention for gait rehabilitation in the chronic stroke population. BMC Neurol. 2024;24(1):200. doi:10.1186/s12883-024-03710-3
38.
KasnerSE.Clinical interpretation and use of stroke scales. Lancet Neurol. 2006;5(7):603-612. doi:10.1016/S1474-4422(06)70495-1
39.
PageSJHadeEPerschA.Psychometrics of the wrist stability and hand mobility subscales of the Fugl-Meyer assessment in moderately impaired stroke. Phys Ther. 2015;95(1):103-108. doi:10.2522/PTJ.20130235
40.
FlansbjerUBHolmbäckAMDownhamDPattenCLexellJ.Reliability of gait performance tests in men and women with hemiparesis after stroke. J Rehabil Med. 2005;37(2):75-82. doi:10.1080/16501970410017215
41.
SeverinsenKJakobsenJKOvergaardKAndersenH.Normalized muscle strength, aerobic capacity, and walking performance in chronic stroke: a population-based study on the potential for endurance and resistance training. Arch Phys Med Rehabil. 2011;92(10):1663-1668. doi:10.1016/J.APMR.2011.04.022
42.
ScalhaTBMiyasakiELimaNMFVBorgesG.Correlations between motor and sensory functions in upper limb chronic hemiparetics after stroke. Arq Neuropsiquiatr. 2011;69(4):624-629. doi:10.1590/S0004-282X2011000500010
43.
CummingTBLoweDLindenTBernhardtJ.The AVERT MoCA data: scoring reliability in a large multicenter trial. Assessment. 2020;27(5):976-981. doi:10.1177/1073191118771516/ASSET/IMAGES/LARGE/10.1177_1073191118771516-FIG3.JPEG
44.
KayaTGoksel KaratepeAGunaydinRKocAAltundal ErcanU.Inter-rater reliability of the Modified Ashworth Scale and modified Modified Ashworth Scale in assessing poststroke elbow flexor spasticity. Int J Rehabil Res. 2011;34(1):59-64. doi:10.1097/MRR.0B013E32833D6CDF
45.
GuyattGHSullivanMJThompsonPJ, et al. The 6-minute walk: a new measure of exercise capacity in patients with chronic heart failure. Can Med Assoc J. 1985;132(8):919. Accessed January 17, 2024. https:///pmc/articles/PMC1345899/?report=abstract
46.
GermanottaMTaborriJRossiS, et al. Spasticity measurement based on tonic stretch reflex threshold in children with cerebral palsy using the pediAnklebot. Front Hum Neurosci. 2017;11:240744. doi:10.3389/FNHUM.2017.00277/BIBTEX
47.
Bertrand-CharetteMDambrevilleCBouyerLJRoyJS.Systematic review of motor control and somatosensation assessment tests for the ankle. BMJ Open Sport Exerc Med. 2020;6(1):e000685. doi:10.1136/BMJSEM-2019-000685
48.
ElangovanNHerrmannAKonczakJ.Assessing proprioceptive function: evaluating joint position matching methods against psychophysical thresholds. Phys Ther. 2014;94(4):553. doi:10.2522/PTJ.20130103
49.
TakeuchiNIzumiSI.Maladaptive plasticity for motor recovery after stroke: mechanisms and approaches. Neural Plast. 2012;2012. doi:10.1155/2012/359728
50.
MadhavanSRogersLMStinearJW.A paradox: after stroke, the non-lesioned lower limb motor cortex may be maladaptive. Eur J Neurosci. 2010;32(6):1032-1039. doi:10.1111/J.1460-9568.2010.07364.X
51.
van MelickNMeddelerBMHoogeboomTJNijhuis-vanderSandenMWGvan CingelREH.How to determine leg dominance: the agreement between self-reported and observed performance in healthy adults. PLoS ONE. 2017;12(12):e0189876. doi:10.1371/journal.pone.0189876
52.
SteffenTMHackerTAMollingerL.Age- and gender-related test performance in community-dwelling elderly people: six-minute walk test, Berg Balance Scale, timed up & go test, and gait speeds. Phys Ther. 2002;82(2):128-137. doi:10.1093/ptj/82.2.128
53.
EdgertonVRRoyRR.Robotic training and spinal cord plasticity. Brain Res Bull. 2009;78(1):4-12. doi:10.1016/j.brainresbull.2008.09.018
54.
KiehnO.Decoding the organization of spinal circuits that control locomotion. Nat Rev Neurosci. 2016;17(4):224-238. doi:10.1038/nrn.2016.9
55.
IandoloRBelliniASaioteC, et al. Neural correlates of lower limbs proprioception: an fMRI study of foot position matching. Hum Brain Mapp. 2018;39(5):1929-1944. doi:10.1002/hbm.23972
56.
HongYBaoDManorBZhouJ.Characterizing the supraspinal sensorimotor control of walking using MRI-compatible system: a systematic review. J Neuroeng Rehabil. 2024;21(1):34. doi:10.1186/s12984-024-01323-y
57.
PresaccoAGoodmanRForresterLContreras-VidalJL.Neural decoding of treadmill walking from noninvasive electroencephalographic signals. J Neurophysiol. 2011;106(4):1875-1887. doi:10.1152/jn.00104.2011
58.
HeYNathanKVenkatakrishnanA, et al. An integrated neuro-robotic interface for stroke rehabilitation using the NASA X1 powered lower limb exoskeleton. Paper presented at: 2014 36th Annual International Conference of the IEEE Engineering in Medicine and Biology Society; August26-30, 2014; Chicago, IL, USA. IEEE; 2014:3985-3988. doi:10.1109/EMBC.2014.6944497
59.
GobleDJCoxonJPVan ImpeA, et al. Brain activity during ankle proprioceptive stimulation predicts balance performance in young and older adults. J Neurosci. 2011;31(45):16344-16352. doi:10.1523/JNEUROSCI.4159-11.2011
60.
Plummer-D’AmatoPAltmannLJPSaracinoDFoxEBehrmanALMarsiskeM.Interactions between cognitive tasks and gait after stroke: a dual task study. Gait Posture. 2008;27(4):683-688. doi:10.1016/j.gaitpost.2007.09.001
61.
JuYYWangCWChengHYK. Effects of active fatiguing movement versus passive repetitive movement on knee proprioception. Clin Biomech. 2010;25(7):708-712. doi:10.1016/j.clinbiomech.2010.04.017
62.
PickardCMSullivanPEAllisonGTSingerKP.Is there a difference in hip joint position sense between young and older groups?J Gerontol A Biol Sci Med Sci. 2003;58(7):M631-M635. doi:10.1093/gerona/58.7.M631
63.
PeterkaRJ.Sensorimotor integration in human postural control. J Neurophysiol. 2002;88(3):1097-1118. doi:10.1152/JN.2002.88.3.1097
64.
BonanIVGaillardFTasseel PoncheSMarquerAVidalPPYelnikAP.Early post-stroke period: a privileged time for sensory re-weighting?J Rehabil Med. 2015;47(6):516-522. doi:10.2340/16501977-1968
65.
MaguireCCSiebenJMde BieRA.The influence of walking-aids on the plasticity of spinal interneuronal networks, central-pattern-generators and the recovery of gait post-stroke. A literature review and scholarly discussion. J Bodyw Mov Ther. 2017;21(2):422-434. doi:10.1016/j.jbmt.2016.09.012
66.
CrichtonSLBrayBDMcKevittCRuddAGWolfeCDA. Patient outcomes up to 15 years after stroke: survival, disability, quality of life, cognition and mental health. J Neurol Neurosurg Psychiatry. 2016;87(10):1091-1098. doi:10.1136/JNNP-2016-313361
CallaghanCMJohnsonCABiswasP, et al. The relationship between stroke-related cognitive impairment and robotic proprioceptive assessment. IEEE Int Conf Rehabil Robot. 2025:2025:1347-1352.
BorichMRBrodieSMGrayWAIontaSBoydLA.Understanding the role of the primary somatosensory cortex: opportunities for rehabilitation. Neuropsychologia. 2015;79:246-255. doi:10.1016/J.NEUROPSYCHOLOGIA.2015.07.007
72.
NielsenJB.Sensorimotor integration at spinal level as a basis for muscle coordination during voluntary movement in humans. J Appl Physiol. 2004;96(5):1961-1967. doi:10.1152/JAPPLPHYSIOL.01073.2003/ASSET/IMAGES/LARGE/ZDG0050430880004.JPEG
73.
DietzV.Spinal cord pattern generators for locomotion. Clin Neurophysiol. 2003;114(8):1379-1389. doi:10.1016/S1388-2457(03)00120-2
74.
CôtéMPMurrayLMKnikouM.Spinal control of locomotion: individual neurons, their circuits and functions. Front Physiol. 2018;9:340854. doi:10.3389/FPHYS.2018.00784/BIBTEX
75.
HsuALTangPFJanMH.Test-retest reliability of isokinetic muscle strength of the lower extremities in patients with stroke. Arch Phys Med Rehabil. 2002;83(8):1130-1137. doi:10.1053/apmr.2002.33652
76.
PattersonKKParafianowiczIDanellsCJ, et al. Gait asymmetry in community-ambulating stroke survivors. Arch Phys Med Rehabil. 2008;89(2):304-310. doi:10.1016/j.apmr.2007.08.142
77.
RehmeAKGrefkesC.Cerebral network disorders after stroke: evidence from imaging-based connectivity analyses of active and resting brain states in humans. J Physiol. 2013;591(1):17-31. doi:10.1113/jphysiol.2012.243469
78.
FrancisSLinXAboushoushahS, et al. fMRI analysis of active, passive and electrically stimulated ankle dorsiflexion. Neuroimage. 2008;44:469-479. doi:10.1016/j.neuroimage.2008.09.017
79.
FraenkelJWallenNHyunH.How to Design and Evaluate Research in Education. Vol. 60. Mc Graw HIll; 2011.
80.
AhmadIVermaSNoohuMMShareefMYHussainME.Sensorimotor and gait training improves proprioception, nerve function, and muscular activation in patients with diabetic peripheral neuropathy: a randomized control trial. J Musculoskelet Neuronal Interact. 2020;20(2):234-248.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
