Quantification of upper limb position sense using an exoskeleton and a virtual reality display

BackgroundProprioceptive sense plays a significant role in the generation and correction of skilled movements and, consequently, in most activities of daily living. We developed a new proprioception assessment protocol that enables the quantification of elbow position sense without using the opposite arm, involving active movement of the evaluated limb or relying on working memory. The aims of this descriptive study were to validate this assessment protocol by quantifying the elbow position sense of healthy adults, before using it in individuals who sustained a stroke, and to investigate its test-retest reliability.MethodsElbow joint position sense was quantified using a robotic device and a virtual reality system. Two assessments were performed, by the same evaluator, with a one-week interval. While the participant’s arms and hands were occluded from vision, the exoskeleton passively moved the dominant arm from an initial to a target position. Then, a virtual arm representation was projected on a screen placed over the participant’s arm. This virtual representation and the real arm were not perfectly superimposed, however. Participants had to indicate verbally the relative position of their arm (more flexed or more extended; two-alternative forced choice paradigm) compared to the virtual representation. Each participant completed a total of 136 trials, distributed in three phases. The angular differences between the participant’s arm and the virtual representation ranged from 1° to 27° and changed pseudo-randomly across trials. No feedback about results was provided to the participants during the task. A discrimination threshold was statistically extracted from a sigmoid curve fit representing the relationship between the angular difference and the percentage of successful trials. Test-retest reliability was evaluated with 3 different complementary approaches, i.e. a Bland-Altman analysis, an intraclass correlation coefficient (ICC) and a standard error of measurement (SEm).ResultsThirty participants (24.6 years old; 17 males, 25 right-handed) completed both assessments. The mean discrimination thresholds were 7.0 ± 2.4 (mean ± standard deviation) and 5.9 ± 2.1 degrees for the first and the second assessment session, respectively. This small difference between assessments was significant (− 1.1 ± 2.2 degrees), however. The assessment protocol was characterized by a fair to good test-retest reliability (ICC = 0.47).ConclusionThis study demonstrated the potential of this assessment protocol to objectively quantify elbow position sense in healthy individuals. Futures studies will validate this protocol in older adults and in individuals who sustained a stroke.

[1]  Derick T Wade,et al.  The Rivermead Assessment of Somatosensory Performance (RASP): standardization and reliability data , 2002, Clinical rehabilitation.

[2]  G Atkinson,et al.  Statistical Methods For Assessing Measurement Error (Reliability) in Variables Relevant to Sports Medicine , 1998, Sports medicine.

[3]  Claude Ghez,et al.  A robotic test of proprioception within the hemiparetic arm post-stroke , 2014, Journal of NeuroEngineering and Rehabilitation.

[4]  L. Carey,et al.  Somatosensory assessment and treatment after stroke: An evidence-practice gap. , 2015, Australian occupational therapy journal.

[5]  Vicky Chan,et al.  Use of a robotic device to measure age-related decline in finger proprioception , 2015, Experimental Brain Research.

[6]  S. Scott,et al.  The independence of deficits in position sense and visually guided reaching following stroke , 2012, Journal of NeuroEngineering and Rehabilitation.

[7]  Meigen Liu,et al.  Clinical usefulness and validity of robotic measures of reaching movement in hemiparetic stroke patients , 2015, Journal of NeuroEngineering and Rehabilitation.

[8]  Martin Tegenthoff,et al.  Age-related changes in the joint position sense of the human hand , 2012, Clinical interventions in aging.

[9]  A. Armstrong,et al.  Reliability of range-of-motion measurement in the elbow and forearm. , 1998, Journal of shoulder and elbow surgery.

[10]  F. Ribeiro,et al.  Knee joint position sense of roller hockey players: a comparative study , 2016, Sports biomechanics.

[11]  D. McCloskey,et al.  The contribution of muscle afferents to kinaesthesia shown by vibration induced illusions of movement and by the effects of paralysing joint afferents. , 1972, Brain : a journal of neurology.

[12]  S. Springate The effect of sample size and bias on the reliability of estimates of error: a comparative study of Dahlberg's formula. , 2012, European journal of orthodontics.

[13]  J. Weir Quantifying test-retest reliability using the intraclass correlation coefficient and the SEM. , 2005, Journal of strength and conditioning research.

[14]  Jennifer A. Semrau,et al.  Anatomical correlates of proprioceptive impairments following acute stroke: A case series , 2014, Journal of the Neurological Sciences.

[15]  Jean-Sébastien Roy,et al.  Development and reliability of a measure evaluating dynamic proprioception during walking with a robotized ankle-foot orthosis, and its relation to dynamic postural control. , 2016, Gait & posture.

[16]  W. Garraway,et al.  Proprioception and spatial neglect after stroke. , 1983, Age and ageing.

[17]  Olivier Lambercy,et al.  Age-based model for metacarpophalangeal joint proprioception in elderly , 2017, Clinical interventions in aging.

[18]  L. Carey,et al.  Impaired limb position sense after stroke: a quantitative test for clinical use. , 1996, Archives of physical medicine and rehabilitation.

[19]  F. J. Clark,et al.  Characteristics of knee joint receptors in the cat , 1969, The Journal of physiology.

[20]  D. Goble,et al.  Proprioceptive Acuity Assessment Via Joint Position Matching: From Basic Science to General Practice , 2010, Physical Therapy.

[21]  R L Sainburg,et al.  Control of limb dynamics in normal subjects and patients without proprioception. , 1995, Journal of neurophysiology.

[22]  G Y Zou,et al.  Sample size formulas for estimating intraclass correlation coefficients with precision and assurance , 2012, Statistics in medicine.

[23]  Thomas Bak,et al.  Frequency and Prognostic Value of Cognitive Disorders in Stroke Patients , 2008, Dementia and Geriatric Cognitive Disorders.

[24]  Sarah F Tyson,et al.  Sensory Loss in Hospital-Admitted People With Stroke: Characteristics, Associated Factors, and Relationship With Function , 2008, Neurorehabilitation and neural repair.

[25]  James Dean Brown,et al.  Standard error vs. Standard error of measurement Standard error vs. Standard error of measurement , 1999 .

[26]  J. Gordon,et al.  Impairments of reaching movements in patients without proprioception. I. Spatial errors. , 1995, Journal of neurophysiology.

[27]  Nicolas Robitaille,et al.  Real-time modulation of visual feedback on human full-body movements in a virtual mirror: development and proof-of-concept , 2015, Journal of NeuroEngineering and Rehabilitation.

[28]  B. Martin,et al.  Age-Related Differences in Upper Limb Proprioceptive Acuity , 2007, Perceptual and motor skills.

[29]  M. M. Taylor,et al.  PEST: Efficient Estimates on Probability Functions , 1967 .

[30]  Stephen H. Scott,et al.  Test–retest reliability of KINARM robot sensorimotor and cognitive assessment: in pediatric ice hockey players , 2015, Journal of NeuroEngineering and Rehabilitation.

[31]  Stephen H. Scott,et al.  Robotic Assessment of Sensorimotor Deficits After Traumatic Brain Injury , 2012, Journal of neurologic physical therapy : JNPT.

[32]  Daniel J Goble,et al.  Plastic changes in hand proprioception following force-field motor learning. , 2010, Journal of neurophysiology.

[33]  S. Rathore,et al.  Characterization of Incident Stroke Signs and Symptoms: Findings From the Atherosclerosis Risk in Communities Study , 2002, Stroke.

[34]  F. J. Clark,et al.  Proprioception with the proximal interphalangeal joint of the index finger. Evidence for a movement sense without a static-position sense. , 1986, Brain : a journal of neurology.

[35]  Nadina B. Lincoln,et al.  The unreliability of sensory assessments , 1991 .

[36]  Jürgen Konczak,et al.  Assessing Proprioceptive Function: Evaluating Joint Position Matching Methods Against Psychophysical Thresholds , 2013, Physical Therapy.

[37]  Valentina Squeri,et al.  Wrist Proprioception: Amplitude or Position Coding? , 2016, Front. Neurorobot..

[38]  Nadina B. Lincoln,et al.  Reliability and Revision of the Nottingham Sensory Assessment for Stroke Patients , 1998 .

[39]  Janice I. Glasgow,et al.  Assessment of Upper-Limb Sensorimotor Function of Subacute Stroke Patients Using Visually Guided Reaching , 2010, Neurorehabilitation and neural repair.

[40]  J. Konczak,et al.  Robot-Aided Assessment of Wrist Proprioception , 2015, Front. Hum. Neurosci..

[41]  S. Scott,et al.  Quantitative Assessment of Limb Position Sense Following Stroke , 2010, Neurorehabilitation and neural repair.

[42]  F. J. Clark,et al.  Contributions of cutaneous and joint receptors to static knee-position sense in man. , 1979, Journal of neurophysiology.

[43]  F. J. Clark Information signaled by sensory fibers in medial articular nerve. , 1975, Journal of neurophysiology.

[44]  C Ghez,et al.  Roles of proprioceptive input in the programming of arm trajectories. , 1990, Cold Spring Harbor symposia on quantitative biology.

[45]  Thomas A Matyas,et al.  Frequency of discriminative sensory loss in the hand after stroke in a rehabilitation setting. , 2011, Journal of rehabilitation medicine.

[46]  M. M. Taylor,et al.  Erratum and Note: PEST: Efficient Estimates on Probability Functions [J. Acoust. Soc. Am. 41, 782–787 (1967)] , 1967 .

[47]  D. Downham,et al.  How to assess the reliability of measurements in rehabilitation. , 2005, American journal of physical medicine & rehabilitation.

[48]  D. McCloskey,et al.  Joint sense, muscle sense, and their combination as position sense, measured at the distal interphalangeal joint of the middle finger. , 1976, The Journal of physiology.

[49]  C Ghez,et al.  Proprioceptive control of interjoint coordination. , 1995, Canadian journal of physiology and pharmacology.

[50]  Olivier Lambercy,et al.  Reliable and Rapid Robotic Assessment of Wrist Proprioception Using a Gauge Position Matching Paradigm , 2016, Front. Hum. Neurosci..

[51]  J. Fleiss The design and analysis of clinical experiments , 1987 .

[52]  J C Rothwell,et al.  Manual motor performance in a deafferented man. , 1982, Brain : a journal of neurology.