Robotic Assessment of Wrist Proprioception During Kinaesthetic Perturbations: A Neuroergonomic Approach

Position sense refers to an aspect of proprioception crucial for motor control and learning. The onset of neurological diseases can damage such sensory afference, with consequent motor disorders dramatically reducing the associated recovery process. In regular clinical practice, assessment of proprioceptive deficits is run by means of clinical scales which do not provide quantitative measurements. However, existing robotic solutions usually do not involve multi-joint movements but are mostly applied to a single proximal or distal joint. The present work provides a testing paradigm for assessing proprioception during coordinated multi-joint distal movements and in presence of kinaesthetic perturbations: we evaluated healthy subjects' ability to match proprioceptive targets along two of the three wrist's degrees of freedom, flexion/extension and abduction/adduction. By introducing rotations along the pronation/supination axis not involved in the matching task, we tested two experimental conditions, which differed in terms of the temporal imposition of the external perturbation: in the first one, the disturbance was provided after the presentation of the proprioceptive target, while in the second one, the rotation of the pronation/ supination axis was imposed during the proprioceptive target presentation. We investigated if (i) the amplitude of the perturbation along the pronation/supination would lead to proprioceptive miscalibration; (ii) the encoding of proprioceptive target, would be influenced by the presentation sequence between the target itself and the rotational disturbance. Eighteen participants were tested by means of a haptic neuroergonomic wrist device: our findings provided evidence that the order of disturbance presentation does not alter proprioceptive acuity. Yet, a further effect has been noticed: proprioception is highly anisotropic and dependent on perturbation amplitude. Unexpectedly, the configuration of the forearm highly influences sensory feedbacks, and significantly alters subjects' performance in matching the proprioceptive targets, defining portions of the wrist workspace where kinaesthetic and proprioceptive acuity are more sensitive. This finding may suggest solutions and applications in multiple fields: from general haptics where, knowing how wrist configuration influences proprioception, might suggest new neuroergonomic solutions in device design, to clinical evaluation after neurological damage, where accurately assessing proprioceptive deficits can dramatically complement regular therapy for a better prediction of the recovery path.

[1]  Luca Citi,et al.  Restoring Natural Sensory Feedback in Real-Time Bidirectional Hand Prostheses , 2014, Science Translational Medicine.

[2]  Leeanne M. Carey,et al.  Somatosensory Loss after Stroke , 1995 .

[3]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[4]  R. Sainburg,et al.  The effect of target modality on visual and proprioceptive contributions to the control of movement distance , 2006, Experimental Brain Research.

[5]  Etienne Burdet,et al.  ReachMAN: a personal robot to train reaching and manipulation , 2009, 2009 IEEE/RSJ International Conference on Intelligent Robots and Systems.

[6]  Allison M. Okamura,et al.  Comparing proprioceptive acuity in the arm between joint space and task space , 2018, 2018 IEEE Haptics Symposium (HAPTICS).

[7]  S. Scott,et al.  Movement kinematics and proprioception in post-stroke spasticity: assessment using the Kinarm robotic exoskeleton , 2019, Journal of NeuroEngineering and Rehabilitation.

[8]  J. Konczak,et al.  The effectiveness of proprioceptive training for improving motor function: a systematic review , 2015, Front. Hum. Neurosci..

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

[10]  Francesco Giovacchini,et al.  On the design of ergonomic wearable robotic devices for motion assistance and rehabilitation , 2012, 2012 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[11]  Uwe Proske,et al.  Kinesthesia: The role of muscle receptors , 2006, Muscle & nerve.

[12]  P. Morasso,et al.  Robot-Aided Mapping of Wrist Proprioceptive Acuity across a 3D Workspace , 2016, PloS one.

[13]  J. V. D. Wal The Architecture of Connective Tissue in the Musculoskeletal System—Often Overlooked Functional Parameter as to the Proprioception of the Locomotor Apparatus , 2009, International journal of therapeutic massage & bodywork.

[14]  Christina T Fuentes,et al.  Where is your arm? Variations in proprioception across space and tasks. , 2010, Journal of neurophysiology.

[15]  C. Colby Action-Oriented Spatial Reference Frames in Cortex , 1998, Neuron.

[16]  Nicholas Moser,et al.  Importance of Wrist Movement Direction in Performing Activities of Daily Living Efficiently , 2020, 2020 42nd Annual International Conference of the IEEE Engineering in Medicine & Biology Society (EMBC).

[17]  D. McCloskey Kinesthetic sensibility. , 1978, Physiological reviews.

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

[19]  D. McCloskey,et al.  The role of joint receptors in human kinaesthesia when intramuscular receptors cannot contribute. , 1987, The Journal of physiology.

[20]  Tae Seob Kim,et al.  A Study on the Measurement of Wrist Motion Range Using the iPhone 4 Gyroscope Application , 2014, Annals of plastic surgery.

[21]  S. Gandevia,et al.  The proprioceptive senses: their roles in signaling body shape, body position and movement, and muscle force. , 2012, Physiological reviews.

[22]  Maura Casadio,et al.  The Interaction Between Position Sense and Force Control , 2018 .

[23]  C. Sherrington ON THE PROPRIO-CEPTIVE SYSTEM, ESPECIALLY IN ITS REFLEX ASPECT , 1907 .

[24]  Simona Crea,et al.  Restoration of Finger and Arm Movements Using Hybrid Brain/Neural Assistive Technology in Everyday Life Environments , 2019, Brain-Computer Interface Research.

[25]  Imre Cikajlo,et al.  Universal Haptic Drive: A Robot for Arm and Wrist Rehabilitation , 2010, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

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

[27]  S. Schabrun,et al.  Evidence for the retraining of sensation after stroke: a systematic review , 2009, Clinical rehabilitation.

[28]  Valentina Squeri,et al.  Robot-aided developmental assessment of wrist proprioception in children , 2017, Journal of NeuroEngineering and Rehabilitation.

[29]  Ashish D. Deshpande,et al.  Assessing Wrist Movement With Robotic Devices , 2018, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[30]  Monica Gori,et al.  Parkinson's disease accelerates age-related decline in haptic perception by altering somatosensory integration. , 2012, Brain : a journal of neurology.

[31]  Michael W. R. Holmes,et al.  Muscle fatigue assessment during robot-mediated movements , 2018, Journal of NeuroEngineering and Rehabilitation.

[32]  D. Reinkensmeyer,et al.  Review of control strategies for robotic movement training after neurologic injury , 2009, Journal of NeuroEngineering and Rehabilitation.

[33]  C. A. Buneo,et al.  Perception of Arm Position in Three-Dimensional Space , 2018, Front. Hum. Neurosci..

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

[35]  Edward V. Evarts,et al.  Sherrington's concept of proprioception , 1981, Trends in Neurosciences.

[36]  Daniel J. Goble,et al.  Dynamic proprioceptive target matching behavior in the upper limb: Effects of speed, task difficulty and arm/hemisphere asymmetries , 2009, Behavioural Brain Research.

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

[38]  Yang Liu,et al.  Adaptive Staircase Measurement of Hand Proprioception , 2015, PloS one.

[39]  G. Sandini,et al.  Eye-Hand Coordination during Dynamic Visuomotor Rotations , 2009, PloS one.

[40]  Richard A. Andersen,et al.  Separate body- and world-referenced representations of visual space in parietal cortex , 1998, Nature.

[41]  J. Soechting,et al.  Frames of Reference for Hand Orientation , 1995, Journal of Cognitive Neuroscience.

[42]  Edward Akelman,et al.  The Effect of Supination and Pronation on Wrist Range of Motion , 2014, Journal of Wrist Surgery.

[43]  Ilana Nisky,et al.  Assessment of bimanual proprioception during an orientation matching task with a physically coupled object , 2019, 2019 IEEE 16th International Conference on Rehabilitation Robotics (ICORR).

[44]  Anne Deblock-Bellamy,et al.  Quantification of upper limb position sense using an exoskeleton and a virtual reality display , 2018, Journal of NeuroEngineering and Rehabilitation.