Biomimetic encoding model for restoring touch in bionic hands through a nerve interface

OBJECTIVE Hand function can be restored in upper-limb amputees by equipping them with anthropomorphic prostheses controlled with signals from residual muscles. The dexterity of these bionic hands is severely limited in large part by the absence of tactile feedback about interactions with objects. We propose that, to the extent that artificial touch mimics its natural counterpart, these sensory signals will be more easily integrated into the motor plan for object manipulation. APPROACH We describe an approach to convey tactile feedback through electrical stimulation of the residual somatosensory nerves that mimics the aggregate activity of tactile fibers that would be produced in the nerve of a native hand during object interactions. Specifically, we build a parsimonious model that maps the stimulus-described as time-varying indentation depth, indentation rate, and acceleration-into continuous estimates of the time-varying population firing rate and of the size of the recruited afferent population. MAIN RESULTS The simple model can reconstruct aggregate afferent responses to a wide range of stimuli, including those experienced during activities of daily living. SIGNIFICANCE We discuss how the proposed model can be implemented with a peripheral nerve interface and anticipate it will lead to improved dexterity for prosthetic hands.

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

[2]  David J. Warren,et al.  Using multiple high-count electrode arrays in human median and ulnar nerves to restore sensorimotor function after previous transradial amputation of the hand , 2014, 2014 36th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[3]  T. Lejeune,et al.  Importance of cutaneous feedback in maintaining a secure grip during manipulation of hand-held objects. , 2003, Journal of neurophysiology.

[4]  P.H. Veltink,et al.  Simulation of intrafascicular and extraneural nerve stimulation , 1988, IEEE Transactions on Biomedical Engineering.

[5]  J. Randall Flanagan,et al.  Coding and use of tactile signals from the fingertips in object manipulation tasks , 2009, Nature Reviews Neuroscience.

[6]  Christian Ethier,et al.  Intrafascicular stimulation of monkey arm nerves evokes coordinated grasp and sensory responses. , 2013, Journal of neurophysiology.

[7]  Hannes P. Saal,et al.  Millisecond Precision Spike Timing Shapes Tactile Perception , 2012, The Journal of Neuroscience.

[8]  G.S. Dhillon,et al.  Direct neural sensory feedback and control of a prosthetic arm , 2005, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[9]  Benoit P. Delhaye,et al.  Simulating tactile signals from the whole hand with millisecond precision , 2017, Proceedings of the National Academy of Sciences.

[10]  Dustin Tyler,et al.  Optimizing nerve cuff stimulation of targeted regions through use of genetic algorithms , 2011, 2011 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[11]  M. Keith,et al.  A neural interface provides long-term stable natural touch perception , 2014, Science Translational Medicine.

[12]  Hannes P. Saal,et al.  Biomimetic approaches to bionic touch through a peripheral nerve interface , 2015, Neuropsychologia.

[13]  O. Frank,et al.  Segregation by modality of myelinated and unmyelinated fibers in human sensory nerve fascicles , 1991, Muscle & nerve.

[14]  S. Diamond,et al.  Effect of Surface , 1982 .

[15]  Ronald J Triolo,et al.  Fascicular anatomy of human femoral nerve: implications for neural prostheses using nerve cuff electrodes. , 2009, Journal of rehabilitation research and development.

[16]  J. F. Dammann,et al.  The Neural Coding of Stimulus Intensity: Linking the Population Response of Mechanoreceptive Afferents with Psychophysical Behavior , 2007, The Journal of Neuroscience.

[17]  M. Hollins,et al.  The vibrations of texture , 2003, Somatosensory & motor research.

[18]  Charles A. Miller,et al.  Electrode configuration influences action potential initiation site and ensemble stochastic response properties , 2003, Hearing Research.

[19]  Dustin J Tyler,et al.  Quantification of human upper extremity nerves and fascicular anatomy , 2017, Muscle & nerve.

[20]  Benoni B. Edin,et al.  Prediction of object contact during grasping , 2008, Experimental Brain Research.

[21]  Ernst Niebur,et al.  A simple model of mechanotransduction in primate glabrous skin. , 2013, Journal of neurophysiology.

[22]  Kenneth O. Johnson,et al.  The roles and functions of cutaneous mechanoreceptors , 2001, Current Opinion in Neurobiology.

[23]  R. S. Johansson,et al.  Roles of glabrous skin receptors and sensorimotor memory in automatic control of precision grip when lifting rougher or more slippery objects , 2004, Experimental Brain Research.

[24]  Benoit P. Delhaye,et al.  The neural basis of perceived intensity in natural and artificial touch , 2016, Science Translational Medicine.

[25]  Keehoon Kim,et al.  Robotic touch shifts perception of embodiment to a prosthesis in targeted reinnervation amputees. , 2011, Brain : a journal of neurology.

[26]  V. Mountcastle,et al.  The sense of flutter-vibration: comparison of the human capacity with response patterns of mechanoreceptive afferents from the monkey hand. , 1968, Journal of neurophysiology.

[27]  Hannes P. Saal,et al.  Touch is a team effort: interplay of submodalities in cutaneous sensibility , 2014, Trends in Neurosciences.

[28]  Benoit P. Delhaye,et al.  Key considerations in designing a somatosensory neuroprosthesis , 2016, Journal of Physiology-Paris.

[29]  T. Stieglitz,et al.  A transverse intrafascicular multichannel electrode (TIME) to interface with the peripheral nerve. , 2010, Biosensors & bioelectronics.

[30]  D. Durand,et al.  Functionally selective peripheral nerve stimulation with a flat interface nerve electrode , 2002, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[31]  Wenqin Luo,et al.  Modality-Based Organization of Ascending Somatosensory Axons in the Direct Dorsal Column Pathway , 2013, The Journal of Neuroscience.

[32]  Paul J. Abbas,et al.  Effects of electrode-to-fiber distance on temporal neural response with electrical stimulation , 2004, IEEE Transactions on Biomedical Engineering.

[33]  M. Schiefer,et al.  Fascicular Perineurium Thickness, Size, and Position Affect Model Predictions of Neural Excitation , 2008, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[34]  Paul J. Abbas,et al.  The Dependence of Auditory Nerve Rate Adaptation on Electric Stimulus Parameters, Electrode Position, and Fiber Diameter: A Computer Model Study , 2010, Journal of the Association for Research in Otolaryngology.

[35]  Johan H. M. Frijns,et al.  The consequences of neural degeneration regarding optimal cochlear implant position in scala tympani: A model approach , 2006, Hearing Research.

[36]  Alan M. Wing,et al.  Internal models of the motor system that explain predictive grip force control , 2004 .

[37]  Jean-Louis Thonnard,et al.  The cutaneous contribution to adaptive precision grip , 2004, Trends in Neurosciences.

[38]  Daniel Tan,et al.  Sensory feedback by peripheral nerve stimulation improves task performance in individuals with upper limb loss using a myoelectric prosthesis , 2016, Journal of neural engineering.

[39]  Dominique M. Durand,et al.  Chronic measurement of the stimulation selectivity of the flat interface nerve electrode , 2004, IEEE Transactions on Biomedical Engineering.

[40]  F. Rattay Analysis of models for extracellular fiber stimulation , 1989, IEEE Transactions on Biomedical Engineering.

[41]  Sung Soo Kim,et al.  Conveying Tactile Feedback in Sensorized Hand Neuroprostheses Using a Biofidelic Model of Mechanotransduction , 2009, IEEE Transactions on Biomedical Circuits and Systems.

[42]  J. F. Dammann,et al.  The Effect of Surface Wave Propagation on Neural Responses to Vibration in Primate Glabrous Skin , 2012, PloS one.

[43]  Stefan Mihalas,et al.  Does Afferent Heterogeneity Matter in Conveying Tactile Feedback Through Peripheral Nerve Stimulation? , 2011, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[44]  K. Horch,et al.  Residual function in peripheral nerve stumps of amputees: implications for neural control of artificial limbs. , 2004, The Journal of hand surgery.

[45]  L. Miller,et al.  Restoring sensorimotor function through intracortical interfaces: progress and looming challenges , 2014, Nature Reviews Neuroscience.

[46]  A. Vallbo,et al.  Activity from skin mechanoreceptors recorded percutaneously in awake human subjects. , 1968, Experimental neurology.