Restoration of sensory information via bionic hands

Individuals who have lost the use of their hands because of amputation or spinal cord injury can use prosthetic hands to restore their independence. A dexterous prosthesis requires the acquisition of control signals that drive the movements of the robotic hand, and the transmission of sensory signals to convey information to the user about the consequences of these movements. In this Review, we describe non-invasive and invasive technologies for conveying artificial sensory feedback through bionic hands, and evaluate the technologies' long-term prospects.

[1]  Rajiv Ranganathan,et al.  Body-Machine Interface Enables People With Cervical Spinal Cord Injury to Control Devices With Available Body Movements: Proof of Concept , 2017, Neurorehabilitation and neural repair.

[2]  Benoit P. Delhaye,et al.  Neural Basis of Touch and Proprioception in Primate Cortex. , 2018, Comprehensive Physiology.

[3]  Ethan Heming,et al.  Designing a somatosensory neural prosthesis: percepts evoked by different patterns of thalamic stimulation , 2010, Journal of neural engineering.

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

[5]  Jamie Kyujin Paik,et al.  Soft Pneumatic Actuator Skin with Piezoelectric Sensors for Vibrotactile Feedback , 2016, Front. Robot. AI.

[6]  Dorian Goueytes,et al.  A fast intracortical brain–machine interface with patterned optogenetic feedback , 2018, Journal of neural engineering.

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

[8]  R. Daroff,et al.  Clinical Neurology for Psychiatrists , 1995, Neurology.

[9]  S. Bensmaia,et al.  Chronic Use of a Sensitized Bionic Hand Does Not Remap the Sense of Touch , 2020, medRxiv.

[10]  Christian Antfolk,et al.  Sensory qualities of the phantom hand map in the residual forearm of amputees. , 2016, Journal of rehabilitation medicine.

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

[12]  R. J. Vogelstein,et al.  Restoring the sense of touch with a prosthetic hand through a brain interface , 2013, Proceedings of the National Academy of Sciences.

[13]  Dustin J. Tyler,et al.  Stability and selectivity of a chronic, multi-contact cuff electrode for sensory stimulation in human amputees , 2013, 2013 6th International IEEE/EMBS Conference on Neural Engineering (NER).

[14]  K. O. Johnson,et al.  Time-course of vibratory adaptation and recovery in cutaneous mechanoreceptive afferents. , 2005, Journal of neurophysiology.

[15]  Robert D. Lipschutz,et al.  Targeted reinnervation for enhanced prosthetic arm function in a woman with a proximal amputation: a case study , 2007, The Lancet.

[16]  Stephen T. Foldes,et al.  Intracortical microstimulation of human somatosensory cortex , 2016, Science Translational Medicine.

[17]  Elizaveta V Okorokova,et al.  Biomimetic sensory feedback through peripheral nerve stimulation improves dexterous use of a bionic hand , 2019, Science Robotics.

[18]  Allister F. McGuire,et al.  A skin-inspired organic digital mechanoreceptor , 2015, Science.

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

[20]  Elizaveta V Okorokova,et al.  Biomimetic encoding model for restoring touch in bionic hands through a nerve interface , 2018, Journal of neural engineering.

[21]  F. Clemente,et al.  The myokinetic control interface: tracking implanted magnets as a means for prosthetic control , 2017, Scientific Reports.

[22]  Silvestro Micera,et al.  A critical review of interfaces with the peripheral nervous system for the control of neuroprostheses and hybrid bionic systems , 2005, Journal of the peripheral nervous system : JPNS.

[23]  Silvestro Micera,et al.  Biomimetic Intraneural Sensory Feedback Enhances Sensation Naturalness, Tactile Sensitivity, and Manual Dexterity in a Bidirectional Prosthesis , 2018, Neuron.

[24]  Silvestro Micera,et al.  A closed-loop hand prosthesis with simultaneous intraneural tactile and position feedback , 2018, Science Robotics.

[25]  Nitish V. Thakor,et al.  Prosthesis with neuromorphic multilayered e-dermis perceives touch and pain , 2018, Science Robotics.

[26]  Enzo Mastinu,et al.  Self-Contained Neuromusculoskeletal Arm Prostheses. , 2020, The New England journal of medicine.

[27]  B. Edin,et al.  Skin strain patterns provide kinaesthetic information to the human central nervous system. , 1995, The Journal of physiology.

[28]  S. Micera,et al.  A three-dimensional self-opening intraneural peripheral interface (SELINE) , 2015, Journal of neural engineering.

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

[30]  Peter H. Veltink,et al.  Vibro- and Electrotactile User Feedback on Hand Opening for Myoelectric Forearm Prostheses , 2012, IEEE Transactions on Biomedical Engineering.

[31]  William F. Agnew,et al.  Histologic and physiologic evaluation of electrically stimulated peripheral nerve: Considerations for the selection of parameters , 2006, Annals of Biomedical Engineering.

[32]  C. McIntyre,et al.  Emerging technologies for improved deep brain stimulation , 2019, Nature Biotechnology.

[33]  Paolo Dario,et al.  Biomedical applications of soft robotics , 2018, Nature Reviews Materials.

[34]  Peripheral projections of sensory fascicles in the human superficial radial nerve. , 2005, Brain : a journal of neurology.

[35]  Aneesha K. Suresh,et al.  Neural Coding of Contact Events in Somatosensory Cortex. , 2019, Cerebral cortex.

[36]  C. Cipriani,et al.  HyVE: Hybrid Vibro-Electrotactile Stimulation for Sensory Feedback and Substitution in Rehabilitation , 2014, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[37]  Vincent Duchaine,et al.  The Impact of Simultaneously Applying Normal Stress and Vibrotactile Stimulation for Feedback of Exteroceptive Information. , 2017, Journal of biomechanical engineering.

[38]  Thierry Keller,et al.  Multichannel Electrotactile Feedback With Spatial and Mixed Coding for Closed-Loop Control of Grasping Force in Hand Prostheses , 2017, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[39]  S. Bensmaia,et al.  Behavioral assessment of sensitivity to intracortical microstimulation of primate somatosensory cortex , 2015, Proceedings of the National Academy of Sciences.

[40]  J. Falkenberg An experimental study of the rate of fracture healing as assessed from the tensile strength and Sr85-activity of the callus with special reference to the effect of intramedullary nailing. , 1961, Acta orthopaedica Scandinavica. Supplementum.

[41]  Hermano Igo Krebs,et al.  A Soft Pneumatic Actuator as a Haptic Wearable Device for Upper Limb Amputees: Toward a Soft Robotic Liner , 2019, IEEE Robotics and Automation Letters.

[42]  F. McGlone,et al.  The cutaneous sensory system , 2010, Neuroscience & Biobehavioral Reviews.

[43]  Z. Kiss,et al.  Designing a Thalamic Somatosensory Neural Prosthesis: Consistency and Persistence of Percepts Evoked by Electrical Stimulation , 2011, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[44]  S. Bensmaia,et al.  The neural basis of tactile motion perception. , 2014, Journal of neurophysiology.

[45]  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.

[46]  Max Ortiz-Catalan,et al.  An osseointegrated human-machine gateway for long-term sensory feedback and motor control of artificial limbs , 2014, Science Translational Medicine.

[47]  E. Fetz,et al.  Direct electrical stimulation of the somatosensory cortex in humans using electrocorticography electrodes: a qualitative and quantitative report , 2013, Journal of neural engineering.

[48]  P. Roelfsema,et al.  Distinct Feedforward and Feedback Effects of Microstimulation in Visual Cortex Reveal Neural Mechanisms of Texture Segregation , 2017, Neuron.

[49]  R. Johansson,et al.  Tactile sensibility in the human hand: relative and absolute densities of four types of mechanoreceptive units in glabrous skin. , 1979, The Journal of physiology.

[50]  J. Wyndaele,et al.  Incidence, prevalence and epidemiology of spinal cord injury: what learns a worldwide literature survey? , 2006, Spinal Cord.

[51]  R J Triolo,et al.  Chronic stability and selectivity of four-contact spiral nerve-cuff electrodes in stimulating the human femoral nerve , 2009, Journal of neural engineering.

[52]  Matteo Bianchi,et al.  Influence of force feedback on grasp force modulation in prosthetic applications: A preliminary study , 2016, 2016 38th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[53]  R. Hallin,et al.  Microneurography in relation to intraneural topography: somatotopic organisation of median nerve fascicles in humans. , 1990, Journal of neurology, neurosurgery, and psychiatry.

[54]  Silvestro Micera,et al.  A somatotopic bidirectional hand prosthesis with transcutaneous electrical nerve stimulation based sensory feedback , 2017, Scientific Reports.

[55]  Silvestro Micera,et al.  Chronic multichannel neural recordings from soft regenerative microchannel electrodes during gait , 2015, Scientific Reports.

[56]  R. N. Scott,et al.  Sensory-feedback system compatible with myoelectric control , 2006, Medical and Biological Engineering and Computing.

[57]  Joshua M Rosenow,et al.  Methodological considerations for a chronic neural interface with the cuneate nucleus of macaques. , 2017, Journal of neurophysiology.

[58]  R. Triolo,et al.  A Model of Selective Activation of the Femoral Nerve With a Flat Interface Nerve Electrode for a Lower Extremity Neuroprosthesis , 2008, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[59]  J. Mcelhaney,et al.  Afferent sensory feedback for lower extremity prosthesis. , 1982, Clinical orthopaedics and related research.

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

[61]  R. Triolo,et al.  Selective activation of the human tibial and common peroneal nerves with a flat interface nerve electrode , 2013, Journal of neural engineering.

[62]  Dario Farina,et al.  Bionic Limbs: Clinical Reality and Academic Promises , 2014, Science Translational Medicine.

[63]  Florian Solzbacher,et al.  Long term in vitro functional stability and recording longevity of fully integrated wireless neural interfaces based on the Utah Slant Electrode Array , 2011, Journal of neural engineering.

[64]  J. Kaas,et al.  The somatotopic organization of area 2 in macaque monkeys , 1985, The Journal of comparative neurology.

[65]  Eric E. Thomson,et al.  Perceiving Invisible Light through a Somatosensory Cortical Prosthesis , 2013, Nature Communications.

[66]  P. Herberts,et al.  Ideas on sensory feedback in hand prostheses , 1979, Prosthetics and orthotics international.

[67]  Joseph E O'Doherty,et al.  A learning–based approach to artificial sensory feedback leads to optimal integration , 2014, Nature Neuroscience.

[68]  Sergey L. Gratiy,et al.  Fully integrated silicon probes for high-density recording of neural activity , 2017, Nature.

[69]  K W Horch,et al.  The neural signal for the intensity of a tactile stimulus , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[70]  Francesco Giovacchini,et al.  Artificial Roughness Encoding with a Bio-inspired MEMS- based Tactile Sensor Array , 2009, Sensors.

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

[72]  P. Rossini,et al.  Intraneural stimulation elicits discrimination of textural features by artificial fingertip in intact and amputee humans , 2016, eLife.

[73]  D. Moran,et al.  Micro-channel sieve electrode for concurrent bidirectional peripheral nerve interface. Part B: stimulation , 2019, Journal of neural engineering.

[74]  Dingguo Zhang,et al.  Developing Non-Somatotopic Phantom Finger Sensation to Comparable Levels of Somatotopic Sensation through User Training With Electrotactile Stimulation , 2017, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[75]  Blair A. Lock,et al.  Redirection of cutaneous sensation from the hand to the chest skin of human amputees with targeted reinnervation , 2007, Proceedings of the National Academy of Sciences.

[76]  V. Brown,et al.  Vagal nerve stimulation: a review of its applications and potential mechanisms that mediate its clinical effects , 2005, Neuroscience & Biobehavioral Reviews.

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

[78]  T. Carlstedt,et al.  Clustering of Pacinian corpuscle afferent fibres in the human median nerve , 1999, Experimental Brain Research.

[79]  A Mazzoni,et al.  Comparison of linear frequency and amplitude modulation for intraneural sensory feedback in bidirectional hand prostheses , 2018, Scientific Reports.

[80]  Sliman J. Bensmaia,et al.  Biological and bionic hands: natural neural coding and artificial perception , 2015, Brain Stimulation.

[81]  Hannes Bleuler,et al.  Active tactile exploration enabled by a brain-machine-brain interface , 2011, Nature.

[82]  Lee E Miller,et al.  Toward a Proprioceptive Neural Interface that Mimics Natural Cortical Activity. , 2016, Advances in experimental medicine and biology.

[83]  W.J. Tompkins,et al.  Electrotactile and vibrotactile displays for sensory substitution systems , 1991, IEEE Transactions on Biomedical Engineering.

[84]  R. Johansson,et al.  Predictive feed-forward sensory control during grasping and manipulation in man , 1993 .

[85]  L. Körner,et al.  Afferent electrical nerve stimulation for sensory feedback in hand prostheses. Clinical and physiological aspects. , 1979, Acta orthopaedica Scandinavica. Supplementum.

[86]  R. Romo,et al.  Sensing without Touching Psychophysical Performance Based on Cortical Microstimulation , 2000, Neuron.

[87]  Sliman J. Bensmaia,et al.  High-dimensional representation of texture in somatosensory cortex of primates , 2018, Proceedings of the National Academy of Sciences.

[88]  Dario Farina,et al.  Time-division multiplexing for myoelectric closed-loop control using electrotactile feedback , 2014, Journal of NeuroEngineering and Rehabilitation.

[89]  J. Mortimer,et al.  A spiral nerve cuff electrode for peripheral nerve stimulation , 1988, IEEE Transactions on Biomedical Engineering.

[90]  Linda Resnik,et al.  Home Use of a Neural-connected Sensory Prosthesis Provides the Functional and Psychosocial Experience of Having a Hand Again , 2018, Scientific Reports.

[91]  Breanne P. Christie,et al.  Frequency Shapes the Quality of Tactile Percepts Evoked through Electrical Stimulation of the Nerves , 2020, The Journal of Neuroscience.

[92]  Ellen A. Lumpkin,et al.  Mechanisms of sensory transduction in the skin , 2007, Nature.

[93]  Michael L. Boninger,et al.  Restored tactile sensation improves neuroprosthetic arm control , 2019, bioRxiv.

[94]  Francesco Tenore,et al.  Beyond intuitive anthropomorphic control: recent achievements using brain computer interface technologies , 2017, Defense + Security.

[95]  Zhenan Bao,et al.  A bioinspired flexible organic artificial afferent nerve , 2018, Science.

[96]  Warren M. Grill,et al.  Sensory percepts induced by microwire array and DBS microstimulation in human sensory thalamus , 2017, Brain Stimulation.

[97]  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.

[98]  Benoit P. Delhaye,et al.  Sensory adaptation to electrical stimulation of the somatosensory nerves , 2018, Journal of neural engineering.

[99]  Rafael Granja-Vazquez,et al.  Illusory movement perception improves motor control for prosthetic hands , 2018, Science Translational Medicine.

[100]  Silvestro Micera,et al.  Six‐Month Assessment of a Hand Prosthesis with Intraneural Tactile Feedback , 2018, Annals of neurology.

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

[102]  J. Collinger,et al.  Sensory restoration by epidural stimulation of the lateral spinal cord in upper-limb amputees , 2020, eLife.

[103]  David Alan Boone,et al.  Development and Real World Use of a Vibratory Haptic Feedback System for Upper-Limb Prosthetic Users , 2016 .

[104]  R. Hallin,et al.  Fitting Pieces in the Peripheral Nerve Puzzle , 2001, Experimental Neurology.

[105]  Xiangyang Zhu,et al.  Somatotopical feedback versus non-somatotopical feedback for phantom digit sensation on amputees using electrotactile stimulation , 2015, Journal of NeuroEngineering and Rehabilitation.

[106]  Sharlene N. Flesher,et al.  Perceptual responses to microstimulation frequency are spatially organized in human somatosensory cortex , 2020, bioRxiv.

[107]  R. Hallin,et al.  Clustering of slowly adapting type II mechanoreceptors in human peripheral nerve and skin. , 1998, Brain : a journal of neurology.

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

[109]  Peter H Veltink,et al.  Hand-opening feedback for myoelectric forearm prostheses: performance in virtual grasping tasks influenced by different levels of distraction. , 2012, Journal of rehabilitation research and development.

[110]  Alberto Mazzoni,et al.  Neuromorphic Artificial Touch for Categorization of Naturalistic Textures , 2017, IEEE Transactions on Neural Networks and Learning Systems.

[111]  Sungshin Kim,et al.  A computational model that predicts behavioral sensitivity to intracortical microstimulation , 2017, Journal of neural engineering.

[112]  Dustin J Tyler,et al.  Artificial tactile and proprioceptive feedback improves performance and confidence on object identification tasks , 2018, PloS one.

[113]  L. Miller,et al.  Electrical Stimulation of the Proprioceptive Cortex (Area 3a) Used to Instruct a Behaving Monkey , 2008, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[114]  Timothy Bretl,et al.  Controlling sensation intensity for electrotactile stimulation in human-machine interfaces , 2018, Science Robotics.

[115]  J. Greenspan,et al.  Neurophysiology of Tactile Perception : A Tribute to Steven Hsiao Neuronal responses to tactile stimuli and tactile sensations evoked by microstimulation in the human thalamic principal somatic sensory nucleus ( ventral caudal ) , 2016 .

[116]  D. Huber,et al.  Rapid Integration of Artificial Sensory Feedback during Operant Conditioning of Motor Cortex Neurons , 2017, Neuron.

[117]  Jack W. Tsao,et al.  Phantom Limb Pain: Theories and Therapies , 2010, The neurologist.

[118]  Julia P. Slopsema,et al.  Surface electrical stimulation to evoke referred sensation. , 2015, Journal of rehabilitation research and development.

[119]  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.

[120]  Timothy H Lucas,et al.  A chronic neural interface to the macaque dorsal column nuclei. , 2016, Journal of neurophysiology.

[121]  S. Vijayakumar,et al.  The role of feed-forward and feedback processes for closed-loop prosthesis control , 2011, Journal of NeuroEngineering and Rehabilitation.

[122]  Benoit P. Delhaye,et al.  Robo-Psychophysics: Extracting Behaviorally Relevant Features from the Output of Sensors on a Prosthetic Finger , 2016, IEEE Transactions on Haptics.

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

[124]  N. A. Bernshteĭn The co-ordination and regulation of movements , 1967 .

[125]  Gregory A. Clark,et al.  Motor Control and Sensory Feedback Enhance Prosthesis Embodiment and Reduce Phantom Pain After Long-Term Hand Amputation , 2018, Front. Hum. Neurosci..

[126]  Hannes P. Saal,et al.  Spatial and temporal codes mediate the tactile perception of natural textures , 2014, 2014 IEEE Haptics Symposium (HAPTICS).

[127]  J. Shoemaker,et al.  Arrangement of sympathetic fibers within the human common peroneal nerve: implications for microneurography. , 2013, Journal of applied physiology.

[128]  Dario Farina,et al.  Closed-Loop Control of Grasping With a Myoelectric Hand Prosthesis: Which Are the Relevant Feedback Variables for Force Control? , 2014, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

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

[130]  K. Yoshida,et al.  Selective stimulation of peripheral nerve fibers using dual intrafascicular electrodes , 1993, IEEE Transactions on Biomedical Engineering.

[131]  Jing Wu,et al.  Task-Specific Somatosensory Feedback via Cortical Stimulation in Humans , 2016, IEEE Transactions on Haptics.

[132]  Dario Farina,et al.  Wearable Dual-Frequency Vibrotactile System for Restoring Force and Stiffness Perception , 2020, IEEE Transactions on Haptics.

[133]  Spencer Kellis,et al.  A cognitive neuroprosthetic that uses cortical stimulation for somatosensory feedback , 2014, Journal of neural engineering.

[134]  K. Horch,et al.  Acute peripheral nerve recording Characteristics of polymer-based longitudinal intrafascicular electrodes , 2004, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[135]  J. Wheeler,et al.  Investigation of Rotational Skin Stretch for Proprioceptive Feedback With Application to Myoelectric Systems , 2010, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[136]  Doubler Ja,et al.  An analysis of extended physiological proprioception as a prosthesis-control technique. , 1984 .

[137]  Dustin J Tyler,et al.  The benefits of sensation on the experience of a hand: A qualitative case series , 2019, PloS one.

[138]  Srihari Y. Sritharan,et al.  Somatosensory encoding with cuneate nucleus microstimulation: Detection of artificial stimuli , 2016, 2016 38th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[139]  S. Francis,et al.  Mapping human somatosensory cortex in individual subjects with 7 T functional MRI 1 Running title : Mapping human somatosensory cortex , 2010 .

[140]  Goodwin,et al.  Differential responses in populations of fingertip tactile afferents to objects' surface curvatures. , 1999, Acta physiologica Scandinavica.

[141]  Elad Alon,et al.  Wireless Recording in the Peripheral Nervous System with Ultrasonic Neural Dust , 2016, Neuron.

[142]  R. Hallin,et al.  Peripheral Afferents With Common Function Cluster in the Median Nerve and Somatotopically Innervate the Human Palm , 1997, Brain Research Bulletin.

[143]  David J. Warren,et al.  Restoration of motor control and proprioceptive and cutaneous sensation in humans with prior upper-limb amputation via multiple Utah Slanted Electrode Arrays (USEAs) implanted in residual peripheral arm nerves , 2017, Journal of NeuroEngineering and Rehabilitation.

[144]  Daniel R Kramer,et al.  Proprioceptive and cutaneous sensations in humans elicited by intracortical microstimulation , 2018, eLife.

[145]  N. Lan,et al.  Restoring Finger-Specific Sensory Feedback for Transradial Amputees via Non-Invasive Evoked Tactile Sensation , 2020, IEEE Open Journal of Engineering in Medicine and Biology.

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

[147]  Shriya S Srinivasan,et al.  Closed-loop functional optogenetic stimulation , 2018, Nature Communications.

[148]  I Delgado-Martínez,et al.  Fascicular nerve stimulation and recording using a novel double-aisle regenerative electrode , 2017, Journal of neural engineering.

[149]  Tamar R. Makin,et al.  Stability of Sensory Topographies in Adult Cortex , 2017, Trends in Cognitive Sciences.

[150]  Xiaogang Hu,et al.  Object Shape and Surface Topology Recognition Using Tactile Feedback Evoked through Transcutaneous Nerve Stimulation , 2020, IEEE Transactions on Haptics.

[151]  Arto V. Nurmikko,et al.  Detection of Optogenetic Stimulation in Somatosensory Cortex by Non-Human Primates - Towards Artificial Tactile Sensation , 2014, PloS one.

[153]  R. Romo,et al.  Somatosensory discrimination based on cortical microstimulation , 1998, Nature.

[154]  Jonathan D. Cohen,et al.  Rubber hands ‘feel’ touch that eyes see , 1998, Nature.

[155]  F. Clippinger,et al.  A sensory feedback system for an upper-limb amputation prosthesis. , 1974, Bulletin of prosthetics research.

[156]  R. Johansson,et al.  First spikes in ensembles of human tactile afferents code complex spatial fingertip events , 2004, Nature Neuroscience.

[157]  M. Keith,et al.  Stimulation Stability and Selectivity of Chronically Implanted Multicontact Nerve Cuff Electrodes in the Human Upper Extremity , 2009, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[158]  Nitish V. Thakor,et al.  Biologically inspired multi-layered synthetic skin for tactile feedback in prosthetic limbs , 2016, 2016 38th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[159]  Silvestro Micera,et al.  Multisensory bionic limb to achieve prosthesis embodiment and reduce distorted phantom limb perceptions , 2018, Journal of Neurology, Neurosurgery, and Psychiatry.

[160]  S S Hsiao,et al.  Vibratory adaptation of cutaneous mechanoreceptive afferents. , 2005, Journal of neurophysiology.

[161]  J. Ochoa,et al.  Sensations evoked by intraneural microstimulation of single mechanoreceptor units innervating the human hand. , 1983, The Journal of physiology.

[162]  Christian Cipriani,et al.  Discrete Vibro-Tactile Feedback Prevents Object Slippage in Hand Prostheses More Intuitively Than Other Modalities , 2018, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[163]  A W Goodwin,et al.  Tactile Discrimination of Edge Shape: Limits on Spatial Resolution Imposed by Parameters of the Peripheral Neural Population , 2001, The Journal of Neuroscience.

[164]  W. Penfield,et al.  SOMATIC MOTOR AND SENSORY REPRESENTATION IN THE CEREBRAL CORTEX OF MAN AS STUDIED BY ELECTRICAL STIMULATION , 1937 .

[165]  D. Burke,et al.  Perceptual responses to microstimulation of single afferents innervating joints, muscles and skin of the human hand. , 1990, The Journal of physiology.

[166]  G. Lundborg,et al.  Sensory feedback from a prosthetic hand based on air-mediated pressure from the hand to the forearm skin. , 2012, Journal of rehabilitation medicine.

[167]  A Cutrone,et al.  Long-term usability and bio-integration of polyimide-based intra-neural stimulating electrodes. , 2017, Biomaterials.

[168]  Jeffrey G. Ojemann,et al.  Ownership of an artificial limb induced by electrical brain stimulation , 2016, Proceedings of the National Academy of Sciences.

[169]  Andrew J Fuglevand,et al.  Object discrimination using electrotactile feedback , 2018, Journal of neural engineering.

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