Sensory feedback for limb prostheses in amputees.
Journal
Nature materials
ISSN: 1476-4660
Titre abrégé: Nat Mater
Pays: England
ID NLM: 101155473
Informations de publication
Date de publication:
07 2021
07 2021
Historique:
received:
26
05
2020
accepted:
22
02
2021
pubmed:
17
4
2021
medline:
15
9
2021
entrez:
16
4
2021
Statut:
ppublish
Résumé
Commercial prosthetic devices currently do not provide natural sensory information on the interaction with objects or movements. The subsequent disadvantages include unphysiological walking with a prosthetic leg and difficulty in controlling the force exerted with a prosthetic hand, thus creating health issues. Restoring natural sensory feedback from the prosthesis to amputees is an unmet clinical need. An optimal device should be able to elicit natural sensations of touch or proprioception, by delivering the complex signals to the nervous system that would be produced by skin, muscles and joints receptors. This Review covers the various neurotechnological approaches that have been proposed for the development of the optimal sensory feedback restoration device for arm and leg amputees.
Identifiants
pubmed: 33859381
doi: 10.1038/s41563-021-00966-9
pii: 10.1038/s41563-021-00966-9
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
925-939Références
Unwin, N. Epidemiology of lower extremity amputation in centres in Europe, North America and East Asia. Br. J. Surg. 87, 328–337 (2000).
Moxey, P. W. et al. Lower extremity amputations—a review of global variability in incidence. Diabet. Med. 28, 1144–1153 (2011).
doi: 10.1111/j.1464-5491.2011.03279.x
Winkler, S. L. H. in Care of the Combat Amputee (eds Pasquina, P. F. et al.) 597–605 (Department of the Army, 2009).
Sanità solo il 5 di amputazioni è legata a infortuni sul lavoro. INAIL https://www.inail.it/cs/internet/comunicazione/news-ed-eventi/news/p1780018061_sanita_solo_il_5_di_amputazi.html (2010).
Atroshi, I. & Rosberg, H. E. Epidemiology of amputations and severe injuries of the hand. Hand Clin. 17, 343–350 (2001).
doi: 10.1016/S0749-0712(21)00515-1
Miller, W. C., Speechley, M. & Deathe, B. The prevalence and risk factors of falling and fear of falling among lower extremity amputees. Arch. Phys. Med. Rehabil. 82, 1031–1037 (2001).
doi: 10.1053/apmr.2001.24295
Nolan, L. et al. Adjustments in gait symmetry with walking speed in trans-femoral and trans-tibial amputees. Gait Posture 17, 142–151 (2003).
doi: 10.1016/S0966-6362(02)00066-8
Waters, R. L., Perry, J., Antonelli, D. & Hislop, H. Energy cost of walking of amputees: the influence of level of amputation. J. Bone Joint Surg. Am. 58, 42–46 (1976).
doi: 10.2106/00004623-197658010-00007
Biddiss, E., Beaton, D. & Chau, T. Consumer design priorities for upper limb prosthetics. Disabil. Rehabil. Assist. Technol. 2, 346–357 (2007).
doi: 10.1080/17483100701714733
Petrini, F. M. et al. Six-month assessment of a hand prosthesis with intraneural tactile feedback. Ann. Neurol. 85, 137–154 (2019).
doi: 10.1002/ana.25384
Williamson, G. M., Schulz, R., Bridges, M. W. & Behan, A. M. Social and psychological factors in adjustment to limb amputation. J. Soc. Behav. Pers. 9, 249–268 (1994).
Blanke, O. Multisensory brain mechanisms of bodily self-consciousness. Nat. Rev. Neurosci. 13, 556–571 (2012).
doi: 10.1038/nrn3292
Heller, B. W., Datta, D. & Howitt, J. A pilot study comparing the cognitive demand of walking for transfemoral amputees using the intelligent prosthesis with that using conventionally damped knees. Clin. Rehabil. 14, 518–522 (2000).
doi: 10.1191/0269215500cr345oa
Makin, T. R., de Vignemont, F. & Faisal, A. A. Neurocognitive barriers to the embodiment of technology. Nat. Biomed. Eng. 1, 0014 (2017).
doi: 10.1038/s41551-016-0014
Flor, H., Nikolajsen, L. & Staehelin Jensen, T. Phantom limb pain: a case of maladaptive CNS plasticity? Nat. Rev. Neurosci. 7, 873–881 (2006).
doi: 10.1038/nrn1991
Roffman, C. E., Buchanan, J. & Allison, G. T. Predictors of non-use of prostheses by people with lower limb amputation after discharge from rehabilitation: development and validation of clinical prediction rules. J. Physiother. 60, 224–231 (2014).
doi: 10.1016/j.jphys.2014.09.003
Torebjörk, H. E., Vallbo, A. A. B. & Ochoa, J. L. Intraneural microstimulation in man: its relation to specificity of tactile sensations. Brain 110, 1509–1529 (1987).
doi: 10.1093/brain/110.6.1509
Strzalkowski, N. D., Peters, R. M., Inglis, J. T. & Bent, L. R. Cutaneous afferent innervation of the human foot sole: what can we learn from single-unit recordings? J. Neurophysiol. 120, 1233–1246 (2018).
doi: 10.1152/jn.00848.2017
Muniak, M. A., Ray, S., Hsiao, S. S., Dammann, J. F. & Bensmaia, S. J. The neural coding of stimulus intensity: linking the population response of mechanoreceptive afferents with psychophysical behavior. J. Neurosci. 27, 11687–11699 (2007).
doi: 10.1523/JNEUROSCI.1486-07.2007
Weber, A. I. et al. Spatial and temporal codes mediate the tactile perception of natural textures. Proc. Natl Acad. Sci. USA 110, 17107–17112 (2013).
doi: 10.1073/pnas.1305509110
Johansson, R. S. & Birznieks, I. First spikes in ensembles of human tactile afferents code complex spatial fingertip events. Nat. Neurosci. 7, 170–177 (2004).
doi: 10.1038/nn1177
Proske, U. & Gandevia, S. C. The proprioceptive senses: their roles in signaling body shape, body position and movement, and muscle force. Physiol. Rev. 92, 1651–1697 (2012).
doi: 10.1152/physrev.00048.2011
Macefield, G., Gandevia, S. C. & Burke, D. Perceptual responses to microstimulation of single afferents innervating joints, muscles and skin of the human hand. J. Physiol. 429, 113–129 (1990).
doi: 10.1113/jphysiol.1990.sp018247
Rusaw, D., Hagberg, K., Nolan, L. & Ramstrand, N. Can vibratory feedback be used to improve postural stability in persons with transtibial limb loss? J. Rehabil. Res. Dev. 49, 1239–1254 (2012).
doi: 10.1682/JRRD.2011.05.0088
Dietrich, C. et al. Leg prosthesis with somatosensory feedback reduces phantom limb pain and increases functionality. Front. Neurol. 9, 270 (2018).
doi: 10.3389/fneur.2018.00270
Shannon, G. F. A myoelectrically-controlled prosthesis with sensory feedback. Med. Biol. Eng. Comput. 17, 73–80 (1979).
doi: 10.1007/BF02440956
Prior, R. E. Supplemental sensory feedback for the VA/NU myoelectric hand background and preliminary designs. Bull. Prosthet. Res. 22, 170–91 (1976).
Dosen, S., Schaeffer, M.-C. & Farina, D. Time-division multiplexing for myoelectric closed-loop control using electrotactile feedback. J. Neuroeng. Rehabil. 11, 138 (2014).
Naples, G. G., Mortimer, J. T., Scheiner, A. & Sweeney, J. D. A spiral nerve cuff electrode for peripheral nerve stimulation. IEEE Trans. Biomed. Eng. 35, 905–916 (1988).
doi: 10.1109/10.8670
Tyler, D. J. & Durand, D. M. Functionally selective peripheral nerve stimulation with a flat interface nerve electrode. IEEE Trans. Neural Syst. Rehabil. Eng. 10, 294–303 (2002).
doi: 10.1109/TNSRE.2002.806840
McNaughton, T. G. & Horch, K. W. Metallized polymer fibers as leadwires and intrafascicular microelectrodes. J. Neurosci. Methods 70, 103–107 (1996).
doi: 10.1016/S0165-0270(96)00111-2
Poppendieck, W. et al. A new generation of double-sided intramuscular electrodes for multi-channel recording and stimulation. In 2015 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC) 7135–7138 (IEEE, 2015).
Wark, H. A. C. et al. A new high-density (25 electrodes/mm
doi: 10.1088/1741-2560/10/4/045003
Boretius, T. et al. A transverse intrafascicular multichannel electrode (TIME) to interface with the peripheral nerve. Biosens. Bioelectron. 26, 62–69 (2010).
doi: 10.1016/j.bios.2010.05.010
Hassler, C., Boretius, T. & Stieglitz, T. Polymers for neural implants. J. Polym. Sci. B 49, 18–33 (2011).
doi: 10.1002/polb.22169
Ordonez, J., Schuettler, M., Boehler, C., Boretius, T. & Stieglitz, T. Thin films and microelectrode arrays for neuroprosthetics. MRS Bull. 37, 590–598 (2012).
doi: 10.1557/mrs.2012.117
Ortiz-Catalan, M., Mastinu, E., Sassu, P., Aszmann, O. & Brånemark, R. Self-contained neuromusculoskeletal arm prostheses. N. Engl. J. Med. 382, 1732–1738 (2020).
doi: 10.1056/NEJMoa1917537
Badia, J., Pascual-Font, A., Vivó, M., Udina, E. & Navarro, X. Topographical distribution of motor fascicles in the sciatic-tibial nerve of the rat. Muscle Nerve 42, 192–201 (2010).
doi: 10.1002/mus.21652
Freeberg, M. J., Stone, M. A., Triolo, R. J. & Tyler, D. J. The design of and chronic tissue response to a composite nerve electrode with patterned stiffness. J. Neural Eng. 14, 036022 (2017).
doi: 10.1088/1741-2552/aa6632
Lawrence, S. M., Dhillon, G. S. & Horch, K. W. Fabrication and characteristics of an implantable, polymer-based, intrafascicular electrode. J. Neurosci. Methods 131, 9–26 (2003).
doi: 10.1016/S0165-0270(03)00231-0
Overstreet, C. K., Cheng, J. & Keefer, E. Fascicle specific targeting for selective peripheral nerve stimulation. J. Neural Eng. https://doi.org/10.1088/1741-2552/ab4370 (2019).
Wurth, S. et al. Long-term usability and bio-integration of polyimide-based intra-neural stimulating electrodes. Biomaterials 122, 114–129 (2017).
doi: 10.1016/j.biomaterials.2017.01.014
Merrill, D. R., Bikson, M. & Jefferys, J. G. Electrical stimulation of excitable tissue: design of efficacious and safe protocols. J. Neurosci. Methods 141, 171–198 (2005).
doi: 10.1016/j.jneumeth.2004.10.020
Cogan, S. F. Neural stimulation and recording electrodes. Annu. Rev. Biomed. Eng. 10, 275–309 (2008).
doi: 10.1146/annurev.bioeng.10.061807.160518
Rossini, P. M. et al. Double nerve intraneural interface implant on a human amputee for robotic hand control. Clin. Neurophysiol. 121, 777–783 (2010).
doi: 10.1016/j.clinph.2010.01.001
Boretius, T. et al. A transverse intrafascicular multichannel electrode (TIME) to treat phantom limb pain—towards human clinical trials. In 2012 4th IEEE RAS & EMBS International Conference on Biomedical Robotics and Biomechatronics (BioRob) 282–287 (IEEE, 2012).
Rose, T. L. & Robblee, L. S. Electrical stimulation with Pt electrodes. VIII. Electrochemically safe charge injection limits with 0.2 ms pulses (neuronal application). IEEE Trans. Biomed. Eng. 37, 1118–1120 (1990).
doi: 10.1109/10.61038
Cogan, S. F. et al. Sputtered iridium oxide films for neural stimulation electrodes. J. Biomed. Mater. Res. B 89, 353–361 (2009).
doi: 10.1002/jbm.b.31223
Grill, W. M. & Mortimer, J. T. Neural and connective tissue response to long-term implantation of multiple contact nerve cuff electrodes. J. Biomed. Mater. Res. 50, 215–226 (2000).
doi: 10.1002/(SICI)1097-4636(200005)50:2<215::AID-JBM17>3.0.CO;2-A
Polasek, K. H., Hoyen, H. A., Keith, M. W., Kirsch, R. F. & Tyler, D. J. Stimulation stability and selectivity of chronically implanted multicontact nerve cuff electrodes in the human upper extremity. IEEE Trans. Neural Syst. Rehabil. Eng. 17, 428–437 (2009).
doi: 10.1109/TNSRE.2009.2032603
Tyler, D. J. & Durand, D. M. Chronic response of the rat sciatic nerve to the flat interface nerve electrode. Ann. Biomed. Eng. 31, 633–642 (2003).
doi: 10.1114/1.1569263
Leventhal, D. K., Cohen, M. & Durand, D. M. Chronic histological effects of the flat interface nerve electrode. J. Neural Eng. 3, 102 (2006).
doi: 10.1088/1741-2560/3/2/004
Tan, D. W. et al. A neural interface provides long-term stable natural touch perception. Sci. Transl. Med. 6, 257ra138 (2014).
doi: 10.1126/scitranslmed.3008669
Lago, N., Yoshida, K., Koch, K. P. & Navarro, X. Assessment of biocompatibility of chronically implanted polyimide and platinum intrafascicular electrodes. IEEE Trans. Biomed. Eng. 54, 281–290 (2007).
doi: 10.1109/TBME.2006.886617
Badia, J. et al. Biocompatibility of chronically implanted transverse intrafascicular multichannel electrode (TIME) in the rat sciatic nerve. IEEE Trans. Biomed. Eng. 58, 2324–2332 (2011).
doi: 10.1109/TBME.2011.2153850
Branner, A., Stein, R. B., Fernandez, E., Aoyagi, Y. & Normann, R. A. Long-term stimulation and recording with a penetrating microelectrode array in cat sciatic nerve. IEEE Trans. Biomed. Eng. 51, 146–157 (2004).
doi: 10.1109/TBME.2003.820321
Christensen, M. B., Wark, H. A. & Hutchinson, D. T. A histological analysis of human median and ulnar nerves following implantation of Utah slanted electrode arrays. Biomaterials 77, 235–242 (2016).
doi: 10.1016/j.biomaterials.2015.11.012
Schady, W., Braune, S., Watson, S., Torebjörk, H. E. & Schmidt, R. Responsiveness of the somatosensory system after nerve injury and amputation in the human hand. Ann. Neurol. 36, 68–75 (1994).
doi: 10.1002/ana.410360114
Clippinger, F. W., Avery, R. & Titus, B. R. A sensory feedback system for an upper-limb amputation prosthesis. Bull. Prosthet. Res. 10, 247–258 (1974).
Clippinger, F. W., Seaber, A. V., McElhaney, J. H., Harrelson, J. M. & Maxwell, G. M. Afferent sensory feedback for lower extremity prosthesis. Clin. Orthop. Relat. Res. 169, 202–206 (1982).
Dhillon, G. S., Lawrence, S. M., Hutchinson, D. T. & Horch, K. W. Residual function in peripheral nerve stumps of amputees: implications for neural control of artificial limbs. J. Hand Surg. Am. 29, 605–615 (2004).
Dhillon, G. S. & Horch, K. W. Direct neural sensory feedback and control of a prosthetic arm. IEEE Trans. Neural Syst. Rehabil. Eng. 13, 468–472 (2005).
doi: 10.1109/TNSRE.2005.856072
Valle, G. et al. Comparison of linear frequency and amplitude modulation for intraneural sensory feedback in bidirectional hand prostheses. Sci. Rep. 8, 16666 (2018).
doi: 10.1038/s41598-018-34910-w
Raspopovic, S. et al. Restoring natural sensory feedback in real-time bidirectional hand prostheses. Sci. Transl. Med. 6, 222ra19 (2014).
doi: 10.1126/scitranslmed.3006820
Valle, G. et al. Biomimetic intraneural sensory feedback enhances sensation naturalness, tactile sensitivity, and manual dexterity in a bidirectional prosthesis. Neuron https://doi.org/10.1016/j.neuron.2018.08.033 (2018).
George, J. A. et al. Biomimetic sensory feedback through peripheral nerve stimulation improves dexterous use of a bionic hand. Sci. Robot. 4, eaax2352 (2019).
doi: 10.1126/scirobotics.aax2352
Horch, K., Meek, S., Taylor, T. G. & Hutchinson, D. T. Object discrimination with an artificial hand using electrical stimulation of peripheral tactile and proprioceptive pathways with intrafascicular electrodes. IEEE Trans. Neural Syst. Rehabil. Eng. 19, 483–489 (2011).
doi: 10.1109/TNSRE.2011.2162635
Zollo, L. et al. Restoring tactile sensations via neural interfaces for real-time force-and-slippage closed-loop control of bionic hands. Sci. Robot. 4, eaau9924 (2019).
doi: 10.1126/scirobotics.aau9924
Ortiz-Catalan, M., Hakansson, B. & Branemark, R. An osseointegrated human-machine gateway for long-term sensory feedback and motor control of artificial limbs. Sci. Transl. Med. 6, 257re6 (2014).
doi: 10.1126/scitranslmed.3008933
Oddo, C. M. et al. Intraneural stimulation elicits discrimination of textural features by artificial fingertip in intact and amputee humans. eLife 5, e09148 (2016).
Davis, T. S. et al. Restoring motor control and sensory feedback in people with upper extremity amputations using arrays of 96 microelectrodes implanted in the median and ulnar nerves. J. Neural Eng. 13, 036001 (2016).
doi: 10.1088/1741-2560/13/3/036001
Wendelken, S. 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. J. Neuroeng. Rehabil. 14, 121 (2017).
doi: 10.1186/s12984-017-0320-4
Rognini, G. et al. Multisensory bionic limb to achieve prosthesis embodiment and reduce distorted phantom limb perceptions. J. Neurol. Neurosurg. Psychiatry 90, 833–836 (2019).
doi: 10.1136/jnnp-2018-318570
Segil, J. L., Cuberovic, I., Graczyk, E. L., Weir, R. F. ff. & Tyler, D. Combination of simultaneous artificial sensory percepts to identify prosthetic hand postures: a case study. Sci. Rep. 10, 6576 (2020).
Graczyk, E. L., Resnik, L., Schiefer, M. A., Schmitt, M. S. & Tyler, D. J. Home use of a neural-connected sensory prosthesis provides the functional and psychosocial experience of having a hand again. Sci. Rep. 8, 9866 (2018).
doi: 10.1038/s41598-018-26952-x
Tan, D. W., Schiefer, M. A., Keith, M. W., Anderson, J. R. & Tyler, D. J. Stability and selectivity of a chronic, multi-contact cuff electrode for sensory stimulation in human amputees. J. Neural Eng. 12, 026002 (2015).
doi: 10.1088/1741-2560/12/2/026002
Kuiken, T. A. et al. Targeted muscle reinnervation for real-time myoelectric control of multifunction artificial arms. JAMA 301, 619–628 (2009).
doi: 10.1001/jama.2009.116
Kuiken, T. A. et al. Targeted reinnervation for enhanced prosthetic arm function in a woman with a proximal amputation: a case study. Lancet 369, 371–380 (2007).
doi: 10.1016/S0140-6736(07)60193-7
Kuiken, T. A., Marasco, P. D., Lock, B. A., Harden, R. N. & Dewald, J. P. A. Redirection of cutaneous sensation from the hand to the chest skin of human amputees with targeted reinnervation. Proc. Natl Acad. Sci. USA 104, 20061–20066 (2007).
doi: 10.1073/pnas.0706525104
Schofield, J. S., Shell, C. E., Beckler, D. T., Thumser, Z. C. & Marasco, P. D. Long-term home-use of sensory-motor-integrated bidirectional bionic prosthetic arms promotes functional, perceptual, and cognitive changes. Front Neurosci. 14, 120 (2020).
doi: 10.3389/fnins.2020.00120
Osborn, L., Betthauser, J., Kaliki, R. & Thakor, N. Live demonstration: targeted transcutaneous electrical nerve stimulation for phantom limb sensory feedback. In 2017 IEEE Biomedical Circuits and Systems Conference (BioCAS) 1-1 (IEEE, 2017); https://doi.org/10.1109/BIOCAS.2017.8325101
Charkhkar, H. et al. High-density peripheral nerve cuffs restore natural sensation to individuals with lower-limb amputations. J. Neural Eng. 15, 056002 (2018).
doi: 10.1088/1741-2552/aac964
Petrini, F. M. et al. Sensory feedback restoration in leg amputees improves walking speed, metabolic cost and phantom pain. Nat. Med. 25, 1356–1363 (2019).
doi: 10.1038/s41591-019-0567-3
Petrini, F. M. et al. Enhancing functional abilities and cognitive integration of the lower limb prosthesis. Sci. Transl. Med. 11, eaav8939 (2019).
doi: 10.1126/scitranslmed.aav8939
Mundell, B. F. et al. The risk of major cardiovascular events for adults with transfemoral amputation. J. Neuroeng. Rehabil. 15, 58 (2018).
doi: 10.1186/s12984-018-0400-0
Clites, T. R. et al. Proprioception from a neurally controlled lower-extremity prosthesis. Sci. Transl. Med. 10, eaap8373 (2018).
doi: 10.1126/scitranslmed.aap8373
Johansson, R. S. & Flanagan, J. R. Coding and use of tactile signals from the fingertips in object manipulation tasks. Nat. Rev. Neurosci. 10, 345–359 (2009).
doi: 10.1038/nrn2621
Marasco, P. D. et al. Illusory movement perception improves motor control for prosthetic hands. Sci. Transl. Med. 10, eaao6990 (2018).
doi: 10.1126/scitranslmed.aao6990
Gandevia, S. C. Illusory movements produced by electrical stimulation of low-threshold muscle afferents from the hand. Brain 108, 965–981 (1985).
doi: 10.1093/brain/108.4.965
Ekedahl, R., Frank, O. & Hallin, R. G. Peripheral afferents with common function cluster in the median nerve and somatotopically innervate the human palm. Brain Res. Bull. 42, 367–376 (1997).
doi: 10.1016/S0361-9230(96)00324-3
Hagbarth, K. E., Wallen, G. & Löfstedt, L. Muscle spindle activity in man during voluntary fast alternating movements. J. Neurol. Neurosurg. Psychiatry 38, 625–635 (1975).
doi: 10.1136/jnnp.38.7.625
Stewart, J. D. Peripheral nerve fascicles: anatomy and clinical relevance. Muscle Nerve 28, 525–541 (2003).
doi: 10.1002/mus.10454
D’Anna, E. et al. A closed-loop hand prosthesis with simultaneous intraneural tactile and position feedback. Sci. Robot. 4, eaau8892 (2019).
doi: 10.1126/scirobotics.aau8892
de la Oliva, N., Mueller, M., Stieglitz, T., Navarro, X. & del Valle, J. On the use of parylene C polymer as substrate for peripheral nerve electrodes. Sci. Rep. 8, 5965 (2018).
Preatoni, G., Valle, G., Petrini, F. M. & Raspopovic, S. Lightening the perceived prosthesis weight with neural embodiment promoted by sensory feedback. Curr. Biol. 31, 1065–1071 (2021).
Gerratt, A. P., Michaud, H. O. & Lacour, S. P. Elastomeric electronic skin for prosthetic tactile sensation. Adv. Funct. Mater. 25, 2287–2295 (2015).
doi: 10.1002/adfm.201404365
Hua, Q. et al. Skin-inspired highly stretchable and conformable matrix networks for multifunctional sensing. Nat. Commun. 9, 244 (2018).
doi: 10.1038/s41467-017-02685-9
Lee, W. W. et al. A neuro-inspired artificial peripheral nervous system for scalable electronic skins. Sci. Robot. 4, eaax2198 (2019).
doi: 10.1126/scirobotics.aax2198
Saal, H. P. & Bensmaia, S. J. Biomimetic approaches to bionic touch through a peripheral nerve interface. Neuropsychologia 79, 344–353 (2015).
doi: 10.1016/j.neuropsychologia.2015.06.010
Kim, L. H., McLeod, R. S. & Kiss, Z. H. A new psychometric questionnaire for reporting of somatosensory percepts. J. Neural Eng. 15, 013002 (2018).
doi: 10.1088/1741-2552/aa966a
Hafner, B. J. & Smith, D. G. Differences in function and safety between Medicare functional classification level-2 and-3 transfemoral amputees and influence of prosthetic knee joint control. J. Rehabil. Res. Dev. 46, 417–433 (2009).
doi: 10.1682/JRRD.2008.01.0007
Navarro, X. et al. A critical review of interfaces with the peripheral nervous system for the control of neuroprostheses and hybrid bionic systems. J. Peripher. Nerv. Syst. 10, 229–258 (2005).
doi: 10.1111/j.1085-9489.2005.10303.x
Ochoa, J. & Torebjörk, E. Sensations evoked by intraneural microstimulation of single mechanoreceptor units innervating the human hand. J. Physiol. 342, 633–654 (1983).
doi: 10.1113/jphysiol.1983.sp014873
Zelechowski, M., Valle, G. & Raspopovic, S. A computational model to design neural interfaces for lower-limb sensory neuroprostheses. J. Neuroeng. Rehabil. 17, 24 (2020).
Raspopovic, S. Advancing limb neural prostheses. Science 370, 290–291 (2020).
doi: 10.1126/science.abb1073
Llewellyn, M. E., Thompson, K. R., Deisseroth, K. & Delp, S. L. Orderly recruitment of motor units under optical control in vivo. Nat. Med. 16, 1161–1165 (2010).
doi: 10.1038/nm.2228
Someya, T., Bao, Z. & Malliaras, G. G. The rise of plastic bioelectronics. Nature 540, 379–385 (2016).
doi: 10.1038/nature21004
Piech, D. K. et al. A wireless millimetre-scale implantable neural stimulator with ultrasonically powered bidirectional communication. Nat. Biomed. Eng. 4, 207–222 (2020).
doi: 10.1038/s41551-020-0518-9
Abraira, V. E. & Ginty, D. D. The sensory neurons of touch. Neuron 79, 618–639 (2013).
doi: 10.1016/j.neuron.2013.07.051
Johansson, R. S. & Flanagan, J. R. in The Senses: A Comprehensive Reference 67–86 (Academic Press, 2008).
Johansson, R. S. & Vallbo, A. B. Tactile sensibility in the human hand: relative and absolute densities of four types of mechanoreceptive units in glabrous skin. J. Physiol. 286, 283–300 (1979).
doi: 10.1113/jphysiol.1979.sp012619
Johansson, R. S. & Vallbo, Å. B. Tactile sensory coding in the glabrous skin of the human hand. Trends Neurosci. 6, 27–32 (1983).
Yildiz, K. A., Shin, A. Y. & Kaufman, K. R. Interfaces with the peripheral nervous system for the control of a neuroprosthetic limb: a review. J. Neuroeng. Rehabil. 17, 43 (2020).
doi: 10.1186/s12984-020-00667-5
Benvenuto, A. et al. Intrafascicular thin-film multichannel electrodes for sensory feedback: evidences on a human amputee. In 2010 Annual International Conference of the IEEE Engineering in Medicine and Biology 1800–1803 (IEEE, 2010).
Negi, S., Bhandari, R., Rieth, L. & Solzbacher, F. In vitro comparison of sputtered iridium oxide and platinum-coated neural implantable microelectrode arrays. Biomed. Mater. 5, 15007 (2010).
doi: 10.1088/1748-6041/5/1/015007
Badia, J. et al. in Direct Nerve Stimulation for Induction of Sensation and Treatment of Phantom Limb Pain 155–169 (River Publishers, 2019).
Graczyk, E. L., Delhaye, B. P., Schiefer, M. A., Bensmaia, S. J. & Tyler, D. J. Sensory adaptation to electrical stimulation of the somatosensory nerves. J. Neural Eng. 15, 046002 (2018).
doi: 10.1088/1741-2552/aab790
Strauss, I. et al. Characterization of multi-channel intraneural stimulation in transradial amputees. Sci. Rep. 9, 9258 (2019).
Kluger, D. T. et al. Virtual reality provides an effective platform for functional evaluations of closed-loop neuromyoelectric control. IEEE Trans. Neural Syst. Rehabil. Eng. 27, 876–886 (2019).
doi: 10.1109/TNSRE.2019.2908817