Interfacing the Somatosensory System to Restore Touch and Proprioception: Essential Considerations

Weber, Douglas J.; Friesen, Rebecca; Miller, Lee E.

doi:10.1080/00222895.2012.735283

Cited by 98Neuroscience and Neural EngineeringTactile and Sensory InteractionsEEG and Brain-Computer Interfaces

Interfacing the Somatosensory System to Restore Touch and Proprioception: Essential Considerations

Weber, Douglas J., Friesen, Rebecca, Miller, Lee E.·2012·Journal of Motor Behavior

DOI 10.1080/00222895.2012.735283

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Abstract

State-of-the-art upper extremity prostheses include anthropomorphic hands with dexterity that approximates that of a human. To be fully useful, these devices will require an advanced somatosensory neural interface to convey tactile and proprioceptive feedback to the user. To this end, microstimulation methods are being developed using microelectrode arrays implanted at various locations along the somatosensory neuraxis, from peripheral nerves to primary somatosensory cortex. There is presently no consensus as to the best approach, although results from animal and human studies lend support for each. The purpose of this review is to outline practical considerations for the design of a somatosensory interface based on present knowledge of the anatomy and physiology, prior attempts to elicit somatic sensations using electrical stimulation, and lessons learned from successful sensory neuroprostheses such as the cochlear implant.

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Previous reviews have highlighted that physiological differences between the brain and peripheral nerves explain the differences in the range of electrical stimulation parameters used in both situations.
“Previous reviews have highlighted that physiological differences between the brain and peripheral nerves explain the differences in the range of electrical stimulation parameters used in both situations [25, 101].”
From Safety of long-term electrical peripheral nerve stimulation: review of the state of the art (2019) · cites this paper as [101]

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Chronic Response of the Rat Sciatic Nerve to the Flat Interface Nerve Electrode
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“FINEs have been tested chronically in rodent (Tyler & Durand, 2003) and feline studies (Leventhal & Durand, 2004).”
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Responses of neurones in motor cortex and in area 3A to controlled stretches of forelimb muscles in cebus monkeys.
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Cochlear Nucleus Implant
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Selective stimulation of the human femoral nerve with a flat interface nerve electrode
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A continuum mechanical model of mechanoreceptive afferent responses to indented spatial patterns
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Electrical Stimulation of the Proprioceptive Cortex (Area 3a) Used to Instruct a Behaving Monkey
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An autonomous implantable computer for neural recording and stimulation in unrestrained primates
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Human motor cortical activity recorded with Micro-ECoG electrodes, during individual finger movements
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Organization of area 3a in macaque monkeys: Contributions to the cortical phenotype
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Sensory capacity of reinnervated skin after redirection of amputated upper limb nerves to the chest
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Systematic assessment of training-induced changes in corticospinal output to hand using frameless stereotaxic transcranial magnetic stimulation
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Intraspinal Microstimulation Excites Multisegmental Sensory Afferents at Lower Stimulus Levels Than Local α-Motoneuron Responses
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Clinical Applications of Electrical Stimulation After Spinal Cord Injury
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Limb-State Information Encoded by Peripheral and Central Somatosensory Neurons: Implications for an Afferent Interface
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Mathematical Models of Proprioceptors. II. Structure and Function of the Golgi Tendon Organ
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Motor deficits in patients with large-fiber sensory neuropathy.
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Functional role of muscle reflexes for force generation in the decerebrate walking cat
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Functional role of the sensory cortex in learning motor skills in cats
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Motor performance of monkeys after bilateral partial and total cerebral decortications.
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The visual sensations produced by electrical stimulation of the medial occipital cortex.
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Limb-state feedback from ensembles of simultaneously recorded dorsal root ganglion neurons
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Proprioceptive and Cutaneous Representations in the Rat Ventral Posterolateral Thalamus
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Coding of position by simultaneously recorded sensory neurones in the cat dorsal root ganglion
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Neural Mechanisms of Tactile Motion Integration in Somatosensory Cortex
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A Prosthesis for the Deaf Based on Cortical Stimulation
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Cochlear Prosthetics
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Primary motor cortical responses to perturbations of prehension in the monkey
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Human neocortical electrical activity recorded on nonpenetrating microwire arrays: applicability for neuroprostheses
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Accessing the tonotopic organization of the ventral cochlear nucleus by intranuclear microstimulation
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Predicting the timing of spikes evoked by tactile stimulation of the hand
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Microstimulation in auditory cortex provides a substrate for detailed behaviors
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Medial Lateral Extent of Thermal and Pain Sensations Evoked By Microstimulation in Somatic Sensory Nuclei of Human Thalamus
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Intrafascicular stimulation of monkey arm nerves evokes coordinated grasp and sensory responses
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Responses of isolated Golgi tendon organs of the cat.
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Active sensing of target location encoded by cortical microstimulation
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Reference Frames for Spinal Proprioception: Kinematics Based or Kinetics Based?
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Microstimulation in the Region of the Human Thalamic Principal Somatic Sensory Nucleus Evokes Sensations Like Those of Mechanical Stimulation and Movement
Ohara, S., Weiss, N., & Lenz, F. A. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00648.2003 · Cited by 59 · see citing works
Neural interfaces for regenerated nerve stimulation and recording
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Sensory correlates of somatic afferent fibre activation.
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Chronic Measurement of the Stimulation Selectivity of the Flat Interface Nerve Electrode
Leventhal, D. K., & Durand, D. M. (2004) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2004.827535 · Cited by 55 · see citing works
Selective motor unit recruitment via intrafascicular multielectrode stimulation
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Microstimulation of primary afferent neurons in the L7 dorsal root ganglia using multielectrode arrays in anesthetized cats: thresholds and recruitment properties
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Cortical microstimulation in auditory cortex of rat elicits best-frequency dependent behaviors
Otto, K. J., Rousche, P. J., & Kipke, D. R. (2005) · Journal of Neural Engineering · doi:10.1088/1741-2560/2/2/005 · Cited by 53 · see citing works
Designing a somatosensory neural prosthesis: percepts evoked by different patterns of thalamic stimulation
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Selective Activation and Graded Recruitment of Functional Muscle Groups through Spinal Cord Stimulation
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Principles of Neural Science, 3rd edition
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Single electrode micro-stimulation of rat auditory cortex: an evaluation of behavioral performance
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Asymmetric Versus Symmetric Pulses for Cortical Microstimulation
Koivuniemi, A. S., & Otto, K. J. (2011) · IEEE Transactions on Neural Systems and Rehabilitation Engineering · doi:10.1109/tnsre.2011.2166563 · Cited by 43 · see citing works
Modality-Specific Axonal Regeneration: Toward Selective Regenerative Neural Interfaces
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Coordinated, multi-joint, fatigue-resistant feline stance produced with intrafascicular hind limb nerve stimulation
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Psychophysical Elements of Place and Modality Specificity in the Thalamic Somatic Sensory Nucleus (Ventral Caudal, Vc) of Awake Humans
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Designing a Thalamic Somatosensory Neural Prosthesis: Consistency and Persistence of Percepts Evoked by Electrical Stimulation
Heming, E. A., Choo, R., Davies, J. N., & Kiss, Z. H. T. (2011) · IEEE Transactions on Neural Systems and Rehabilitation Engineering · doi:10.1109/tnsre.2011.2152858 · Cited by 29 · see citing works
State-space decoding of primary afferent neuron firing rates
Wagenaar, J., Ventura, V., & Weber, D. J. (2011) · Journal of Neural Engineering · doi:10.1088/1741-2560/8/1/016002 · Cited by 28 · see citing works
Self-citation
Typology, early differentiation, and exuberant growth of a set of cortical axons
Bressoud, R., & Innocenti, G. M. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19990329)406:1 · Cited by 27 · see citing works
Neural Feedback for Instantaneous Spatiotemporal Modulation of Afferent Pathways in Bi-Directional Brain–Machine Interfaces
Liu, J., Khalil, H. K., & Oweiss, K. G. (2011) · IEEE Transactions on Neural Systems and Rehabilitation Engineering · doi:10.1109/tnsre.2011.2162003 · Cited by 26 · see citing works
A computational model for estimating recruitment of primary afferent fibers by intraneural stimulation in the dorsal root ganglia
Bourbeau, D. J., Hokanson, J., Rubin, J. E., & Weber, D. J. (2011) · Journal of Neural Engineering · doi:10.1088/1741-2560/8/5/056009 · Cited by 23 · see citing works
Self-citation
Temporal excitation properties of paresthesias evoked by thalamic microstimulation
Grill, W. M., Simmons, A. M., Cooper, S. E., Miocinovic, S., Montgomery, E. B., Baker, K. B., & Rezai, A. R. (2005) · Clinical Neurophysiology · doi:10.1016/j.clinph.2004.12.020 · Cited by 23 · see citing works
Accessing Ampli-Tonotopic Organization of Rat Auditory Cortex by Microstimulation of Cochlear Nucleus
Takahashi, H., Nakao, M., & Kaga, K. (2005) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2005.847554 · Cited by 22 · see citing works
An Animal Model of Auditory Cortex Prostheses
Scheich, H., & Breindl, A. (2002) · Audiology and Neurotology · doi:10.1159/000058309 · Cited by 18 · see citing works
Guest Editorial Brain Training: Cortical Plasticity and Afferent Feedback in Brain-Machine Interface Systems
Miller, L. E., & Weber, D. J. (2011) · IEEE Transactions on Neural Systems and Rehabilitation Engineering · doi:10.1109/tnsre.2011.2168989 · Cited by 11 · see citing works
Self-citation
The Somatosensory System
Hendry, S. H. C., & Hsiao, S. S. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-385870-2.00024-x · Cited by 10 · see citing works
A Wideband Wireless Neural Stimulation Platform for High-Density Microelectrode Arrays
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Chronic microstimulation of cat auditory cortex effective to evoke detection behaviors
Wang, J., Liu, Y., Qin, L., Chimoto, S., Nakamoto, K. T., & Sato, Y. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.01.012 · Cited by 5 · see citing works

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Pursuing prosthetic electronic skin
Chortos, A., Liu, J., & Bao, Z. (2016) · Nature Materials · doi:10.1038/nmat4671 · Cited by 2,396 · see citing works
Intracortical microstimulation of human somatosensory cortex
Flesher, S. N., Collinger, J. L., Foldes, S. T., Weiss, J. M., Downey, J. E., Tyler-Kabara, E. C., Bensmaia, S. J., Schwartz, A. B., Boninger, M. L., & Gaunt, R. A. (2016) · Science Translational Medicine · doi:10.1126/scitranslmed.aaf8083 · Cited by 704 · see citing works
An osseointegrated human-machine gateway for long-term sensory feedback and motor control of artificial limbs
Ortiz-Catalan, M., Håkansson, B., & Brånemark, R. (2014) · Science Translational Medicine · doi:10.1126/scitranslmed.3008933 · Cited by 484 · see citing works
Safety of long-term electrical peripheral nerve stimulation: review of the state of the art
Günter, C., Delbeke, J., & Ortiz-Catalan, M. (2019) · Journal of NeuroEngineering and Rehabilitation · doi:10.1186/s12984-018-0474-8 · Cited by 198 · see citing works
A learning-based approach to artificial sensory feedback leads to optimal integration
Dadarlat, M. C., O'Doherty, J. E., & Sabes, P. N. (2015) · Nature Neuroscience · doi:10.1038/nn.3883 · Cited by 210 · see citing works
Biomimetic approaches to bionic touch through a peripheral nerve interface
Saal, H. P., & Bensmaia, S. J. (2015) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2015.06.010 · Cited by 179 · see citing works
Beyond the brain: Optogenetic control in the spinal cord and peripheral nervous system
Montgomery, K. L., Iyer, S. M., Christensen, A. J., Deisseroth, K., & Delp, S. L. (2016) · Science Translational Medicine · doi:10.1126/scitranslmed.aad7577 · Cited by 147 · see citing works
Neuromorphic hardware for somatosensory neuroprostheses
Donati, E., & Valle, G. (2024) · Nature Communications · doi:10.1038/s41467-024-44723-3 · Cited by 115 · see citing works
Design of a Closed-Loop, Bidirectional Brain Machine Interface System With Energy Efficient Neural Feature Extraction and PID Control
Liu, X., Zhang, M., Richardson, A. G., Lucas, T. H., & der Spiegel, J. V. (2016) · IEEE Transactions on Biomedical Circuits and Systems · doi:10.1109/tbcas.2016.2622738 · Cited by 109 · see citing works
Neural interfaces for somatosensory feedback: bringing life to a prosthesis
Tyler, D. J. (2015) · Current Opinion in Neurology · doi:10.1097/wco.0000000000000266 · Cited by 105 · see citing works
Neural stimulation and recording performance in human sensorimotor cortex over 1500 days
Hughes, C. L., Flesher, S. N., Weiss, J. M., Downey, J. E., Boninger, M. L., Collinger, J. L., & Gaunt, R. A. (2021) · Journal of Neural Engineering · doi:10.1088/1741-2552/ac18ad · Cited by 93 · see citing works
Selectivity and Longevity of Peripheral-Nerve and Machine Interfaces: A Review.
Ghafoor, U., Kim, S., & Hong, K.-S. (2017) · Frontiers in Neurorobotics · doi:10.3389/fnbot.2017.00059 · Cited by 88 · see citing works
“There are several locations at which the interaction with the residual somatosensory system can be established (Weber et al., 2012).”
Direct Electrical Stimulation in Electrocorticographic Brain–Computer Interfaces: Enabling Technologies for Input to Cortex
Caldwell, D. J., Ojemann, J. G., & Rao, R. P. N. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00804 · Cited by 81 · see citing works
Dynamic causal modeling of touch-evoked potentials in the rubber hand illusion
Zeller, D., Friston, K. J., & Claßen, J. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2016.05.065 · Cited by 74 · see citing works
Bioinspired Prosthetic Interfaces
Li, P., Ali, H. P. A., Cheng, W. M., Yang, J., & Tee, B. C. K. (2020) · Advanced Materials Technologies · doi:10.1002/admt.201900856 · Cited by 75 · see citing works
An Artificial Olfactory System Based on a Chemi‐Memristive Device
Chun, S. Y., Song, Y. G., Kim, J. E., Kwon, J. U., Soh, K., Kwon, J. Y., Kang, C., & Yoon, J. H. (2023) · Advanced Materials · doi:10.1002/adma.202302219 · Cited by 68 · see citing works
Auditory midbrain implant: Research and development towards a second clinical trial
Lim, H. H., & Lenarz, T. (2015) · Hearing Research · doi:10.1016/j.heares.2015.01.006 · Cited by 65 · see citing works
Autonomy in Rehabilitation Robotics: An Intersection
Argall, B. (2018) · Annual Review of Control Robotics and Autonomous Systems · doi:10.1146/annurev-control-061417-041727 · Cited by 63 · see citing works
Implantable Neural Interfaces and Wearable Tactile Systems for Bidirectional Neuroprosthetics Systems
Cutrone, A., & Micera, S. (2019) · Advanced Healthcare Materials · doi:10.1002/adhm.201801345 · Cited by 57 · see citing works
Artifact-free recordings in human bidirectional brain–computer interfaces
Weiss, J. M., Flesher, S. N., Franklin, R. K., Collinger, J. L., & Gaunt, R. A. (2018) · Journal of Neural Engineering · doi:10.1088/1741-2552/aae748 · Cited by 55 · see citing works
Anatomical correlates of proprioceptive impairments following acute stroke: A case series
Kenzie, J. M., Semrau, J. A., Findlater, S. E., Herter, T. M., Hill, M. D., Scott, S. H., & Dukelow, S. P. (2014) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2014.04.025 · Cited by 55 · see citing works
Upper Extremity Proprioception After Stroke: Bridging the Gap Between Neuroscience and Rehabilitation
Findlater, S. E., & Dukelow, S. P. (2016) · Journal of Motor Behavior · doi:10.1080/00222895.2016.1219303 · Cited by 55 · see citing works
E-Skins: Biomimetic Sensing and Encoding for Upper Limb Prostheses
Iskarous, M. M., & Thakor, N. V. (2019) · Proceedings of the IEEE · doi:10.1109/jproc.2019.2939369 · Cited by 54 · see citing works
Implantable neurotechnologies: bidirectional neural interfaces—applications and VLSI circuit implementations
Greenwald, E., Masters, M. R., & Thakor, N. V. (2016) · Medical & Biological Engineering & Computing · doi:10.1007/s11517-015-1429-x · Cited by 53 · see citing works
Brain computer interface learning for systems based on electrocorticography and intracortical microelectrode arrays
Hiremath, S. V., Chen, W., Wang, W., Foldes, S., Yang, Y., Tyler-Kabara, E. C., Collinger, J. L., & Boninger, M. L. (2015) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2015.00040 · Cited by 53 · see citing works
Recording and decoding for neural prostheses
Warren, D. J., Kellis, S., Nieveen, J. G., Wendelken, S. M., Dantas, H., Davis, T. S., Hutchinson, D. T., Normann, R. A., Clark, G. A., & Mathews, V. J. (2016) · Proceedings of the IEEE · doi:10.1109/jproc.2015.2507180 · Cited by 52 · see citing works
Multi-electrode stimulation in somatosensory cortex increases probability of detection
Zaaimi, B., Ruiz-Torres, R., Solla, S. A., & Miller, L. E. (2013) · Journal of Neural Engineering · doi:10.1088/1741-2560/10/5/056013 · Cited by 51 · see citing works
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Authors: Weber, D. J., Friesen, R., & Miller, L. E.
Affiliations: United States Department of Veterans Affairs (US)
Northwestern University (US)
ORCID: Weber, Douglas J.
Friesen, Rebecca
Miller, Lee E.
Venue: Journal of Motor Behavior
Publisher: Informa UK Limited
Published: 2012-01
Volume: 44
Issue: 6
Pages: 403-418
ISSN: 0022-2895 (ISSN-L)
1940-1027
DOI: 10.1080/00222895.2012.735283
OpenAlex: W2060215837
Cited by: 98
References: 162
Citations by year: 2025: 4 · 2024: 3 · 2023: 4 · 2022: 6 · 2021: 10 · 2020: 4 · 2019: 12 · 2018: 7 · 2017: 8 · 2016: 13 · 2015: 8 · 2014: 13 · 2013: 6
FWCI: 3.56
Type: journal article
Language: en
Open access: closed
Locations: Journal of Motor Behavior (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of Neurological Disorders and Stroke (R21NS056136)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neural Engineering
Life Sciences › Neuroscience › Cognitive Neuroscience › Tactile and Sensory Interactions
Life Sciences › Neuroscience › Cognitive Neuroscience › EEG and Brain-Computer Interfaces
Keywords: upper limb prosthesis, tactile feedback, proprioception, microelectrode arrays, peripheral nerve stimulation, primary somatosensory cortex, cochlear implants, prosthetic hand
MeSH terms: Animals, Central Nervous System, Humans, Neural Pathways, Proprioception, Peripheral Nervous System, Feedback, Physiological, Touch Perception, Neural Prostheses

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Interfacing the Somatosensory System to Restore Touch and Proprioception: Essential Considerations

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