Intrafascicular stimulation of monkey arm nerves evokes coordinated grasp and sensory responses
Open accessAbstract
High-count microelectrode arrays implanted in peripheral nerves could restore motor function after spinal cord injury or sensory function after limb loss. In this study, we implanted Utah Slanted Electrode Arrays (USEAs) intrafascicularly at the elbow or shoulder in arm nerves of rhesus monkeys (n = 4) under isoflurane anesthesia. Input-output curves indicated that pulse-width-modulated single-electrode stimulation in each arm nerve could recruit single muscles with little or no recruitment of other muscles. Stimulus trains evoked specific, natural, hand movements, which could be combined via multielectrode stimulation to elicit coordinated power or pinch grasp. Stimulation also elicited short-latency evoked potentials (EPs) in primary somatosensory cortex, which might be used to provide sensory feedback from a prosthetic limb. These results demonstrate a high-resolution, high-channel-count interface to the peripheral nervous system for restoring hand function after neural injury or disruption or for examining nerve structure.
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Ledbetter et al. achieved 5 to 10 different muscle contractions in a monkey arm using stimulation via the USEA.
“Ledbetter et al. achieved 5 to 10 different muscle contractions in a monkey arm using stimulation via the USEA (Ledbetter et al., 2013).”
From Update on Peripheral Nerve Electrodes for Closed-Loop Neuroprosthetics (2018) · cites this paper as Ledbetter et al., 2013
In a study with four monkeys, USEA implantation at elbow and shoulder levels promoted precise muscle activation; extrinsic muscles of the hand were activated selectively, whereas intrinsic muscles grouped for similar functions were often activated together.
“In a study done with four monkeys, the USEA implantation on elbow level and shoulder level promoted precise muscle activation. In particular, the extrinsic muscles of the hand were activated selectively, whereas the intrinsic muscles grouped for similar functions were often activated together [112].”
From Interfaces with the peripheral nervous system for the control of a neuroprosthetic limb: a review (2020) · cites this paper as [112]
Cites
Targeted Muscle Reinnervation for Real-time Myoelectric Control of Multifunction Artificial Arms
Kuiken, T. A. (2009) · JAMA · doi:10.1001/jama.2009.116 · Cited by 1,089 · see citing works
Biran, R., Martin, D. C., & Tresco, P. A. (2005) · Experimental Neurology · doi:10.1016/j.expneurol.2005.04.020 · Cited by 893 · see citing works
Biddiss, E. A., & Chau, T. T. (2007) · American Journal of Physical Medicine & Rehabilitation · doi:10.1097/phm.0b013e3181587f6c · Cited by 646 · see citing works
Direct control of paralysed muscles by cortical neurons
Moritz, C. T., Perlmutter, S. I., & Fetz, E. E. (2008) · Nature · doi:10.1038/nature07418 · Cited by 602 · see citing works
Direct neural sensory feedback and control of a prosthetic arm
Dhillon, G. S., & Horch, K. W. (2005) · IEEE Transactions on Neural Systems and Rehabilitation Engineering · doi:10.1109/tnsre.2005.856072 · Cited by 573 · see citing works
Simeral, J. D., Kim, S.-P., Black, M. J., Donoghue, J. P., & Hochberg, L. R. (2011) · Journal of Neural Engineering · doi:10.1088/1741-2560/8/2/025027 · Cited by 496 · see citing works
Restoration of grasp following paralysis through brain-controlled stimulation of muscles
Ethier, C., Oby, E. R., Bauman, M. J., & Miller, L. E. (2012) · Nature · doi:10.1038/nature10987 · Cited by 485 · see citing works
Self-citationDouble nerve intraneural interface implant on a human amputee for robotic hand control
Rossini, P. M., Micera, S., Benvenuto, A., Carpaneto, J., Cavallo, G., Citi, L., Cipriani, C., Denaro, L., Denaro, V., Di Pino, G., et al. (2010) · Clinical Neurophysiology · doi:10.1016/j.clinph.2010.01.001 · Cited by 396 · see citing works
Pezzin, L. E., Dillingham, T. R., MacKenzie, E. J., Ephraim, P. L., & Rossbach, P. (2004) · Archives of Physical Medicine and Rehabilitation · doi:10.1016/j.apmr.2003.06.002 · Cited by 366 · see citing works
Dhillon, G. S., Lawrence, S. M., Hutchinson, D. T., & Horch, K. W. (2004) · The Journal of Hand Surgery · doi:10.1016/j.jhsa.2004.02.006 · Cited by 354 · see citing works
A method for pneumatically inserting an array of penetrating electrodes into cortical tissue
Rousche, P. J., & Normann, R. A. (1992) · Annals of Biomedical Engineering · doi:10.1007/bf02368133 · Cited by 305 · see citing works
Long-term stimulation and recording with a penetrating microelectrode array in cat sciatic nerve
Branner, A., Stein, R. B., Fernandez, E., Aoyagi, Y., & Normann, R. A. (2004) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2003.820321 · Cited by 301 · see citing works
Long, C., Conrad, P. W., Hall, E. A., et al. (1970) · PubMed · Cited by 282 · see citing works
Intrinsic-Extrinsic Muscle Control of the Hand in Power Grip and Precision Handling
Long, C., Conrad, P. W., HALL, E. A., et al. (1970) · Journal of Bone and Joint Surgery · doi:10.2106/00004623-197052050-00001 · Cited by 260 · see citing works
A multielectrode array for intrafascicular recording and stimulation in sciatic nerve of cats
Branner, A., & Normann, R. A. (2000) · Brain Research Bulletin · doi:10.1016/s0361-9230(99)00231-2 · Cited by 234 · see citing works
Baldi, J. C., Jackson, R. D., Moraille, R., et al. (1998) · Spinal Cord · doi:10.1038/sj.sc.3100679 · Cited by 229 · see citing works
Schieber, M. H. (1991) · Journal of Neurophysiology · doi:10.1152/jn.1991.65.6.1381 · Cited by 222 · see citing works
Muscular production of individuated finger movements: the roles of extrinsic finger muscles
Schieber, M. H. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-01-00284.1995 · Cited by 209 · see citing works
The application of implant technology for cybernetic systems
Warwick, K., Gasson, M., Hutt, B., Goodhew, I., Kyberd, P., Andrews, B., Teddy, P., & Shad, A. (2003) · Archives of Neurology · doi:10.1001/archneur.60.10.1369 · Cited by 206 · see citing works
EMG activation patterns during force production in precision grip
Maier, M. A., & Hepp‐Reymond, M. (1995) · Experimental Brain Research · doi:10.1007/bf00241969 · Cited by 189 · see citing works
An Implanted Upper-Extremity Neuroprosthesis Using Myoelectric Control
Kilgore, K. L., Hoyen, H. A., Bryden, A. M., Hart, R. L., Keith, M. W., & Peckham, P. H. (2008) · The Journal Of Hand Surgery · doi:10.1016/j.jhsa.2008.01.007 · Cited by 188 · see citing works
EMG activation patterns during force production in precision grip
Maier, M. A., & Hepp‐Reymond, M. (1995) · Experimental Brain Research · doi:10.1007/bf00241970 · Cited by 183 · see citing works
Sensory nerve recording for closed‐loop control to restore motor functions
Popovic, D. B., Stein, R. B., Jovanovic, K. L., Dai, R., Kostov, A., & Armstrong, W. W. (1993) · IEEE Transactions on Biomedical Engineering · doi:10.1109/10.247801 · Cited by 159 · see citing works
Pohlmeyer, E. A., Oby, E. R., Perreault, E. J., Solla, S. A., Kilgore, K. L., Kirsch, R. F., & Miller, L. E. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005924 · Cited by 137 · see citing works
Self-citationPrediction of upper limb muscle activity from motor cortical discharge during reaching
Pohlmeyer, E. A., Solla, S. A., Perreault, E. J., & Miller, L. E. (2007) · Journal of Neural Engineering · doi:10.1088/1741-2560/4/4/003 · Cited by 118 · see citing works
Self-citationGustafson, K. J., Pinault, G. C. J., Neville, J. J., Syed, I., Jr, J. A. D., Jean-Claude, J., & Triolo, R. J. (2009) · The Journal of Rehabilitation Research and Development · doi:10.1682/jrrd.2008.08.0097 · Cited by 107 · see citing works
Topographical distribution of motor fascicles in the sciatic‐tibial nerve of the rat
Badia, J., Pascual‐Font, A., Vivó, M., Udina, E., & Navarro, X. (2010) · Muscle & Nerve · doi:10.1002/mus.21652 · Cited by 98 · see citing works
McDonnall, D., Clark, G. A., & Normann, R. A. (2004) · IEEE Transactions on Neural Systems and Rehabilitation Engineering · doi:10.1109/tnsre.2004.828425 · Cited by 98 · see citing works
Self-citationBrissot, R., Gallien, P., Bot, M. L., Beaubras, A., Laisné, D., Beillot, J., & Dassonville, J. (2000) · Spine · doi:10.1097/00007632-200002150-00018 · Cited by 97 · see citing works
Anani, A. B., Ikeda, K., & Körner, L. M. (1977) · Medical & Biological Engineering & Computing · doi:10.1007/bf02457988 · Cited by 74 · see citing works
Recording sensory and motor information from peripheral nerves with Utah Slanted Electrode Arrays
Clark, G. A., Ledbetter, N. M., Warren, D. J., & Harrison, R. R. (2011) · Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC) · doi:10.1109/iembs.2011.6091149 · Cited by 71 · see citing works
Self-citationMartens, F. M. J., & Heesakkers, J. P. F. A. (2011) · Advances in Urology · doi:10.1155/2011/709708 · Cited by 67 · see citing works
PERIPHERAL PROJECTIONS OF FASCICLES IN THE HUMAN MEDIAN NERVE
Schady, W., Ochoa, J. L., Torebjörk, H. E., & CHEN, L. S. (1983) · Brain · doi:10.1093/brain/106.3.745 · Cited by 64 · see citing works
Hallin, R. G. (1990) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp.53.9.736 · Cited by 62 · see citing works
Normann, R. A., Dowden, B. R., Frankel, M. A., Wilder, A. M., Hiatt, S. D., Ledbetter, N. M., Warren, D. A., & Clark, G. A. (2012) · Journal of Neural Engineering · doi:10.1088/1741-2560/9/2/026019 · Cited by 37 · see citing works
Self-citationEnergy consumption of locomotion with orthosis versus Parastep-assisted gait: a single case study
Spadone, R., Merati, G., Bertocchi, E., et al. (2003) · Spinal Cord · doi:10.1038/sj.sc.3101420 · Cited by 35 · see citing works
Ekedahl, R., Frank, O., & Hallin, R. G. (1997) · Brain Research Bulletin · doi:10.1016/s0361-9230(96)00324-3 · Cited by 27 · see citing works
Frankel, M. A., Dowden, B. R., Mathews, V. J., Normann, R. A., Clark, G. A., & Meek, S. G. (2011) · IEEE Transactions on Neural Systems and Rehabilitation Engineering · doi:10.1109/tnsre.2011.2123920 · Cited by 25 · see citing works
Self-citationSelective and Graded Recruitment of Cat Hamstring Muscles With Intrafascicular Stimulation
Dowden, B. R., Wilder, A. M., Hiatt, S. D., Normann, R. A., Brown, N. A. T., & Clark, G. A. (2009) · IEEE Transactions on Neural Systems and Rehabilitation Engineering · doi:10.1109/tnsre.2008.2011988 · Cited by 19 · see citing works
Self-citationNerve cuff stimulation and the effect of fascicular organization for hand grasp in nonhuman primates
Brill, N., Polasek, K. H., Oby, E. R., Éthier, C., Miller, L. E., & Tyler, D. J. (2009) · Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC) · doi:10.1109/iembs.2009.5332395 · Cited by 18 · see citing works
Self-citationAutomated Stimulus-Response Mapping of High-Electrode-Count Neural Implants
Wilder, A. M., Hiatt, S. D., Dowden, B. R., Brown, N. A. T., Normann, R. A., & Clark, G. A. (2009) · IEEE Transactions on Neural Systems and Rehabilitation Engineering · doi:10.1109/tnsre.2009.2029494 · Cited by 16 · see citing works
Self-citationFromm, B., Rupp, R., & Gerner, H. J. (2001) · Handchirurgie · Mikrochirurgie · Plastische Chirurgie · doi:10.1055/s-2001-15129 · Cited by 15 · see citing works
Liu, J., Lau, H., Pereira, B. P., et al. (1996) · Cells Tissues Organs · doi:10.1159/000147788 · Cited by 13 · see citing works
Model of fasciculation and sorting in mixed populations of axons
Chaudhuri, D., Borowski, P., & Zapotocky, M. (2011) · Physical Review E · doi:10.1103/physreve.84.021908 · Cited by 12 · see citing works
Control of Skeletal Muscle Force with Currents Injected Via an Intrafascicular, Microelectrode Array
Normann, R. A., McDonnall, D., & Clark, G. A. (2005) · Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC) · doi:10.1109/iembs.2005.1616282 · Cited by 7 · see citing works
Self-citationFuture of computer implant technology and intelligent human-machine systems.
Warwick, K. (2005) · PubMed · Cited by 2 · see citing works
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Saal, H. P., & Bensmaia, S. J. (2015) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2015.06.010 · Cited by 179 · see citing works
“2C) (Ledbetter et al., 2013).”
Borton, D., Micera, S., Millán, J. D. R., & Courtine, G. (2013) · Science Translational Medicine · doi:10.1126/scitranslmed.3005968 · Cited by 171 · see citing works
Xie, X., Rieth, L., Williams, L., Negi, S., Bhandari, R., Caldwell, R., Sharma, R., Tathireddy, P., & Solzbacher, F. (2014) · Journal of Neural Engineering · doi:10.1088/1741-2560/11/2/026016 · Cited by 137 · see citing works
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McCallum, G. A., Sui, X., Qiu, C., Marmerstein, J., Zheng, Y., Eggers, T. E., Hu, C., Dai, L., & Durand, D. M. (2017) · Scientific Reports · doi:10.1038/s41598-017-10639-w · Cited by 102 · see citing works
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Nghiem, B. T., Sando, I. C., Gillespie, R. B., McLaughlin, B. L., Gerling, G. J., Langhals, N. B., Urbanchek, M. G., & Cederna, P. S. (2015) · Plastic and Reconstructive Surgery · doi:10.1097/prs.0000000000001289 · Cited by 104 · see citing works
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Weber, D. J., Friesen, R., & Miller, L. E. (2012) · Journal of Motor Behavior · doi:10.1080/00222895.2012.735283 · Cited by 98 · see citing works
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MethodInfluentialSelectivity and Longevity of Peripheral-Nerve and Machine Interfaces: A Review.
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- Authors
- Ledbetter, N. M., Ethier, C., Oby, E. R., Hiatt, S. D., Wilder, A. M., Ko, J. H., Agnew, S. P., Miller, L. E., & Clark, G. A.
- Affiliations
- University of Utah (US)
- Department of Physiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois;
- Northwestern University (US)
- Corresponding author
- Clark, Gregory A.
- ORCID
- Venue
- Journal of Neurophysiology
- Publisher
- American Physiological Society
- Published
- 2013-01-15
- Volume
- 109
- Issue
- 2
- Pages
- 580-590
- ISSN
- 0022-3077 (ISSN-L)
- 1522-1598
- PMC
- PMC3545468
- OpenAlex
- W2007905118
- Cited by
- 69
- References
- 46
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 5 · 2023: 5 · 2022: 3 · 2021: 5 · 2020: 5 · 2019: 7 · 2018: 8 · 2017: 7 · 2016: 6 · 2015: 6 · 2014: 4 · 2013: 3 · 2012: 1
- FWCI
- 1.85
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Neurophysiology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (01-NS-053603, R01NS053603)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neural Engineering
- Physical Sciences › Engineering › Biomedical Engineering › Muscle activation and electromyography studies
- Life Sciences › Neuroscience › Neurology › Vagus Nerve Stimulation Research
- Keywords
- peripheral nerve stimulation, rhesus monkeys, hand grasp, muscle recruitment, input-output curves, short-latency evoked potentials, primary somatosensory cortex, sensory feedback, artificial limbs, spinal cord injury, nerve regeneration, neural interfaces
- MeSH terms
- Animals, Haplorhini, Arm, Electric Stimulation, Evoked Potentials, Somatosensory, Fascia, Peripheral Nerves, Somatosensory Cortex, Muscle, Skeletal, Hand Strength, Evoked Potentials, Motor, Feedback, Sensory
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