Proprioceptive and cutaneous sensations in humans elicited by intracortical microstimulation
Open accessAbstract
Pioneering work with nonhuman primates and recent human studies established intracortical microstimulation (ICMS) in primary somatosensory cortex (S1) as a method of inducing discriminable artificial sensation. However, these artificial sensations do not yet provide the breadth of cutaneous and proprioceptive percepts available through natural stimulation. In a tetraplegic human with two microelectrode arrays implanted in S1, we report replicable elicitations of sensations in both the cutaneous and proprioceptive modalities localized to the contralateral arm, dependent on both amplitude and frequency of stimulation. Furthermore, we found a subset of electrodes that exhibited multimodal properties, and that proprioceptive percepts on these electrodes were associated with higher amplitudes, irrespective of the frequency. These novel results demonstrate the ability to provide naturalistic percepts through ICMS that can more closely mimic the body’s natural physiological capabilities. Furthermore, delivering both cutaneous and proprioceptive sensations through artificial somatosensory feedback could improve performance and embodiment in brain-machine interfaces.
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The perceptual characteristics of microstimulation have been elucidated in recent studies of humans with chronically implanted microelectrode arrays.
“it is only in recent studies of humans with chronically implanted microelectrode arrays that the perceptual characteristics of microstimulation have been elucidated (19, 20).”
From A brain-computer interface that evokes tactile sensations improves robotic arm control (2021) · cites this paper as [20]
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Cites
Active tactile exploration using a brain–machine–brain interface
O’Doherty, J. E., Lebedev, M. A., Ifft, P. J., Zhuang, K. Z., Shokur, S., Bleuler, H., & Nicolelis, M. A. L. (2011) · Nature · doi:10.1038/nature10489 · Cited by 629 · see citing works
Restoring sensorimotor function through intracortical interfaces: progress and looming challenges
Bensmaia, S. J., & Miller, L. E. (2014) · Nature Reviews Neuroscience · doi:10.1038/nrn3724 · Cited by 368 · see citing works
The neural basis of perceived intensity in natural and artificial touch
Graczyk, E. L., Schiefer, M. A., Saal, H. P., Delhaye, B. P., Bensmaia, S. J., & Tyler, D. J. (2016) · Science Translational Medicine · doi:10.1126/scitranslmed.aaf5187 · Cited by 258 · see citing works
Flagged first, then by citations
Research works printed but not linked: 26
- Aflalo T Kellis S Klaes C Lee B Shi Y Pejsa K Shanfield K Hayes-Jackson S Aisen M Heck C Liu C Andersen RA 2015 Neurophysiology. Decoding motor imagery from the posterior parietal cortex of a tetraplegic human Science 348 906 910 10.1126/science.aaa5417 25999506 PMC4896830 · DOI · Paper page
- Cole J Cole JO 1995 Pride and a Daily Marathon MIT Press
- Dadarlat MC O'Doherty JE Sabes PN 2015 A learning-based approach to artificial sensory feedback leads to optimal integration Nature Neuroscience 18 138 144 10.1038/nn.3883 25420067 PMC4282864 · DOI · Paper page
- Darie R Powell M Borton D 2017 Delivering the sense of touch to the human brain Neuron 93 728 730 10.1016/j.neuron.2017.02.008 28231460 · DOI
- de Lafuente V Romo R 2005 Neuronal correlates of subjective sensory experience Nature Neuroscience 8 1698 1703 10.1038/nn1587 16286929 · DOI
- Flesher SN Collinger JL Foldes ST Weiss JM Downey JE Tyler-Kabara EC Bensmaia SJ Schwartz AB Boninger ML Gaunt RA 2016 Intracortical microstimulation of human somatosensory cortex Science Translational Medicine 8 361ra141 10.1126/scitranslmed.aaf8083 27738096 · DOI · Paper page
- Florence SL Taub HB Kaas JH 1998 Large-scale sprouting of cortical connections after peripheral injury in adult macaque monkeys Science 282 1117 1121 10.1126/science.282.5391.1117 9804549 · DOI
- Friedman RM Chen LM Roe AW 2004 Modality maps within primate somatosensory cortex PNAS 101 12724 12729 10.1073/pnas.0404884101 15308779 PMC514661 · DOI
- Geyer S Schleicher A Zilles K 1999 Areas 3a, 3b, and 1 of human primary somatosensory cortex NeuroImage 10 63 83 10.1006/nimg.1999.0440 10385582 · DOI
- Johnson LA Wander JD Sarma D Su DK Fetz EE Ojemann JG 2013 Direct electrical stimulation of the somatosensory cortex in humans using electrocorticography electrodes: a qualitative and quantitative report Journal of Neural Engineering 10 036021 10.1088/1741-2560/10/3/036021 23665776 PMC3718452 · DOI
- Kaas JH Merzenich MM Killackey HP 1983 The reorganization of somatosensory cortex following peripheral nerve damage in adult and developing mammals Annual Review of Neuroscience 6 325 356 10.1146/annurev.ne.06.030183.001545 6340591 · DOI
- Kaas JH Nelson RJ Sur M Lin CS Merzenich MM 1979 Multiple representations of the body within the primary somatosensory cortex of primates Science 204 521 523 10.1126/science.107591 107591 · DOI · Paper page
- Kaas JH 1983 What, if anything, is SI? Organization of first somatosensory area of cortex Physiological Reviews 63 206 231 10.1152/physrev.1983.63.1.206 6401864 · DOI
- Kastner S De Weerd P Desimone R Ungerleider LG 1998 Mechanisms of directed attention in the human extrastriate cortex as revealed by functional MRI Science 282 108 111 10.1126/science.282.5386.108 9756472 · DOI
- Kim S Callier T Tabot GA Gaunt RA Tenore FV Bensmaia SJ 2015a Behavioral assessment of sensitivity to intracortical microstimulation of primate somatosensory cortex PNAS 112 15202 15207 10.1073/pnas.1509265112 26504211 PMC4679002 · DOI · Paper page
- Kim SS Gomez-Ramirez M Thakur PH Hsiao SS 2015b Multimodal interactions between proprioceptive and cutaneous signals in primary somatosensory cortex Neuron 86 555 566 10.1016/j.neuron.2015.03.020 25864632 PMC4409561 · DOI
- Klaes C Shi Y Kellis S Minxha J Revechkis B Andersen RA 2014 A cognitive neuroprosthetic that uses cortical stimulation for somatosensory feedback Journal of Neural Engineering 11 056024 10.1088/1741-2560/11/5/056024 25242377 PMC4410973 · DOI
- McKenna TM Whitsel BL Dreyer DA 1982 Anterior parietal cortical topographic organization in macaque monkey: a reevaluation Journal of Neurophysiology 48 289 317 10.1152/jn.1982.48.2.289 7119852 · DOI
- Moore CI Stern CE Dunbar C Kostyk SK Gehi A Corkin S 2000 Referred phantom sensations and cortical reorganization after spinal cord injury in humans PNAS 97 14703 14708 10.1073/pnas.250348997 11114177 PMC18982 · DOI
- Romo R Hernández A Zainos A Brody CD Lemus L 2000 Sensing without touching Neuron 26 273 278 10.1016/S0896-6273(00)81156-3 10798410 · DOI
- Romo R Hernández A Zainos A Salinas E 1998 Somatosensory discrimination based on cortical microstimulation Nature 392 387 390 10.1038/32891 9537321 · DOI
- Sainburg RL Poizner H Ghez C 1993 Loss of proprioception produces deficits in interjoint coordination Journal of Neurophysiology 70 2136 2147 10.1152/jn.1993.70.5.2136 8294975 PMC10710694 · DOI
- Staines WR Graham SJ Black SE McIlroy WE 2002 Task-relevant modulation of contralateral and ipsilateral primary somatosensory cortex and the role of a prefrontal-cortical sensory gating system NeuroImage 15 190 199 10.1006/nimg.2001.0953 11771988 · DOI
- Tabot GA Dammann JF Berg JA Tenore FV Boback JL Vogelstein RJ Bensmaia SJ 2013 Restoring the sense of touch with a prosthetic hand through a brain interface PNAS 110 18279 18284 10.1073/pnas.1221113110 24127595 PMC3831459 · DOI · Paper page
- Tomlinson T Miller LE 2016 Toward a proprioceptive neural interface that mimics natural cortical activity Advances in Experimental Medicine and Biology 957 367 388 10.1007/978-3-319-47313-0_20 28035576 PMC5452683 · DOI
- Yau JM Kim SS Thakur PH Bensmaia SJ 2016 Feeling form: the neural basis of haptic shape perception Journal of Neurophysiology 115 631 642 10.1152/jn.00598.2015 26581869 PMC4752307 · DOI
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Fifer, M. S., McMullen, D. P., Osborn, L. E., Thomas, T. M., Christie, B., Nickl, R. W., Candrea, D. N., Pohlmeyer, E. A., Thompson, M. C., Anaya, M. A., et al. (2022) · Neurology · doi:10.1212/wnl.0000000000013173 · Cited by 103 · see citing works
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Self-citationBullard, A. J., Hutchison, B. C., Lee, J., Chestek, C. A., & Patil, P. G. (2020) · Neuromodulation: Technology at the Neural Interface · doi:10.1111/ner.13069 · Cited by 65 · see citing works
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Zalucki, O., Brown, D. J., & Key, B. (2023) · Biology & Philosophy · doi:10.1007/s10539-023-09924-y · Cited by 7 · see citing works
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- Authors
- Armenta Salas, M., Bashford, L., Kellis, S., Jafari, M., Jo, H., Kramer, D., Shanfield, K., Pejsa, K., Lee, B., Liu, C. Y., & Andersen, R. A.
- Affiliations
- Department of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
- California Institute of Technology (US)
- University of Southern California (US)
- Rancho Los Amigos National Rehabilitation Center (US)
- Corresponding author
- Andersen, Richard A
- ORCID
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2018-04-10
- Volume
- 7
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC5896877
- OpenAlex
- W2798055435
- Cited by
- 263
- References
- 3
- Citations by year
- 2026: 24 · 2025: 32 · 2024: 41 · 2023: 30 · 2022: 33 · 2021: 44 · 2020: 25 · 2019: 28 · 2018: 6
- FWCI
- 11.73
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institute of Neurological Disorders and Stroke (5U01NS098975-02, NS099008-01)
- Della Martin Foundation
- David Geffen School of Medicine, University of California, Los Angeles (David Geffen Medical Scholarship)
- James G. Boswell Foundation
- National Science Foundation (1028725)
- T & C Chen Brain-machine Interface Center
- 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
- intracortical microstimulation, primary somatosensory cortex, proprioception, skin sensation, tetraplegia, brain-computer interface, somatosensory feedback, stimulation amplitude, stimulation frequency, embodiment
- MeSH terms
- Electric Stimulation, Electrodes, Implanted, Evoked Potentials, Somatosensory, Hand, Humans, Microelectrodes, Proprioception, Skin, Somatosensory Cortex, Touch Perception, Brain-Computer Interfaces
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