The effect of chronic intracortical microstimulation on the electrode–tissue interface
Open accessAbstract
OBJECTIVE: Somatosensation is critical for effective object manipulation, but current upper limb prostheses do not provide such feedback to the user. For individuals who require use of prosthetic limbs, this lack of feedback transforms a mundane task into one that requires extreme concentration and effort. Although vibrotactile motors and sensory substitution devices can be used to convey gross sensations, a direct neural interface is required to provide detailed and intuitive sensory feedback. The viability of intracortical microstimulation (ICMS) as a method to deliver feedback depends in part on the long-term reliability of implanted electrodes used to deliver the stimulation. The objective of the present study is to investigate the effects of chronic ICMS on the electrode-tissue interface. APPROACH: We stimulate the primary somatosensory cortex of three Rhesus macaques through chronically implanted electrodes for 4 h per day over a period of six months, with different electrodes subjected to different regimes of stimulation. We measure the impedance and voltage excursion as a function of time and of ICMS parameters. We also test the sensorimotor consequences of chronic ICMS by having animals grasp and manipulate small treats. MAIN RESULTS: We show that impedance and voltage excursion both decay with time but stabilize after 10-12 weeks. The magnitude of this decay is dependent on the amplitude of the ICMS and, to a lesser degree, the duration of individual pulse trains. Furthermore, chronic ICMS does not produce any deficits in fine motor control. SIGNIFICANCE: The results suggest that chronic ICMS has only a minor effect on the electrode-tissue interface and may thus be a viable means to convey sensory feedback in neuroprosthetics.
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ICMS pulse trains transferred through implanted electrodes (UEAs) in a monkey can restore sensory feedback.
“In other studies, ICMS pulse trains have been transferred through implanted electrodes (UEAs) in a monkey for restoration of sensory feedback (Bensmaia and Miller, 2014; Chen et al., 2014; Kim et al., 2015).”
From Selectivity and Longevity of Peripheral-Nerve and Machine Interfaces: A Review. (2017) · cites this paper as Chen et al., 2014
The Methods (Subjects, Arrays, and Stimulation protocol; page unavailable) describe ICMS pulse trains delivered through implanted UEAs in rhesus macaques. The Introduction identifies sensory feedback as a potential application, but the Results (Behavioral effects of chronic microstimulation; page unavailable) assess grasping for adverse effects, not whether stimulation restored sensory feedback. (LLM, conf=0.86)
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Cites
Neural Stimulation and Recording Electrodes
Cogan, S. F. (2008) · Annual Review of Biomedical Engineering · doi:10.1146/annurev.bioeng.10.061807.160518 · Cited by 2,243 · see citing works
High-performance neuroprosthetic control by an individual with tetraplegia
Collinger, J. L., Wodlinger, B., Downey, J. E., Wang, W., Tyler-Kabara, E. C., Weber, D. J., McMorland, A. J., Velliste, M., Boninger, M. L., & Schwartz, A. B. (2013) · The Lancet · doi:10.1016/s0140-6736(12)61816-9 · Cited by 1,848 · see citing works
Brain-Controlled Interfaces: Movement Restoration with Neural Prosthetics
Schwartz, A. B., Cui, X. T., Weber, D. J., & Moran, D. W. (2006) · Neuron · doi:10.1016/j.neuron.2006.09.019 · Cited by 792 · see citing works
Charge density and charge per phase as cofactors in neural injury induced by electrical stimulation
McCreery, D. B., Agnew, W. F., Yuen, T. G. H., & Bullara, L. (1990) · IEEE Transactions on Biomedical Engineering · doi:10.1109/10.102812 · Cited by 708 · see citing works
A high-performance brain–computer interface
Santhanam, G., Ryu, S. I., Yu, B. M., Afshar, A., & Shenoy, K. V. (2006) · Nature · doi:10.1038/nature04968 · Cited by 698 · see citing works
Control of limb dynamics in normal subjects and patients without proprioception
Sainburg, R. L., Ghilardi, M. F., Poizner, H., & Ghez, C. (1995) · Journal of Neurophysiology · doi:10.1152/jn.1995.73.2.820 · Cited by 662 · see citing works
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
Chronic Neural Recording Using Silicon-Substrate Microelectrode Arrays Implanted in Cerebral Cortex
Vetter, R. J., Williams, J. C., Hetke, J. F., Nunamaker, E. A., & Kipke, D. R. (2004) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2004.826680 · Cited by 477 · see citing works
In Vivo Measurement of Cortical Impedance Spectrum in Monkeys: Implications for Signal Propagation
Logothetis, N. K., Kayser, C., & Oeltermann, A. (2007) · Neuron · doi:10.1016/j.neuron.2007.07.027 · Cited by 447 · see citing works
Complex impedance spectroscopy for monitoring tissue responses to inserted neural implants
Williams, J. C., Hippensteel, J. A., Dilgen, J., Shain, W. G., & Kipke, D. R. (2007) · Journal of Neural Engineering · doi:10.1088/1741-2560/4/4/007 · Cited by 399 · see citing works
Electrical properties of implant encapsulation tissue
Grill, W. M., & Mortimer, J. T. (1994) · Annals of Biomedical Engineering · doi:10.1007/bf02368219 · Cited by 377 · see citing works
Xerri, C., Merzenich, M. M., Peterson, B. E., & Jenkins, W. M. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.79.4.2119 · Cited by 355 · see citing works
Restoring the sense of touch with a prosthetic hand through a brain interface
Tabot, G. A., Dammann, J. F., Berg, J. A., Tenore, F. V., Boback, J. L., Vogelstein, R. J., & Bensmaia, S. J. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1221113110 · Cited by 320 · see citing works
Self-citationLiu, X., McCreery, D. B., Carter, R. R., Bullara, L. A., Yuen, T. G. H., & Agnew, W. F. (1999) · IEEE Transactions on Rehabilitation Engineering · doi:10.1109/86.788468 · Cited by 272 · see citing works
Chronic neural stimulation with thin-film, iridium oxide electrodes
Weiland, J. D., & Anderson, D. J. (2000) · IEEE Transactions on Biomedical Engineering · doi:10.1109/10.846685 · Cited by 263 · see citing works
Incorporating Feedback from Multiple Sensory Modalities Enhances Brain–Machine Interface Control
Suminski, A. J., Tkach, D. C., Fagg, A. H., & Hatsopoulos, N. G. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3967-10.2010 · Cited by 232 · see citing works
Beebe, X., & Rose, T. L. (1988) · IEEE Transactions on Biomedical Engineering · doi:10.1109/10.2122 · Cited by 220 · see citing works
Brummer, S. B., Robblee, L. S., & Hambrecht, F. T. (1983) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1983.tb31628.x · Cited by 205 · see citing works
Negi, S., Bhandari, R., Rieth, L. W., & Solzbacher, F. (2010) · Biomedical Materials · doi:10.1088/1748-6041/5/1/015007 · Cited by 202 · see citing works
Rousche, P. J., & Normann, R. A. (1999) · IEEE Transactions on Rehabilitation Engineering · doi:10.1109/86.750552 · Cited by 187 · see citing works
A Miniature Vibrotactile Sensory Substitution Device for Multifingered Hand Prosthetics
Cipriani, C., D’Alonzo, M., & Carrozza, M. C. (2011) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2011.2173342 · Cited by 164 · see citing works
Tykocinski, M., Cohen, L. T., & Cowan, R. (2005) · Otology & Neurotology · doi:10.1097/01.mao.0000185056.99888.f3 · Cited by 156 · see citing works
Sputtered iridium oxide films (SIROFs) for low-impedance neural stimulation and recording electrodes
Cogan, S. F., Plante, T. D., & Ehrlich, J. (2005) · The 26th Annual International Conference of the IEEE Engineering in Medicine and Biology Society · doi:10.1109/iembs.2004.1404158 · Cited by 138 · see citing works
McCreery, D. B., Pikov, V., & Troyk, P. R. (2010) · Journal of Neural Engineering · doi:10.1088/1741-2560/7/3/036005 · Cited by 137 · see citing works
Otto, K. J., Johnson, M. D., & Kipke, D. R. (2006) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2005.862530 · Cited by 132 · see citing works
Self-citationRepeated voltage biasing improves unit recordings by reducing resistive tissue impedances
Johnson, M. D., Otto, K. J., & Kipke, D. R. (2005) · IEEE Transactions on Neural Systems and Rehabilitation Engineering · doi:10.1109/tnsre.2005.847373 · Cited by 131 · see citing works
Self-citationNegi, S., Bhandari, R., Rieth, L. W., Wagenen, R. V., & Solzbacher, F. (2009) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2009.10.016 · Cited by 127 · see citing works
Electrical Stimulation of the Proprioceptive Cortex (Area 3a) Used to Instruct a Behaving Monkey
London, B. M., Jordan, L. R., Jackson, C. R., & Miller, L. E. (2008) · IEEE Transactions on Neural Systems and Rehabilitation Engineering · doi:10.1109/tnsre.2007.907544 · Cited by 124 · see citing works
Behavioral Demonstration of a Somatosensory Neuroprosthesis
Berg, J. A., Dammann, J. F., Tenore, F. V., Tabot, G. A., Boback, J. L., Manfredi, L. R., Peterson, M. L., Katyal, K. D., Johannes, M. S., Makhlin, A., et al. (2013) · IEEE Transactions on Neural Systems and Rehabilitation Engineering · doi:10.1109/tnsre.2013.2244616 · Cited by 119 · see citing works
Self-citationElectrical Performance of Penetrating Microelectrodes Chronically Implanted in Cat Cortex
Kane, S. R., Cogan, S. F., Ehrlich, J., Plante, T. D., McCreery, D. B., & Troyk, P. R. (2013) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2013.2248152 · Cited by 95 · see citing works
Davis, T. S., Parker, R. A., House, P. A., Bagley, E. E., Wendelken, S., Normann, R. A., & Greger, B. E. (2012) · Journal of Neural Engineering · doi:10.1088/1741-2560/9/6/065003 · Cited by 91 · see citing works
Paasche, G., Tasche, C., Stöver, T., Lesinski‐Schiedat, A., & Lenarz, T. (2009) · Otology & Neurotology · doi:10.1097/mao.0b013e3181ab8fba · Cited by 90 · see citing works
SENSORY SUBSTITUTION IN PROSTHETICS
Lundborg, G., & Rosén, B. (2001) · Hand Clinics · doi:10.1016/s0749-0712(21)00526-6 · Cited by 80 · see citing works
Virtual Active Touch Using Randomly Patterned Intracortical Microstimulation
O’Doherty, J. E., Lebedev, M., Li, Z., & Nicolelis, M. A. L. (2011) · IEEE Transactions on Neural Systems and Rehabilitation Engineering · doi:10.1109/tnsre.2011.2166807 · Cited by 72 · see citing works
Electrical stimulation causes rapid changes in electrode impedance of cell-covered electrodes
Newbold, C., Richardson, R. T., Millard, R. E., et al. (2011) · Journal of Neural Engineering · doi:10.1088/1741-2560/8/3/036029 · Cited by 65 · see citing works
The role of methane in mammalian physiology—is it a gasotransmitter?
Boros, M., Tuboly, E., Mészáros, A., & Amann, A. (2015) · Journal of Breath Research · doi:10.1088/1752-7155/9/1/014001 · Cited by 62 · 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
Sauvage, R., da Costa, D. L., Erre, J., & Aran, J. (1997) · Hearing Research · doi:10.1016/s0378-5955(97)00066-x · Cited by 48 · see citing works
The functional consequences of chronic, physiologically effective intracortical microstimulation
Parker, R., Davis, T. S., House, P. A., Normann, R. A., & Greger, B. E. (2011) · Progress in brain research · doi:10.1016/b978-0-444-53815-4.00010-8 · Cited by 47 · see citing works
Multimodal, longitudinal assessment of intracortical microstimulation
Koivuniemi, A. S., Wilks, S. J., Woolley, A. J., & Otto, K. J. (2011) · Progress in brain research · doi:10.1016/b978-0-444-53815-4.00011-x · Cited by 45 · see citing works
Self-citationAsymmetric 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
Self-citationWang, C., Brunton, E., Haghgooie, S., Cassells, K., Lowery, A. J., & Rajan, R. (2013) · Journal of Neural Engineering · doi:10.1088/1741-2560/10/4/046010 · Cited by 39 · see citing works
Sommakia, S., Rickus, J. L., & Otto, K. J. (2009) · Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC) · doi:10.1109/iembs.2009.5332456 · Cited by 20 · see citing works
Self-citationElectrical performance of penetrating microelectrodes chronically implanted in cat cortex
Kane, S. R., Cogan, S. F., Ehrlich, J., Plante, T. D., & McCreery, D. B. (2011) · Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC) · doi:10.1109/iembs.2011.6091339 · Cited by 18 · see citing works
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- [12]O’Doherty JE 2011 Active tactile exploration using a brain–machine–brain interface Nature 479 228– 31 21976021 PMC3236080
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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
Self-citationRestoring 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
Kim, S., Callier, T., Tabot, G. A., Gaunt, R. A., Tenore, F. V., & Bensmaia, S. J. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1509265112 · Cited by 125 · see citing works
Self-citationSelectivity 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
“, 2016): The neurons (or neuronal tissues) at the implanted surface and the electrodes (implanted interface) degrade over time (McCreery et al., 2010; Prasad et al., 2012; Kane et al., 2013; Chen et al., 2014).”
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Self-citationFifer, 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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Sharma, G., Annetta, N., Friedenberg, D., Blanco, T., Vasconcelos, D., Shaikhouni, A., Rezai, A. R., & Bouton, C. (2015) · Bioelectronic Medicine · doi:10.15424/bioelectronmed.2015.00010 · Cited by 41 · see citing works
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- Authors
- Chen, K. H., Dammann, J. F., Boback, J. L., Tenore, F. V., Otto, K. J., Gaunt, R. A., & Bensmaia, S. J.
- Affiliations
- University of Chicago (US)
- Johns Hopkins University (US)
- Purdue University West Lafayette (US)
- University of Pittsburgh (US)
- Venue
- Journal of Neural Engineering
- Publisher
- IOP Publishing
- Published
- 2014-02-06
- Volume
- 11
- Issue
- 2
- Pages
- 026004
- ISSN
- 1741-2552 (ISSN-L)
- 1741-2560
- PMC
- PMC8129589
- OpenAlex
- W2001010190
- Cited by
- 59
- References
- 44
- Citations by year
- 2026: 4 · 2025: 7 · 2024: 1 · 2023: 2 · 2022: 5 · 2021: 8 · 2020: 3 · 2019: 6 · 2018: 4 · 2017: 3 · 2016: 5 · 2015: 6 · 2014: 5
- FWCI
- 2.89
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- Journal of Neural Engineering (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (5r03dc009339-03)
- National Institute on Deafness and Other Communication Disorders (R03-DC009339)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neural Engineering
- Life Sciences › Neuroscience › Cognitive Neuroscience › EEG and Brain-Computer Interfaces
- Health Sciences › Medicine › Anesthesiology and Pain Medicine › Pain Management and Treatment
- Keywords
- intracortical microstimulation, electrode-tissue interface, chronic stimulation, primary somatosensory cortex, voltage excursions, neuroprosthetics, sensory feedback, upper limb prosthesis, rhesus monkeys, fine motor control
- MeSH terms
- Animals, Electric Stimulation, Electrodes, Implanted, Female, Macaca mulatta, Male, Microelectrodes, Somatosensory Cortex, Time Factors, Hand Strength
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