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Neuropathological effects of chronically implanted, intracortical microelectrodes in a tetraplegic patient

Szymanski, Linda J. and Kellis, Spencer and Liu, Charles Y. and Jones, Kymry T. and Andersen, Richard A. and Commins, Deborah and Lee, Brian and McCreery, Douglas B. and Miller, Carol A. (2021) Neuropathological effects of chronically implanted, intracortical microelectrodes in a tetraplegic patient. Journal of Neural Engineering, 18 (4). Art. No. 0460b9. ISSN 1741-2560. doi:10.1088/1741-2552/ac127e. https://resolver.caltech.edu/CaltechAUTHORS:20210513-111744586

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Abstract

Objective. Intracortical microelectrode arrays (MEA) can be used as part of a brain–machine interface system to provide sensory feedback control of an artificial limb to assist persons with tetraplegia. Variability in functionality of electrodes has been reported but few studies in humans have examined the impact of chronic brain tissue responses revealed postmortem on electrode performance in vivo. Approach. In a tetraplegic man, recording MEAs were implanted into the anterior intraparietal area and Brodmann's area 5 (BA5) of the posterior parietal cortex and a recording and stimulation array was implanted in BA1 of the primary somatosensory cortex (S1). The participant expired from unrelated causes seven months after MEA implantation. The underlying tissue of two of the three devices was processed for histology and electrophysiological recordings were assessed. Main results. Recordings of neuronal activity were obtained from all three MEAs despite meningeal encapsulation. However, the S1 array had a greater encapsulation, yielded lower signal quality than the other arrays and failed to elicit somatosensory percepts with electrical stimulation. Histological examination of tissues underlying S1 and BA5 implant sites revealed localized leptomeningeal proliferation and fibrosis, lymphocytic infiltrates, astrogliosis, and foreign body reaction around the electrodes. The BA5 recording site showed focal cerebral microhemorrhages and leptomeningeal vascular ectasia. The S1 site showed focal tissue damage including vascular recanalization, neuronal loss, and extensive subcortical white matter necrosis. The tissue response at the S1 site included hemorrhagic-induced injury suggesting a likely mechanism for reduced function of the S1 implant. Significance. Our findings are similar to those from animal studies with chronic intracortical implants and suggest that vascular disruption and microhemorrhage during device implantation are important contributors to overall array and individual electrode performance and should be a topic for future device development to mitigate tissue responses. Neurosurgical considerations are also discussed.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1088/1741-2552/ac127eDOIArticle
ORCID:
AuthorORCID
Szymanski, Linda J.0000-0003-4783-9906
Kellis, Spencer0000-0002-5158-1058
Liu, Charles Y.0000-0001-6423-8577
Andersen, Richard A.0000-0002-7947-0472
Lee, Brian0000-0002-3592-8146
Miller, Carol A.0000-0002-9411-3027
Additional Information:© 2021 The Author(s). Published by IOP Publishing Ltd. Original content from this work may be used under the terms of the Creative Commons Attribution 4.0 license. Any further distribution of this work must maintain attribution to the author(s) and the title of the work, journal citation and DOI. Received 12 May 2021; Accepted 8 July 2021; Published 27 July 2021. We wish to acknowledge the family of the research participant for graciously allowing the histological studies. This work was funded by NINDS Grants 5U01NS098975-02 and 5R01NS088379-05. Data availability statement: All data that support the findings of this study are included within the article (and any supplementary files). The authors declare that no competing interests exist. Author Contributions: Neuropathology, L J S, C A M, K T J, D M; Device Engineers, S K and R A A; Neurosurgery, C Y L and B L.
Group:Tianqiao and Chrissy Chen Institute for Neuroscience
Funders:
Funding AgencyGrant Number
NIH5U01NS098975-02
NIH5R01NS088379-05
Subject Keywords:postmortem human neuropathology, neuroport intracortical microelectrode arrays, electrical stimulation, tetraplegic, recording of neuronal action potentials
Issue or Number:4
DOI:10.1088/1741-2552/ac127e
Record Number:CaltechAUTHORS:20210513-111744586
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20210513-111744586
Official Citation:Linda J Szymanski et al 2021 J. Neural Eng. 18 0460b9
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:109114
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:02 Aug 2021 21:08
Last Modified:02 Aug 2021 21:24

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