Decoding Neural Activity in Sulcal and White Matter Areas of the Brain to Accurately Predict Individual Finger Movement and Tactile Stimuli of the Human Hand.

neural decoding neuroprosthetics sensorimotor stereoelectroencephalography tactile stimuli

Journal

Frontiers in neuroscience
ISSN: 1662-4548
Titre abrégé: Front Neurosci
Pays: Switzerland
ID NLM: 101478481

Informations de publication

Date de publication:
2021
Historique:
received: 23 04 2021
accepted: 22 07 2021
entrez: 6 9 2021
pubmed: 7 9 2021
medline: 7 9 2021
Statut: epublish

Résumé

Millions of people worldwide suffer motor or sensory impairment due to stroke, spinal cord injury, multiple sclerosis, traumatic brain injury, diabetes, and motor neuron diseases such as ALS (amyotrophic lateral sclerosis). A brain-computer interface (BCI), which links the brain directly to a computer, offers a new way to study the brain and potentially restore impairments in patients living with these debilitating conditions. One of the challenges currently facing BCI technology, however, is to minimize surgical risk while maintaining efficacy. Minimally invasive techniques, such as stereoelectroencephalography (SEEG) have become more widely used in clinical applications in epilepsy patients since they can lead to fewer complications. SEEG depth electrodes also give access to sulcal and white matter areas of the brain but have not been widely studied in brain-computer interfaces. Here we show the first demonstration of decoding sulcal and subcortical activity related to both movement and tactile sensation in the human hand. Furthermore, we have compared decoding performance in SEEG-based depth recordings versus those obtained with electrocorticography electrodes (ECoG) placed on gyri. Initial poor decoding performance and the observation that most neural modulation patterns varied in amplitude trial-to-trial and were transient (significantly shorter than the sustained finger movements studied), led to the development of a feature selection method based on a repeatability metric using temporal correlation. An algorithm based on temporal correlation was developed to isolate features that consistently repeated (required for accurate decoding) and possessed information content related to movement or touch-related stimuli. We subsequently used these features, along with deep learning methods, to automatically classify various motor and sensory events for individual fingers with high accuracy. Repeating features were found in sulcal, gyral, and white matter areas and were predominantly phasic or phasic-tonic across a wide frequency range for both HD (high density) ECoG and SEEG recordings. These findings motivated the use of long short-term memory (LSTM) recurrent neural networks (RNNs) which are well-suited to handling transient input features. Combining temporal correlation-based feature selection with LSTM yielded decoding accuracies of up to 92.04 ± 1.51% for hand movements, up to 91.69 ± 0.49% for individual finger movements, and up to 83.49 ± 0.72% for focal tactile stimuli to individual finger pads while using a relatively small number of SEEG electrodes. These findings may lead to a new class of minimally invasive brain-computer interface systems in the future, increasing its applicability to a wide variety of conditions.

Identifiants

pubmed: 34483823
doi: 10.3389/fnins.2021.699631
pmc: PMC8415782
doi:

Types de publication

Journal Article

Langues

eng

Pagination

699631

Informations de copyright

Copyright © 2021 Bouton, Bhagat, Chandrasekaran, Herrero, Markowitz, Espinal, Kim, Ramdeo, Xu, Glasser, Bickel and Mehta.

Déclaration de conflit d'intérêts

CB has ownership interests in Neuvotion, LLC and is an inventor on multiple patents in the related field of neuroprosthetics. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Références

IEEE Trans Biomed Circuits Syst. 2018 Dec;12(6):1230-1245
pubmed: 30418885
Nature. 2016 Apr 13;533(7602):247-50
pubmed: 27074513
PLoS One. 2016 Mar 10;11(3):e0150359
pubmed: 26963246
J Neurosci Methods. 2017 Apr 1;281:40-48
pubmed: 28192130
Neurosurg Focus. 2013 Jun;34(6):E3
pubmed: 23724837
J Neural Eng. 2009 Dec;6(6):066001
pubmed: 19794237
Sci Rep. 2017 Jun 30;7(1):4461
pubmed: 28667328
Sci Transl Med. 2016 Oct 19;8(361):361ra141
pubmed: 27738096
Neurosci Res. 2014 Jun;83:1-7
pubmed: 24726922
Nature. 2006 Jul 13;442(7099):164-71
pubmed: 16838014
J Neural Eng. 2011 Apr;8(2):025006
pubmed: 21436521
Front Neurosci. 2020 Feb 14;14:100
pubmed: 32116533
Elife. 2020 Jul 14;9:
pubmed: 32660692
J Neurosci Methods. 2012 Jan 30;203(2):311-4
pubmed: 22044847
Science. 2021 May 21;372(6544):831-836
pubmed: 34016775
PLoS Biol. 2003 Nov;1(2):E42
pubmed: 14624244
Brain Stimul. 2021 Aug 3;14(5):1184-1196
pubmed: 34358704
Bioelectron Med. 2018 Jul 31;4:11
pubmed: 32232087
Neuroimage. 2013 Oct 15;80:105-24
pubmed: 23668970
Neuroimage. 2017 Feb 15;147:219-232
pubmed: 27554533
PLoS One. 2012;7(10):e47992
pubmed: 23110153
Magn Reson Med. 2012 May;67(5):1210-24
pubmed: 21858868
Annu Int Conf IEEE Eng Med Biol Soc. 2019 Jul;2019:3062-3066
pubmed: 31946534
Elife. 2020 Jan 23;9:
pubmed: 31971510
IEEE Trans Biomed Eng. 2021 Aug;68(8):2509-2519
pubmed: 33373294
Neuroimage. 2001 Dec;14(6):1370-86
pubmed: 11707093
Neuroimage. 2013 Dec;83:991-1001
pubmed: 23899722
IEEE Trans Neural Netw. 1994;5(2):157-66
pubmed: 18267787
Sci Rep. 2019 Jan 29;9(1):874
pubmed: 30696881
Neurosurgery. 2013 Mar;72(3):353-66; discussion 366
pubmed: 23168681
Am J Public Health. 2016 Oct;106(10):1855-7
pubmed: 27552260
J Neurophysiol. 2011 Sep;106(3):1125-65
pubmed: 21653723
J Neural Eng. 2017 Feb;14(1):016005
pubmed: 27900947

Auteurs

Chad Bouton (C)

Feinstein Institutes for Medical Research at Northwell Health, New York, NY, United States.
Institute of Bioelectronic Medicine, Feinstein Institutes for Medical Research, New York, NY, United States.
Hofstra-Northwell Medical School, New York, NY, United States.

Nikunj Bhagat (N)

Feinstein Institutes for Medical Research at Northwell Health, New York, NY, United States.
Institute of Bioelectronic Medicine, Feinstein Institutes for Medical Research, New York, NY, United States.

Santosh Chandrasekaran (S)

Feinstein Institutes for Medical Research at Northwell Health, New York, NY, United States.
Institute of Bioelectronic Medicine, Feinstein Institutes for Medical Research, New York, NY, United States.

Jose Herrero (J)

Feinstein Institutes for Medical Research at Northwell Health, New York, NY, United States.
Institute of Bioelectronic Medicine, Feinstein Institutes for Medical Research, New York, NY, United States.
Department of Neurosurgery, Northwell Health, New York, NY, United States.

Noah Markowitz (N)

Institute of Bioelectronic Medicine, Feinstein Institutes for Medical Research, New York, NY, United States.

Elizabeth Espinal (E)

Feinstein Institutes for Medical Research at Northwell Health, New York, NY, United States.
Institute of Bioelectronic Medicine, Feinstein Institutes for Medical Research, New York, NY, United States.

Joo-Won Kim (JW)

Department of Radiology and Psychiatry, Baylor College of Medicine, Houston, TX, United States.

Richard Ramdeo (R)

Feinstein Institutes for Medical Research at Northwell Health, New York, NY, United States.
Institute of Bioelectronic Medicine, Feinstein Institutes for Medical Research, New York, NY, United States.

Junqian Xu (J)

Department of Radiology and Psychiatry, Baylor College of Medicine, Houston, TX, United States.

Matthew F Glasser (MF)

Department of Radiology and Neuroscience, Washington University in St. Louis, St. Louis, MO, United States.

Stephan Bickel (S)

Feinstein Institutes for Medical Research at Northwell Health, New York, NY, United States.
Institute of Bioelectronic Medicine, Feinstein Institutes for Medical Research, New York, NY, United States.
Hofstra-Northwell Medical School, New York, NY, United States.
Department of Neurosurgery, Northwell Health, New York, NY, United States.
Department of Neurology, Northwell Health, New York, NY, United States.

Ashesh Mehta (A)

Feinstein Institutes for Medical Research at Northwell Health, New York, NY, United States.
Institute of Bioelectronic Medicine, Feinstein Institutes for Medical Research, New York, NY, United States.
Hofstra-Northwell Medical School, New York, NY, United States.
Department of Neurosurgery, Northwell Health, New York, NY, United States.

Classifications MeSH