Applications of brain-computer interfaces in neurodegenerative diseases.

Alzheimer’s disease Amyotrophic lateral sclerosis Brain-computer interfaces Neurodegenerative diseases Neurological rehabilitation

Journal

Neurosurgical review
ISSN: 1437-2320
Titre abrégé: Neurosurg Rev
Pays: Germany
ID NLM: 7908181

Informations de publication

Date de publication:
31 May 2023
Historique:
received: 15 01 2023
accepted: 23 05 2023
revised: 06 05 2023
medline: 2 6 2023
pubmed: 31 5 2023
entrez: 31 5 2023
Statut: epublish

Résumé

Brain-computer interfaces (BCIs) provide the central nervous system with channels of direct communication to the outside world, without having to go through the peripheral nervous system. Neurodegenerative diseases (NDs) are notoriously incurable and burdensome medical conditions that will result in progressive deterioration of the nervous system. The applications of BCIs in NDs have been studied for decades now through different approaches, resulting in a considerable amount of literature in all related areas. In this study, we begin by introducing BCIs and proceed by explaining the principles of BCI-based neurorehabilitation. Then, we go through four specific types of NDs, including amyotrophic lateral sclerosis, Parkinson's disease, Alzheimer's disease, and spinal muscular atrophy, and review some of the applications of BCIs in the neural rehabilitation of these diseases. We conclude with a discussion of the characteristics, challenges, and future possibilities of research in the field. Going through the uses of BCIs in NDs, we can see that approaches and strategies employed to tackle the wide range of limitations caused by NDs are numerous and diverse. Furthermore, NDs can fall under different categories based on the target area of neurodegeneration and thus require different methods of BCI-based rehabilitation. In recent years, neurotechnology companies have substantially invested in research on BCIs, focusing on commercializing BCIs and bringing BCI-based technologies from bench to bedside. This can mean the beginning of a new era for BCI-based neurorehabilitation, with an anticipated spike in interest among researchers, practitioners, engineers, and entrepreneurs alike.

Identifiants

pubmed: 37256332
doi: 10.1007/s10143-023-02038-9
pii: 10.1007/s10143-023-02038-9
doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

131

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

Références

Tiwari N, Edla DR, Dodia S, Bablani A (2018) Brain computer interface: a comprehensive survey. Biol Inspired Cogn Arc 26:118–129
Nicolas-Alonso LF, Gomez-Gil J (2012) Brain computer interfaces, a review. Sensors 12(2):1211–1279
pubmed: 22438708 pmcid: 3304110
Zhuang M, Wu Q, Wan F, Hu Y (2020) State-of-the-art non-invasive brain–computer interface for neural rehabilitation: a review. J Neurorestoratology 8(1):12–25
Bertani R, Melegari C, De Cola MC, Bramanti A, Bramanti P, Calabrò RS (2017) Effects of robot-assisted upper limb rehabilitation in stroke patients: a systematic review with meta-analysis. Neurol Sci 38(9):1561–1569
pubmed: 28540536
Pichiorri F, Morone G, Petti M, Toppi J, Pisotta I, Molinari M et al (2015) Brain–computer interface boosts motor imagery practice during stroke recovery. Ann Neurol 77(5):851–865
pubmed: 25712802
Friedrich EV, Suttie N, Sivanathan A, Lim T, Louchart S, Pineda JA (2014) Brain–computer interface game applications for combined neurofeedback and biofeedback treatment for children on the autism spectrum. Front Neuroeng 7:21
pubmed: 25071545 pmcid: 4080880
Lim CG, Lee TS, Guan C, Fung DSS, Zhao Y, Teng SSW et al (2012) A brain-computer interface based attention training program for treating attention deficit hyperactivity disorder. PloS One 7(10):e46692
pubmed: 23115630 pmcid: 3480363
Swann NC, de Hemptinne C, Miocinovic S, Qasim S, Ostrem JL, Galifianakis NB et al (2017) Chronic multisite brain recordings from a totally implantable bidirectional neural interface: experience in 5 patients with Parkinson’s disease. J Neurosurg 128(2):605–616
pubmed: 28409730 pmcid: 5641233
Milekovic T, Sarma AA, Bacher D, Simeral JD, Saab J, Pandarinath C et al (2018) Stable long-term BCI-enabled communication in ALS and locked-in syndrome using LFP signals. J Neurophysiol 120(7):343–360
pubmed: 29694279 pmcid: 6093965
Erkkinen MG, Kim M-O, Geschwind MD (2018) Clinical neurology and epidemiology of the major neurodegenerative diseases. Cold Spring Harb Perspect Biol 10(4):a033118
pubmed: 28716886 pmcid: 5880171
World Health Organization. GHE: Life expectancy and healthy life expectancy.  https://www.who.int/data/gho/data/themes/mortality-and-global-health-estimates/ghe-life-expectancy-and-healthylife-expectancy . Accessed 20 Jul 2022
World Health Organization. Dementia.  https://www.who.int/news-room/factsheets/detail/dementia . Accessed 20 Jul 2022
MedlinePlus. Bethesda (MD): National Library of Medicine (US); Degenerative Nerve diseases.  https://medlineplus.gov/degenerativenervediseases.html . Accessed 20 Jul 2022
Dugger BN, Dickson DW (2017) Pathology of neurodegenerative diseases. Cold Spring Harb Perspect Biol 9(7):a028035
pubmed: 28062563 pmcid: 5495060
Poddar MK, Chakraborty A, Banerjee S (2021) Neurodegeneration: Diagnosis, prevention, and therapy.  https://doi.org/10.5772/intechopen.94950
Durães F, Pinto M, Sousa E (2018) Old drugs as new treatments for neurodegenerative diseases. Pharmaceuticals 11(2):44
pubmed: 29751602 pmcid: 6027455
Mridha MF, Das SC, Kabir MM, Lima AA, Islam MR, Watanobe Y (2021) Brain-computer interface: advancement and challenges. Sensors 21(17):5746
pubmed: 34502636 pmcid: 8433803
Bashashati A, Fatourechi M, Ward RK, Birch GE (2007) A survey of signal processing algorithms in brain–computer interfaces based on electrical brain signals. J Neural Eng 4(2):R32
pubmed: 17409474
Lotte F, Congedo M, Lécuyer A, Lamarche F, Arnaldi B (2007) A review of classification algorithms for EEG-based brain–computer interfaces. J Neural Eng 4(2):R1
pubmed: 17409472
Wieloch T, Nikolich K (2006) Mechanisms of neural plasticity following brain injury. Curr Opin Neurobiol 16(3):258–264
pubmed: 16713245
Di Prisco GV (1984) Hebb synaptic plasticity. Prog Neurobiol 22(2):89–102
Van Es MA, Hardiman O, Chio A, Al-Chalabi A, Pasterkamp RJ, Veldink JH et al (2017) Amyotrophic lateral sclerosis. The Lancet 390(10107):2084–2098
Rowland LP (2001) How amyotrophic lateral sclerosis got its name: the clinical-pathologic genius of Jean-Martin Charcot. Arch Neurol 58(3):512–515
pubmed: 11255459
Wijesekera LC, Nigel LP (2009) Amyotrophic lateral sclerosis. Orphanet J Rare Dis 4(1):1–22
Braun AT, Caballero-Eraso C, Lechtzin N (2018) Amyotrophic lateral sclerosis and the respiratory system. Clin Chest Med 39(2):391–400
pubmed: 29779597
McFarland DJ, Wolpaw JR (2011) Brain-computer interfaces for communication and control. Commun ACM 54(5):60–66
pubmed: 21984822 pmcid: 3188401
Vansteensel MJ, Klein E, van Thiel G, Gaytant M, Simmons Z, Wolpaw JR et al (2023) Towards clinical application of implantable brain-computer interfaces for people with late-stage ALS: medical and ethical considerations. J Neurol 270(3):1323–1336
pubmed: 36450968
Farwell LA, Donchin E (1988) Talking off the top of your head: toward a mental prosthesis utilizing event-related brain potentials. Electroencephalogr Clin Neurophysiol 70(6):510–523
pubmed: 2461285
Marchetti M, Priftis K (2015) Brain–computer interfaces in amyotrophic lateral sclerosis: a metanalysis. Clin Neurophysiol 126(6):1255–1263
pubmed: 25449558
Vaughan TM (2020) Brain-computer interfaces for people with amyotrophic lateral sclerosis. Handb Clin Neurol 168:33–38
pubmed: 32164864
Wolpaw JR, Bedlack RS, Reda DJ, Ringer RJ, Banks PG, Vaughan TM et al (2018) Independent home use of a brain-computer interface by people with amyotrophic lateral sclerosis. Neurology 91(3):e258–ee67
pubmed: 29950436 pmcid: 6059033
Nijboer F, Sellers E, Mellinger J, Jordan MA, Matuz T, Furdea A et al (2008) A P300-based brain–computer interface for people with amyotrophic lateral sclerosis. Clin Neurophysiol 119(8):1909–1916
pubmed: 18571984 pmcid: 2853977
Oxley TJ, Yoo PE, Rind GS, Ronayne SM, Lee CS, Bird C et al (2021) Motor neuroprosthesis implanted with neurointerventional surgery improves capacity for activities of daily living tasks in severe paralysis: first in-human experience. J Neurointerv Surg 13(2):102–108
pubmed: 33115813
Lee A, Gilbert RM (2016) Epidemiology of Parkinson disease. Neurol Clin 34(4):955–965
pubmed: 27720003
World Health Organization. Parkinson disease.  https://www.who.int/newsroom/fact-sheets/detail/parkinson-disease . Accessed 26 Jul 2022
Dorsey ER, Elbaz A, Nichols E, Abbasi N, Abd-Allah F, Abdelalim A et al (2018) Global, regional, and national burden of Parkinson's disease, 1990–2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Neurol 17(11):939–953
Armstrong MJ, Okun MS (2020) Diagnosis and treatment of Parkinson disease: a review. Jama 323(6):548–560
pubmed: 32044947
Chaudhuri KR, Martinez-Martin P, Brown RG, Sethi K, Stocchi F, Odin P et al (2007) The metric properties of a novel non-motor symptoms scale for Parkinson’s disease: results from an international pilot study. Mov Disord 22(13):1901–1911
pubmed: 17674410
Poewe W, Seppi K, Tanner CM, Halliday GM, Brundin P, Volkmann J et al (2017) Parkinson disease. Nat Rev Dis Primers 3(1):1–21
Guidetti M, Marceglia S, Loh A, Harmsen IE, Meoni S, Foffani G et al (2021) Clinical perspectives of adaptive deep brain stimulation. Brain Stimul 14(5):1238–1247
pubmed: 34371211
Little S, Pogosyan A, Neal S, Zavala B, Zrinzo L, Hariz M et al (2013) Adaptive deep brain stimulation in advanced Parkinson disease. Ann Neurol 74(3):449–457
pubmed: 23852650 pmcid: 3886292
Arlotti M, Marceglia S, Foffani G, Volkmann J, Lozano AM, Moro E et al (2018) Eight-hours adaptive deep brain stimulation in patients with Parkinson disease. Neurology 90(11):e971–e9e6
pubmed: 29444973 pmcid: 5858949
Little S, Beudel M, Zrinzo L, Foltynie T, Limousin P, Hariz M et al (2016) Bilateral adaptive deep brain stimulation is effective in Parkinson’s disease. J Neurol Neurosurg Psychiatry 87(7):717–721
pubmed: 26424898
Ruiz S, Buyukturkoglu K, Rana M, Birbaumer N, Sitaram R (2014) Real-time fMRI brain computer interfaces: self-regulation of single brain regions to networks. Biol Psychol 95:4–20
pubmed: 23643926
Buyukturkoglu K, Rana M, Ruiz S, Hackley SA, Soekadar SR, Birbaumer N, Sitaram R (2013) Volitional regulation of the supplementary motor area with fMRI-BCI neurofeedback in Parkinson’s disease: a pilot study. In: 2013 6th International IEEE/EMBS Conference on Neural Engineering (NER).  https://doi.org/10.1109/NER.2013.6696025
Subramanian L, Hindle JV, Johnston S, Roberts MV, Husain M, Goebel R et al (2011) Real-time functional magnetic resonance imaging neurofeedback for treatment of Parkinson’s disease. J Neurosci 31(45):16309–16317
pubmed: 22072682 pmcid: 6633236
Miladinović A, Ajčević M, Busan P, Jarmolowska J, Silveri G, Deodato M, Mezzarobba S, Battaglini P, Accardo A (2020) Evaluation of motor imagery-based BCI methods in neurorehabilitation of Parkinson’s disease patients, pp 3058–3061. https://doi.org/10.1109/EMBC44109.2020.9176651
Liberati G, Veit R, Kim S, Birbaumer N, Von Arnim C, Jenner A et al (2013) Development of a binary fMRI-BCI for Alzheimer patients: a semantic conditioning paradigm using affective unconditioned stimuli. Proceedings - 2013 Humaine Association Conference on Affective Computing and Intelligent Interaction, ACII, pp 838–842.  https://doi.org/10.1109/ACII.2013.157
Linden DE, Turner DL (2016) Real-time functional magnetic resonance imaging neurofeedback in motor neurorehabilitation. Curr Opin Neurol 29(4):412
pubmed: 27213774 pmcid: 4947535
Giuliana G, Mario M, Yassin J (2011) A quality parameter for the detection of the intentionality of movement in patients with neurological tremor performing a finger-to-nose test. Conference proceedings: Annual International Conference of the IEEE Engineering in Medicine and Biology Society. Conf Proc IEEE Eng Med Biol Soc 7707–10.  https://doi.org/10.1109/IEMBS.2011.6091899
Jalbert JJ, Daiello LA, Lapane KL (2008) Dementia of the Alzheimer type. Epidemiol Rev 30(1):15–34
pubmed: 18635578
2021 Alzheimer’s disease facts and figures. Alzheimers Dement 17(3):327–406.  https://doi.org/10.1002/alz.12328
Cummings JL, Cole G (2002) Alzheimer disease. Jama 287(18):2335–2338
pubmed: 11988038
Liberati G, Da Rocha JLD, Van der Heiden L, Raffone A, Birbaumer N, Olivetti Belardinelli M et al (2012) Toward a brain-computer interface for Alzheimer’s disease patients by combining classical conditioning and brain state classification. J Alzheimers Dis 31:S211–20.  https://doi.org/10.3233/JAD-2012-112129
Pavlov PI (2010) Conditioned reflexes: an investigation of the physiological activity of the cerebral cortex. Ann Neurosci 17(3):136
pubmed: 25205891
Liberati G, van der Heiden L, Sitaram R, Kim S, Rana M, Raffone A et al (2011) Classical conditioning of the BOLD signal as a paradigm for basic BCI communication in Alzheimer patients. Alzheimers Dement 7(4):S720
Orhan U, Hild KE, Erdogmus D, Roark B, Oken B, Fried-Oken M (2012) RSVP keyboard: an EEG based typing interface. Proceedings of the IEEE International Conference on Acoustics, Speech and Signal Processing sponsored by the Institute of Electrical and Electronics Engineers Signal Processing Society. ICASSP.  https://doi.org/10.1109/ICASSP.2012.6287966
Galvin-McLaughlin D, Klee D, Memmott T, Peters B, Wiedrick J, Fried-Oken M et al (2022) Methodology and preliminary data on feasibility of a neurofeedback protocol to improve visual attention to letters in mild Alzheimer’s disease. Contemp Clin Trials Commun 28:100950
pubmed: 35754975 pmcid: 9228283
White PJ, Moussavi Z (2016) Neurocognitive treatment for a patient with Alzheimer’s disease using a virtual reality navigational environment. J Exp Neurosci 10:S40827
Wen D, Fan Y, Hsu S-H, Xu J, Zhou Y, Tao J et al (2021) Combining brain–computer interface and virtual reality for rehabilitation in neurological diseases: a narrative review. Ann Phys Rehabil Med 64(1):101404
pubmed: 32561504
Arnold ES, Fischbeck KH (2018) Spinal muscular atrophy. Handb Clin Neurol 148:591–601
pubmed: 29478602
Lunn MR, Wang CH (2008) Spinal muscular atrophy. The Lancet 371(9630):2120–2133
Verhaart IE, Robertson A, Wilson IJ, Aartsma-Rus A, Cameron S, Jones CC et al (2017) Prevalence, incidence and carrier frequency of 5q–linked spinal muscular atrophy–a literature review. Orphanet J Rare Dis 12(1):1–15
Cincotti F, Mattia D, Aloise F, Bufalari S, Schalk G, Oriolo G et al (2008) Non-invasive brain–computer interface system: towards its application as assistive technology. Brain Res Bull 75(6):796–803
pubmed: 18394526 pmcid: 2896271
Bao S-C, Yuan K, Chen C, Lau, C, Tong RK-Y (2021) A motor imagery-based brain-computer interface scheme for a spinal muscular atrophy subject in CYBATHLON Race. In: 2021 10th International IEEE/EMBS Conference on Neural Engineering (NER), pp 532–535.  https://doi.org/10.1109/NER49283.2021.9441351
Hagengruber A, Vogel J (2018) Functional tasks performed by people with severe muscular atrophy using an semg controlled robotic manipulator. In: 2018 40th Annual International Conference of the IEEE Engineering in Medicine and Biology Society. Conf Proc IEEE Eng Med Biol Soc, pp 1713–1718.  https://doi.org/10.1109/EMBC.2018.8512703
Walker LC (2016) Proteopathic strains and the heterogeneity of neurodegenerative diseases. Annu Rev Genet 50:329
pubmed: 27893962 pmcid: 6690197
Portillo-Lara R, Tahirbegi B, Chapman CA, Goding JA, Green RA (2021) Mind the gap: State-of-the-art technologies and applications for EEG-based brain–computer interfaces. APL Bioeng 5(3):031507
pubmed: 34327294 pmcid: 8294859
Birbaumer N, Cohen LG (2007) Brain–computer interfaces: communication and restoration of movement in paralysis. J Physiol 579(3):621–636
pubmed: 17234696 pmcid: 2151357
Bronnick K, Emre M, Lane R, Tekin S, Aarsland D (2007) Profile of cognitive impairment in dementia associated with Parkinson’s disease compared with Alzheimer’s disease. J Neurol Neurosurg Psychiatry 78(10):1064–1068
pubmed: 17287236 pmcid: 2117535
Reitz C, Brayne C, Mayeux R (2011) Epidemiology of Alzheimer disease. Nat Rev Neurol 7(3):137–152
pubmed: 21304480 pmcid: 3339565
Wong W (2020) Economic burden of Alzheimer disease and managed care considerations. Am J Manag Care 26(8 Suppl):S177–SS83
pubmed: 32840331
Mokdad AH, Ballestros K, Echko M, Glenn S, Olsen HE, Mullany E et al (2018) The state of US health, 1990-2016: burden of diseases, injuries, and risk factors among US states. Jama 319(14):1444–1472
pubmed: 29634829 pmcid: 5933332
Friedman EM, Shih RA, Langa KM, Hurd MD (2015) US prevalence and predictors of informal caregiving for dementia. Health Affairs 34(10):1637–1641
pubmed: 26438738
Association As (2019) 2019 Alzheimer’s disease facts and figures. Alzheimers Dement 15(3):321–387
Lunn JS, Sakowski SA, Hur J, Feldman EL (2011) Stem cell technology for neurodegenerative diseases. Ann Neurol 70(3):353–361
pubmed: 21905078 pmcid: 3177143
Wang J, Hu W-W, Jiang Z, Feng M-J (2020) Advances in treatment of neurodegenerative diseases: perspectives for combination of stem cells with neurotrophic factors. World J Stem Cells 12(5):323
pubmed: 32547681 pmcid: 7280867
Modi G, Pillay V, Choonara YE (2010) Advances in the treatment of neurodegenerative disorders employing nanotechnology. Ann N Y Acad Sci 1184(1):154–172
pubmed: 20146696
Gu M, Owen A, Toffa S, Cooper J, Dexter D, Jenner P et al (1998) Mitochondrial function, GSH and iron in neurodegeneration and Lewy body diseases. J Neurol Sci 158(1):24–29
pubmed: 9667773
Cacciatore I, Baldassarre L, Fornasari E, Mollica A, Pinnen F (2012) Recent advances in the treatment of neurodegenerative diseases based on GSH delivery systems. Oxid Med Cell Longev 2012:240146
pubmed: 22701755 pmcid: 3372378

Auteurs

Hossein Tayebi (H)

Neurosurgical Research Network (NRN), Universal Scientific Education and Research Network (USERN), Tehran, Iran.
School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran.

Sina Azadnajafabad (S)

Neurosurgical Research Network (NRN), Universal Scientific Education and Research Network (USERN), Tehran, Iran.
Department of Surgery, Tehran University of Medical Sciences, Tehran, Iran.

Seyed Farzad Maroufi (SF)

Neurosurgical Research Network (NRN), Universal Scientific Education and Research Network (USERN), Tehran, Iran.
School of Medicine, Tehran University of Medical Sciences, Tehran, Iran.

Ahmad Pour-Rashidi (A)

Neurosurgical Research Network (NRN), Universal Scientific Education and Research Network (USERN), Tehran, Iran.
Department of Neurosurgery, Sina Hospital, Tehran University of Medical Sciences, Tehran, Iran.

MirHojjat Khorasanizadeh (M)

Department of Neurosurgery, Mount Sinai Hospital, Icahn School of Medicine, New York City, NY, USA.

Sina Faramarzi (S)

University of California, Irvine, Irvine, CA, USA.

Konstantin V Slavin (KV)

Department of Neurosurgery, University of Illinois at Chicago, Chicago, IL, 60612, USA. Kslavin@uic.edu.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH