Intracortical brain-computer interfaces for improved motor function: a systematic review.
brain-computer interface
brain-machine interface
implant
intracortical
motor cortex
Journal
Reviews in the neurosciences
ISSN: 2191-0200
Titre abrégé: Rev Neurosci
Pays: Germany
ID NLM: 8711016
Informations de publication
Date de publication:
17 Oct 2023
17 Oct 2023
Historique:
received:
18
07
2023
accepted:
23
09
2023
medline:
17
10
2023
pubmed:
17
10
2023
entrez:
17
10
2023
Statut:
aheadofprint
Résumé
In this systematic review, we address the status of intracortical brain-computer interfaces (iBCIs) applied to the motor cortex to improve function in patients with impaired motor ability. This study followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) 2020 Guidelines for Systematic Reviews. Risk Of Bias In Non-randomized Studies - of Interventions (ROBINS-I) and the Effective Public Health Practice Project (EPHPP) were used to assess bias and quality. Advances in iBCIs in the last two decades demonstrated the use of iBCI to activate limbs for functional tasks, achieve neural typing for communication, and other applications. However, the inconsistency of performance metrics employed by these studies suggests the need for standardization. Each study was a pilot clinical trial consisting of 1-4, majority male (64.28 %) participants, with most trials featuring participants treated for more than 12 months (55.55 %). The systems treated patients with various conditions: amyotrophic lateral sclerosis, stroke, spinocerebellar degeneration without cerebellar involvement, and spinal cord injury. All participants presented with tetraplegia at implantation and were implanted with microelectrode arrays via pneumatic insertion, with nearly all electrode locations solely at the precentral gyrus of the motor cortex (88.88 %). The development of iBCI devices using neural signals from the motor cortex to improve motor-impaired patients has enhanced the ability of these systems to return ability to their users. However, many milestones remain before these devices can prove their feasibility for recovery. This review summarizes the achievements and shortfalls of these systems and their respective trials.
Identifiants
pubmed: 37845811
pii: revneuro-2023-0077
doi: 10.1515/revneuro-2023-0077
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2023 Walter de Gruyter GmbH, Berlin/Boston.
Références
Ajiboye, A.B., Willett, F.R., Young, D.R., Memberg, W.D., Murphy, B.A., Miller, J.P., Walter, B.L., Sweet, J.A., Hoyen, H.A., Keith, M.W., et al.. (2017). Restoration of reaching and grasping movements through brain-controlled muscle stimulation in a person with tetraplegia: a proof-of-concept demonstration. Lancet 389: 1821–1830, https://doi.org/10.1016/s0140-6736(17)30601-3 .
doi: 10.1016/s0140-6736(17)30601-3
Annetta, N.V., Zhang, M., Mysiw, W.J., Rezai, A.R., Sharma, G., Friend, J., Schimmoeller, A., Buck, V.S., Friedenberg, D.A., Bouton, C.E., et al.. (2019). A high definition noninvasive neuromuscular electrical stimulation system for cortical control of combinatorial rotary hand movements in a human with tetraplegia. IEEE Trans. Biomed. Eng. 66: 910–919, https://doi.org/10.1109/tbme.2018.2864104 .
doi: 10.1109/tbme.2018.2864104
Bacher, D., Jarosiewicz, B., Masse, N.Y., Stavisky, S.D., Simeral, J.D., Newell, K., Oakley, E.M., Cash, S.S., Friehs, G., and Hochberg, L.R. (2015). Neural point-and-click communication by a person with incomplete locked-in syndrome. Neurorehabilitation Neural Repair 29: 462–471, https://doi.org/10.1177/1545968314554624 .
doi: 10.1177/1545968314554624
Bockbrader, M., Annetta, N., Friedenberg, D., Schwemmer, M., Skomrock, N., Colachis, S., Zhang, M., Bouton, C., Rezai, A., Sharma, G., et al.. (2019). Clinically significant gains in skillful grasp coordination by an individual with tetraplegia using an implanted brain-computer interface with forearm transcutaneous muscle stimulation. Arch. Phys. Med. Rehabil. 100: 1201–1217, https://doi.org/10.1016/j.apmr.2018.07.445 .
doi: 10.1016/j.apmr.2018.07.445
Bouton, C.E., Shaikhouni, A., Annetta, N.V., Bockbrader, M.A., Friedenberg, D.A., Nielson, D.M., Sharma, G., Sederberg, P.B., Glenn, B.C., Mysiw, W.J., et al.. (2016). Restoring cortical control of functional movement in a human with quadriplegia. Nature 533: 247–250, https://doi.org/10.1038/nature17435 .
doi: 10.1038/nature17435
Brandman, D.M., Hosman, T., Saab, J., Burkhart, M.C., Shanahan, B.E., Ciancibello, J.G., Sarma, A.A., Milstein, D.J., Vargas-Irwin, C.E., Franco, B., et al.. (2018). Rapid calibration of an intracortical brain–computer interface for people with tetraplegia. J. Neural. Eng. 15: 026007, https://doi.org/10.1088/1741-2552/aa9ee7 .
doi: 10.1088/1741-2552/aa9ee7
Buzsàki, G., Bickford, R.G., Ryan, L.J., Young, S., Prohaska, O., Mandel, R.J., and Gage, F.H. (1989). Multisite recording of brain field potentials and unit activity in freely moving rats. J. Neurosci. Methods 28: 209–217, https://doi.org/10.1016/0165-0270(89)90038-1 .
doi: 10.1016/0165-0270(89)90038-1
Colachis, S.C., Bockbrader, M.A., Zhang, M., Friedenberg, D.A., Annetta, N.V., Schwemmer, M.A., Skomrock, N.D., Mysiw, W.J., Rezai, A.R., Bresler, H.S., et al.. (2018). Dexterous control of seven functional hand movements using cortically-controlled transcutaneous muscle stimulation in a person with tetraplegia. Front. Neurosci. 12: 208, https://doi.org/10.3389/fnins.2018.00208 .
doi: 10.3389/fnins.2018.00208
Collinger, J.L., Gaunt, R.A., and Schwartz, A.B. (2018). Progress towards restoring upper limb movement and sensation through intracortical brain-computer interfaces. Curr. Opin. Biomed. Eng. 8: 84–92, https://doi.org/10.1016/j.cobme.2018.11.005 .
doi: 10.1016/j.cobme.2018.11.005
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., and Schwartz, A.B. (2013). High-performance neuroprosthetic control by an individual with tetraplegia. Lancet 381: 557–564, https://doi.org/10.1016/s0140-6736(12)61816-9 .
doi: 10.1016/s0140-6736(12)61816-9
Downey, J.E., Brane, L., Gaunt, R.A., Tyler-Kabara, E.C., Boninger, M.L., and Collinger, J.L. (2017). Motor cortical activity changes during neuroprosthetic-controlled object interaction. Sci. Rep. 7: 16947, https://doi.org/10.1038/s41598-017-17222-3 .
doi: 10.1038/s41598-017-17222-3
Downey, J.E., Weiss, J.M., Flesher, S.N., Thumser, Z.C., Marasco, P.D., Boninger, M.L., Gaunt, R.A., and Collinger, J.L. (2018). Implicit grasp force representation in human motor cortical recordings. Front. Neurosci. 12: 801, https://doi.org/10.3389/fnins.2018.00801 .
doi: 10.3389/fnins.2018.00801
Downey, J.E., Weiss, J.M., Muelling, K., Venkatraman, A., Valois, J.-S., Hebert, M., Bagnell, J.A., Schwartz, A.B., and Collinger, J.L. (2016). Blending of brain-machine interface and vision-guided autonomous robotics improves neuroprosthetic arm performance during grasping. J. NeuroEng. Rehabil. 13: 28, https://doi.org/10.1186/s12984-016-0134-9 .
doi: 10.1186/s12984-016-0134-9
Fatima, N., Shuaib, A., and Saqqur, M. (2020). Intra-cortical brain-machine interfaces for controlling upper-limb powered muscle and robotic systems in spinal cord injury. Clin. Neurol. Neurosurg. 196: 106069, https://doi.org/10.1016/j.clineuro.2020.106069 .
doi: 10.1016/j.clineuro.2020.106069
Fitzsimmons, N.A. (2009). Extracting kinematic parameters for monkey bipedal walking from cortical neuronal ensemble activity. Front. Integr. Neurosci. 3: 1–19, https://doi.org/10.3389/neuro.07.003.2009 .
doi: 10.3389/neuro.07.003.2009
Flesher, S.N., Downey, J.E., Weiss, J.M., Hughes, C.L., Herrera, A.J., Tyler-Kabara, E.C., Boninger, M.L., Collinger, J.L., and Gaunt, R.A. (2021). A brain-computer interface that evokes tactile sensations improves robotic arm control. Science 372: 831–836, https://doi.org/10.1126/science.abd0380 .
doi: 10.1126/science.abd0380
Frank, K. (1971). Use of neural signals to control external device. Neurosci. Res. Prog. Bull. 9: 113–118.
Friedenberg, D.A., Schwemmer, M.A., Landgraf, A.J., Annetta, N.V., Bockbrader, M.A., Bouton, C.E., Zhang, M., Rezai, A.R., Mysiw, W.J., Bresler, H.S., et al.. (2017). Neuroprosthetic-enabled control of graded arm muscle contraction in a paralyzed human. Sci. Rep. 7: 8386, https://doi.org/10.1038/s41598-017-08120-9 .
doi: 10.1038/s41598-017-08120-9
Gilja, V., Pandarinath, C., Blabe, C.H., Nuyujukian, P., Simeral, J.D., Sarma, A.A., Sorice, B.L., Perge, J.A., Jarosiewicz, B., Hochberg, L.R., et al.. (2015). Clinical translation of a high-performance neural prosthesis. Nat. Med. 21: 1142–1145, https://doi.org/10.1038/nm.3953 .
doi: 10.1038/nm.3953
Hochberg, L.R., Bacher, D., Jarosiewicz, B., Masse, N.Y., Simeral, J.D., Vogel, J., Haddadin, S., Liu, J., Cash, S.S., Van Der Smagt, P., et al.. (2012). Reach and grasp by people with tetraplegia using a neurally controlled robotic arm. Nature 485: 372–375, https://doi.org/10.1038/nature11076 .
doi: 10.1038/nature11076
Hochberg, L.R., Serruya, M.D., Friehs, G.M., Mukand, J.A., Saleh, M., Caplan, A.H., Branner, A., Chen, D., Penn, R.D., and Donoghue, J.P. (2006). Neuronal ensemble control of prosthetic devices by a human with tetraplegia. Nature 442: 164–171, https://doi.org/10.1038/nature04970 .
doi: 10.1038/nature04970
Jackson, N. and Waters, E. (2005). Criteria for the systematic review of health promotion and public health interventions. Health Promot. Int. 20: 367–374, https://doi.org/10.1093/heapro/dai022 .
doi: 10.1093/heapro/dai022
Jarosiewicz, B., Masse, N.Y., Bacher, D., Cash, S.S., Eskandar, E., Friehs, G., Donoghue, J.P., and Hochberg, L.R. (2013). Advantages of closed-loop calibration in intracortical brain–computer interfaces for people with tetraplegia. J. Neural. Eng. 10: 046012, https://doi.org/10.1088/1741-2560/10/4/046012 .
doi: 10.1088/1741-2560/10/4/046012
Jarosiewicz, B., Sarma, A.A., Bacher, D., Masse, N.Y., Simeral, J.D., Sorice, B., Oakley, E.M., Blabe, C., Pandarinath, C., Gilja, V., et al. (2015). Virtual typing by people with tetraplegia using a self-calibrating intracortical brain-computer interface. Sci. Transl. Med. 313: 1–10, https://doi.org/10.1126/scitranslmed.aac7328 .
doi: 10.1126/scitranslmed.aac7328
Lebedev, M.A., Carmena, J.M., O’Doherty, J.E., Zacksenhouse, M., Henriquez, C.S., Principe, J.C., and Nicolelis, M.A.L. (2005). Cortical ensemble adaptation to represent velocity of an artificial actuator controlled by a brain-machine interface. J. Neurosci. 25: 4681–4693, https://doi.org/10.1523/jneurosci.4088-04.2005 .
doi: 10.1523/jneurosci.4088-04.2005
Lebedev, M.A. and Nicolelis, M.A.L. (2017). Brain-machine interfaces: from basic science to neuroprostheses and neurorehabilitation. Physiol. Rev. 97: 767–837, https://doi.org/10.1152/physrev.00027.2016 .
doi: 10.1152/physrev.00027.2016
Moses, D.A., Metzger, S.L., Liu, J.R., Anumanchipalli, G.K., Makin, J.G., Sun, P.F., Chartier, J., Dougherty, M.E., Liu, P.M., Abrams, G.M., et al.. (2021). Neuroprosthesis for decoding speech in a paralyzed person with anarthria. N. Engl. J. Med. 385: 217–227, https://doi.org/10.1056/nejmoa2027540 .
doi: 10.1056/nejmoa2027540
Nicolelis, M.A., Baccala, L.A., Lin, R.C., and Chapin, J.K. (1995). Sensorimotor encoding by synchronous neural ensemble activity at multiple levels of the somatosensory system. Science 268: 1353–1358, https://doi.org/10.1126/science.7761855 .
doi: 10.1126/science.7761855
Nicolelis, M.A.L., Ghazanfar, A.A., Stambaugh, C.R., Oliveira, L.M.O., Laubach, M., Chapin, J.K., Nelson, R.J., and Kaas, J.H. (1998). Simultaneous encoding of tactile information by three primate cortical areas. Nat. Neurosci. 1: 621–630, https://doi.org/10.1038/2855 .
doi: 10.1038/2855
Nicolelis, M.A., Lin, R.C., Woodward, D.J., and Chapin, J.K. (1993a). Dynamic and distributed properties of many-neuron ensembles in the ventral posterior medial thalamus of awake rats. Proc. Natl. Acad. Sci. U.S.A. 90: 2212–2216, https://doi.org/10.1073/pnas.90.6.2212 .
doi: 10.1073/pnas.90.6.2212
Nicolelis, M.A., Lin, R.C., Woodward, D.J., and Chapin, J.K. (1993b). Induction of immediate spatiotemporal changes in thalamic networks by peripheral block of ascending cutaneous information. Nature 361: 533–536, https://doi.org/10.1038/361533a0 .
doi: 10.1038/361533a0
Nowlis, D.P. and Kamiya, J. (1970). The control of electroencephalographic alpha rhythms through auditory feedback and the associated mental activity. Psychophysiology 6: 476–484, https://doi.org/10.1111/j.1469-8986.1970.tb01756.x .
doi: 10.1111/j.1469-8986.1970.tb01756.x
Nowlis, D.P. and Wortz, E.C. (1973). Control of the ratio of midline parietal to midline frontal EEG alpha rhythms through auditory feedback. Percept. Mot. Skills 37: 815–824, https://doi.org/10.1177/003151257303700329 .
doi: 10.1177/003151257303700329
Nuyujukian, P., Albites Sanabria, J., Saab, J., Pandarinath, C., Jarosiewicz, B., Blabe, C.H., Franco, B., Mernoff, S.T., Eskandar, E.N., Simeral, J.D., et al.. (2018). Cortical control of a tablet computer by people with paralysis. PLoS One 13: e0204566, https://doi.org/10.1371/journal.pone.0204566 .
doi: 10.1371/journal.pone.0204566
O’Doherty, J.E., Lebedev, M.A., Ifft, P.J., Zhuang, K.Z., Shokur, S., Bleuler, H., and Nicolelis, M.A.L. (2011). Active tactile exploration using a brain-machine-brain interface. Nature 479: 228–231, https://doi.org/10.1038/nature10489 .
doi: 10.1038/nature10489
Ouzzani, M., Hammady, H., Fedorowicz, Z., and Elmagarmid, A. (2016). Rayyan—a web and mobile app for systematic reviews. Syst. Rev. 5: 210, https://doi.org/10.1186/s13643-016-0384-4 .
doi: 10.1186/s13643-016-0384-4
Page, M.J., McKenzie, J.E., Bossuyt, P.M., Boutron, I., Hoffmann, T.C., Mulrow, C.D., Shamseer, L., Tetzlaff, J.M., Akl, E.A., Brennan, S.E., et al. (2021). The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. Br. Med. J. 372: n71, https://doi.org/10.1136/bmj.n71 .
doi: 10.1136/bmj.n71
Pandarinath, C., Nuyujukian, P., Blabe, C.H., Sorice, B.L., Saab, J., Willett, F.R., Hochberg, L.R., Shenoy, K.V., and Henderson, J.M. (2017). High performance communication by people with paralysis using an intracortical brain-computer interface. ELife 6: e18554, https://doi.org/10.7554/elife.18554 .
doi: 10.7554/elife.18554
Patil, P.G., Carmena, J.M., Nicolelis, M.A.L., and Turner, D.A. (2004). Ensemble recordings of human subcortical neurons as a source of motor control signals for a brain-machine interface. Neurosurgery 55: 27–35; discussion 35–38, https://doi.org/10.1227/01.neu.0000126872.23715.e5 .
doi: 10.1227/01.neu.0000126872.23715.e5
Quick, K.M., Weiss, J.M., Clemente, F., Gaunt, R.A., and Collinger, J.L. (2020). Intracortical microstimulation feedback improves grasp force accuracy in a human using a brain-computer interface. In: 2020 42nd annual international conference of the IEEE engineering in medicine and biology society (EMBC) , pp. 3355–3358.
Schmidt, E.M. (1993). Cortical control of robotic devices and neuromuscular stimulators. In: Neurobionics . Elsevier, Amsterdam, pp. 289–295.
Sharma, G., Friedenberg, D.A., Annetta, N., Glenn, B., Bockbrader, M., Majstorovic, C., Domas, S., Mysiw, W.J., Rezai, A., and Bouton, C. (2016). Using an artificial neural bypass to restore cortical control of rhythmic movements in a human with quadriplegia. Sci. Rep. 6: 33807, https://doi.org/10.1038/srep33807 .
doi: 10.1038/srep33807
Shih, J.J., Krusienski, D.J., and Wolpaw, J.R. (2012). Brain-computer interfaces in medicine. Mayo Clin. Proc. 87: 268–279, https://doi.org/10.1016/j.mayocp.2011.12.008 .
doi: 10.1016/j.mayocp.2011.12.008
Simeral, J.D., Hosman, T., Saab, J., Flesher, S.N., Vilela, M., Franco, B., Kelemen, J.N., Brandman, D.M., Ciancibello, J.G., Rezaii, P.G., et al.. (2021). Home use of a percutaneous wireless intracortical brain-computer interface by individuals with tetraplegia. IEEE Trans. Biomed. Eng. 68: 2313–2325, https://doi.org/10.1109/tbme.2021.3069119 .
doi: 10.1109/tbme.2021.3069119
Stavisky, S.D., Willett, F.R., Wilson, G.H., Murphy, B.A., Rezaii, P., Avansino, D.T., Memberg, W.D., Miller, J.P., Kirsch, R.F., Hochberg, L.R., et al.. (2019). Neural ensemble dynamics in dorsal motor cortex during speech in people with paralysis. eLife 8: e46015, https://doi.org/10.7554/elife.46015 .
doi: 10.7554/elife.46015
Sterman, M.B. (1973). Neurophysiologic and clinical studies of sensorimotor EEG biofeedback training: some effects on epilepsy. Semin. Psychiatr. 5: 507–525.
Sterman, M.B. (1981). EEG biofeedback: physiological behavior modification. Neurosci. Biobehav. Rev. 5: 405–412, https://doi.org/10.1016/0149-7634(81)90036-1 .
doi: 10.1016/0149-7634(81)90036-1
Sterman, M.B. and Friar, L. (1972). Suppression of seizures in an epileptic following sensorimotor EEG feedback training. Electroencephalogr. Clin. Neurophysiol. 33: 89–95, https://doi.org/10.1016/0013-4694(72)90028-4 .
doi: 10.1016/0013-4694(72)90028-4
Sterman, M.B., Macdonald, L.R., and Stone, R.K. (1974). Biofeedback training of the sensorimotor electroencephalogram rhythm in man: effects on epilepsy. Epilepsia 15: 395–416, https://doi.org/10.1111/j.1528-1157.1974.tb04016.x .
doi: 10.1111/j.1528-1157.1974.tb04016.x
Thompson, D.E., Quitadamo, L.R., Mainardi, L., Laghari, K.U.R., Gao, S., Kindermans, P.-J., Simeral, J.D., Fazel-Rezai, R., Matteucci, M., Falk, T.H., et al.. (2014). Performance measurement for brain–computer or brain–machine interfaces: a tutorial. J. Neural. Eng. 11: 035001, https://doi.org/10.1088/1741-2560/11/3/035001 .
doi: 10.1088/1741-2560/11/3/035001
Wessberg, J., Stambaugh, C.R., Kralik, J.D., Beck, P.D., Laubach, M., Chapin, J.K., Kim, J., Biggs, S.J., Srinivasan, M.A., and Nicolelis, M.A.L. (2000). Real-time prediction of hand trajectory by ensembles of cortical neurons in primates. Nature 408: 361–365, https://doi.org/10.1038/35042582 .
doi: 10.1038/35042582
Willett, F.R., Avansino, D.T., Hochberg, L.R., Henderson, J.M., and Shenoy, K.V. (2021). High-performance brain-to-text communication via handwriting. Nature 593: 249–254, https://doi.org/10.1038/s41586-021-03506-2 .
doi: 10.1038/s41586-021-03506-2
Wodlinger, B., Downey, J.E., Tyler-Kabara, E.C., Schwartz, A.B., Boninger, M.L., and Collinger, J.L. (2015). Ten-dimensional anthropomorphic arm control in a human brain−machine interface: difficulties, solutions, and limitations. J. Neural. Eng. 12: 016011, https://doi.org/10.1088/1741-2560/12/1/016011 .
doi: 10.1088/1741-2560/12/1/016011
Woeppel, K., Hughes, C., Herrera, A.J., Eles, J.R., Tyler-Kabara, E.C., Gaunt, R.A., Collinger, J.L., and Cui, X.T. (2021). Explant analysis of Utah electrode arrays implanted in human cortex for brain-computer-interfaces. Front. Bioeng. Biotechnol. 9: 759711, https://doi.org/10.3389/fbioe.2021.759711 .
doi: 10.3389/fbioe.2021.759711