De Novo Brain-Computer Interfacing Deforms Manifold of Populational Neural Activity Patterns in Human Cerebral Cortex.

Publisher: Society for Neuroscience Country of Publication: United States NLM ID: 101647362 Publication Model: Electronic-Print Cited Medium: Internet ISSN: 2373-2822 (Electronic) Linking ISSN: 23732822 NLM ISO Abbreviation: eNeuro Subsets: MEDLINE

Original Publication: [Washington, DC] : Society for Neuroscience, [2014]-

Electroencephalography*/methods ; Cerebral Cortex*; Humans ; Male ; Female ; Brain/physiology ; Algorithms ; Computers

Human brains are capable of modulating innate activities to adapt to novel environments and tasks; for sensorimotor neural system this means acquisition of a rich repertoire of activity patterns that improve behavioral performance. To directly map the process of acquiring the neural repertoire during tasks onto performance improvement, we analyzed net neural populational activity during the learning of its voluntary modulation by brain-computer interface (BCI) operation in female and male humans. The recorded whole-head high-density scalp electroencephalograms (EEGs) were subjected to dimensionality reduction algorithm to capture changes in cortical activity patterns represented by the synchronization of neuronal oscillations during adaptation. Although the preserved variance of targeted features in the reduced dimensions was 20%, we found systematic interactions between the activity patterns and BCI classifiers that detected motor attempt; the neural manifold derived in the embedded space was stretched along with motor-related features of EEG by model-based fixed classifiers but not with adaptive classifiers that were constantly recalibrated to user activity. Moreover, the manifold was deformed to be orthogonal to the boundary by de novo classifiers with a fixed decision boundary based on biologically unnatural features. Collectively, the flexibility of human cortical signaling patterns (i.e., neural plasticity) is only induced by operation of a BCI whose classifier required fixed activities, and the adaptation could be induced even the requirement is not consistent with biologically natural responses. These principles of neural adaptation at a macroscopic level may underlie the ability of humans to learn wide-ranging behavioral repertoires and adapt to novel environments.
Competing Interests: J.U. is a founder and representative director of the university startup company, LIFESCAPES Inc., involved in the research, development, and sales of rehabilitation devices including brain-computer interfaces, he receives a salary from LIFESCAPES Inc., and holds shares in LIFESCAPES Inc. This company does not have any relationships with the device or setup used in the current study. All other authors declare no competing financial interests.
(Copyright © 2022 Iwama et al.)

Nature. 1995 Sep 14;377(6545):155-8. (PMID: 7675082)
Neuroimage. 2020 Apr 1;209:116500. (PMID: 31927130)
Neuron. 2018 Nov 21;100(4):964-976.e7. (PMID: 30344047)
Cereb Cortex. 2020 Jan 10;30(1):371-381. (PMID: 31204431)
Nat Commun. 2018 Oct 12;9(1):4233. (PMID: 30315158)
Neurosci Biobehav Rev. 2014 Jul;44:159-82. (PMID: 24690579)
Brain. 2002 Feb;125(Pt 2):404-20. (PMID: 11844740)
Clin Neurophysiol. 1999 Nov;110(11):1842-57. (PMID: 10576479)
Behav Res Methods. 2007 May;39(2):175-91. (PMID: 17695343)
J Neurosci. 2004 Jan 21;24(3):628-33. (PMID: 14736848)
Nat Neurosci. 2020 Feb;23(2):260-270. (PMID: 31907438)
J Neurophysiol. 2013 Sep;110(5):1158-66. (PMID: 23761697)
Neuropsychologia. 2014 Apr;56:393-400. (PMID: 24561034)
Science. 2011 Dec 9;334(6061):1413-5. (PMID: 22158821)
Nat Neurosci. 2019 Sep;22(9):1512-1520. (PMID: 31406365)
Neuroimage. 2019 Oct 1;199:127-142. (PMID: 31132450)
Nat Neurosci. 2002 Nov;5(11):1226-35. (PMID: 12404008)
J Neurosci. 1996 Jan 15;16(2):785-807. (PMID: 8551360)
Sci Rep. 2019 Mar 22;9(1):5030. (PMID: 30903012)
Nature. 2000 Jan 13;403(6766):192-5. (PMID: 10646603)
Neuroimage. 2018 Nov 1;181:797-806. (PMID: 30010005)
Neuroimage. 2020 Dec;223:117298. (PMID: 32828924)
Front Neuroinform. 2015 Jun 18;9:16. (PMID: 26150785)
Proc Natl Acad Sci U S A. 2020 Sep 22;117(38):23886-23897. (PMID: 32900934)
Philos Trans R Soc Lond B Biol Sci. 2012 Apr 5;367(1591):906-18. (PMID: 22371613)
Neuroimage. 2019 Jul 1;194:283-290. (PMID: 30898654)
Neuroimage. 2006 May 15;31(1):153-9. (PMID: 16443377)
Proc Natl Acad Sci U S A. 2019 Jul 23;116(30):15210-15215. (PMID: 31182595)
Nature. 2014 Aug 28;512(7515):423-6. (PMID: 25164754)
Neuron. 2014 Jan 8;81(1):35-48. (PMID: 24411730)
Sci Robot. 2021 May 19;6(54):. (PMID: 34043536)
PLoS Biol. 2018 May 10;16(5):e2003787. (PMID: 29746465)
Sci Robot. 2019 Jun 26;4(31):. (PMID: 31656937)
Neuroimage. 2019 Jan 1;184:36-44. (PMID: 30205210)
Proc Natl Acad Sci U S A. 2009 Oct 27;106(43):18379-84. (PMID: 19820167)
Cereb Cortex. 2015 Sep;25(9):2409-15. (PMID: 24626608)
Neuroimage. 2019 Sep;198:181-197. (PMID: 31103785)
Neuroimage. 2007 Aug 15;37(2):539-50. (PMID: 17475513)
Nat Commun. 2021 Jan 27;12(1):633. (PMID: 33504773)
Neural Netw. 2021 Oct;142:583-596. (PMID: 34352492)
Lancet Neurol. 2019 Dec;18(12):1112-1122. (PMID: 31587955)
J Neural Eng. 2013 Oct;10(5):056014. (PMID: 23985960)
Nat Neurosci. 2018 Apr;21(4):607-616. (PMID: 29531364)
Brain. 2018 May 1;141(5):e40. (PMID: 29547965)
J Neurophysiol. 2008 Oct;100(4):2397-408. (PMID: 18667540)
Nat Rev Neurosci. 2004 Jul;5(7):532-46. (PMID: 15208695)
Sci Robot. 2018 Jul 25;3(20):. (PMID: 33141729)
Nat Neurosci. 2014 Nov;17(11):1500-9. (PMID: 25151264)
Methods Find Exp Clin Pharmacol. 2002;24 Suppl D:5-12. (PMID: 12575463)
Cogn Neurosci. 2019 Jan;10(1):30-43. (PMID: 29327652)
Hum Brain Mapp. 2002 Jan;15(1):1-25. (PMID: 11747097)
Proc Natl Acad Sci U S A. 2004 Dec 21;101(51):17849-54. (PMID: 15585584)
J Neurosci. 2005 Oct 26;25(43):9919-31. (PMID: 16251440)
Nature. 2001 Nov 22;414(6862):446-9. (PMID: 11719805)
Stroke. 2008 Mar;39(3):910-7. (PMID: 18258825)
Neuron. 2015 Oct 7;88(1):220-35. (PMID: 26447583)
Nat Neurosci. 2015 May;18(5):744-51. (PMID: 25849989)
J Neurosci Methods. 2021 Apr 1;353:109089. (PMID: 33508408)
Proc Natl Acad Sci U S A. 2013 Jun 25;110(26):10818-23. (PMID: 23754426)
Neuroimage. 2016 Jan 15;125:522-532. (PMID: 26505298)
J Neurosci. 2014 Oct 8;34(41):13768-79. (PMID: 25297103)
Nat Commun. 2019 Jun 3;10(1):2401. (PMID: 31160580)
Nat Neurosci. 2021 May;24(5):727-736. (PMID: 33782622)
Elife. 2020 May 13;9:. (PMID: 32401193)
Electroencephalogr Clin Neurophysiol. 1997 Sep;103(3):386-94. (PMID: 9305287)
Sci Rep. 2021 Sep 16;11(1):18487. (PMID: 34531441)
Neuron. 2014 Jun 18;82(6):1380-93. (PMID: 24945777)
Nat Biotechnol. 2021 Mar;39(3):326-335. (PMID: 32895549)
J Neurosci Methods. 2004 Mar 15;134(1):9-21. (PMID: 15102499)

Keywords: brain-computer interface; de novo learning; neural plasticity; nonlinear dimensionality reduction; sensorimotor activity

Date Created: 20221114 Date Completed: 20221130 Latest Revision: 20221222

20231215

PMC9721308

10.1523/ENEURO.0145-22.2022

36376067