Closed-loop enhancement and neural decoding of cognitive control in humans

Ishita Basu; Ali Yousefi; Britni Crocker; Rina Zelmann; Angelique C. Paulk; Noam Peled; Kristen K. Ellard; Daniel S. Weisholtz; G. Rees Cosgrove; Thilo Deckersbach; Uri T. Eden; Emad N. Eskandar; Darin D. Dougherty; Sydney S. Cash; Alik S. Widge

doi:10.1038/s41551-021-00804-y

Closed-loop enhancement and neural decoding of cognitive control in humans

Ishita Basu
, Ali Yousefi
, Britni Crocker
, Rina Zelmann
, Angelique C. Paulk
, Noam Peled
, Kristen K. Ellard
, Daniel S. Weisholtz
, G. Rees Cosgrove
, Thilo Deckersbach
, Uri T. Eden
, Emad N. Eskandar
, Darin D. Dougherty
, Sydney S. Cash
, Alik S. Widge

Psychiatry & Behavioral Sciences

Research output: Contribution to journal › Article › peer-review

83 Scopus citations

Abstract

Deficits in cognitive control—that is, in the ability to withhold a default pre-potent response in favour of a more adaptive choice—are common in depression, anxiety, addiction and other mental disorders. Here we report proof-of-concept evidence that, in participants undergoing intracranial epilepsy monitoring, closed-loop direct stimulation of the internal capsule or striatum, especially the dorsal sites, enhances the participants’ cognitive control during a conflict task. We also show that closed-loop stimulation upon the detection of lapses in cognitive control produced larger behavioural changes than open-loop stimulation, and that task performance for single trials can be directly decoded from the activity of a small number of electrodes via neural features that are compatible with existing closed-loop brain implants. Closed-loop enhancement of cognitive control might remediate underlying cognitive deficits and aid the treatment of severe mental disorders.

Original language	English (US)
Pages (from-to)	576-588
Number of pages	13
Journal	Nature Biomedical Engineering
Volume	7
Issue number	4
DOIs	https://doi.org/10.1038/s41551-021-00804-y
State	Published - Apr 2023

Bibliographical note

Funding Information:
We thank A. Afzal, G. Belok, K. Farnes, J. Felicione, R. Franklin, A. Gilmour, A. Gosai, M. Moran, M. Robertson, C. Salthouse, D. Vallejo-Lopez and S. Zorowitz for technical assistance with data collection and the research participants, without whose generous help none of this would have been possible. This work was supported by grants from the Defense Advanced Research Projects Agency (DARPA) under Cooperative Agreement Number W911NF-14-2-0045 issued by the Army Research Organization (ARO) contracting office in support of DARPA’s SUBNETS Program, the National Institutes of Health (UH3NS100548, R01MH111917, R01MH086400, R01DA026297, R01EY017658, K24NS088568), Ellison Foundation, Tiny Blue Dot Foundation, MGH Executive Council on Research, OneMind Institute, and the MnDRIVE and Medical Discovery Team-Addictions initiatives at the University of Minnesota. The views, opinions and findings expressed are those of the authors. They should not be interpreted as representing the official views or policies of the Department of Defense, Department of Health and Human Services, any other branch of the US Government, or any other funding entity.

Publisher Copyright:
© 2021, The Author(s), under exclusive licence to Springer Nature Limited.

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Basu, I., Yousefi, A., Crocker, B., Zelmann, R., Paulk, A. C., Peled, N., Ellard, K. K., Weisholtz, D. S., Cosgrove, G. R., Deckersbach, T., Eden, U. T., Eskandar, E. N., Dougherty, D. D., Cash, S. S., & Widge, A. S. (2023). Closed-loop enhancement and neural decoding of cognitive control in humans. Nature Biomedical Engineering, 7(4), 576-588. https://doi.org/10.1038/s41551-021-00804-y

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title = "Closed-loop enhancement and neural decoding of cognitive control in humans",

abstract = "Deficits in cognitive control{\textemdash}that is, in the ability to withhold a default pre-potent response in favour of a more adaptive choice{\textemdash}are common in depression, anxiety, addiction and other mental disorders. Here we report proof-of-concept evidence that, in participants undergoing intracranial epilepsy monitoring, closed-loop direct stimulation of the internal capsule or striatum, especially the dorsal sites, enhances the participants{\textquoteright} cognitive control during a conflict task. We also show that closed-loop stimulation upon the detection of lapses in cognitive control produced larger behavioural changes than open-loop stimulation, and that task performance for single trials can be directly decoded from the activity of a small number of electrodes via neural features that are compatible with existing closed-loop brain implants. Closed-loop enhancement of cognitive control might remediate underlying cognitive deficits and aid the treatment of severe mental disorders.",

author = "Ishita Basu and Ali Yousefi and Britni Crocker and Rina Zelmann and Paulk, \{Angelique C.\} and Noam Peled and Ellard, \{Kristen K.\} and Weisholtz, \{Daniel S.\} and Cosgrove, \{G. Rees\} and Thilo Deckersbach and Eden, \{Uri T.\} and Eskandar, \{Emad N.\} and Dougherty, \{Darin D.\} and Cash, \{Sydney S.\} and Widge, \{Alik S.\}",

note = "Funding Information: We thank A. Afzal, G. Belok, K. Farnes, J. Felicione, R. Franklin, A. Gilmour, A. Gosai, M. Moran, M. Robertson, C. Salthouse, D. Vallejo-Lopez and S. Zorowitz for technical assistance with data collection and the research participants, without whose generous help none of this would have been possible. This work was supported by grants from the Defense Advanced Research Projects Agency (DARPA) under Cooperative Agreement Number W911NF-14-2-0045 issued by the Army Research Organization (ARO) contracting office in support of DARPA{\textquoteright}s SUBNETS Program, the National Institutes of Health (UH3NS100548, R01MH111917, R01MH086400, R01DA026297, R01EY017658, K24NS088568), Ellison Foundation, Tiny Blue Dot Foundation, MGH Executive Council on Research, OneMind Institute, and the MnDRIVE and Medical Discovery Team-Addictions initiatives at the University of Minnesota. The views, opinions and findings expressed are those of the authors. They should not be interpreted as representing the official views or policies of the Department of Defense, Department of Health and Human Services, any other branch of the US Government, or any other funding entity. Publisher Copyright: {\textcopyright} 2021, The Author(s), under exclusive licence to Springer Nature Limited.",

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doi = "10.1038/s41551-021-00804-y",

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AU - Yousefi, Ali

AU - Crocker, Britni

AU - Zelmann, Rina

AU - Paulk, Angelique C.

AU - Peled, Noam

AU - Ellard, Kristen K.

AU - Weisholtz, Daniel S.

AU - Cosgrove, G. Rees

AU - Deckersbach, Thilo

AU - Eden, Uri T.

AU - Eskandar, Emad N.

AU - Dougherty, Darin D.

AU - Cash, Sydney S.

AU - Widge, Alik S.

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N2 - Deficits in cognitive control—that is, in the ability to withhold a default pre-potent response in favour of a more adaptive choice—are common in depression, anxiety, addiction and other mental disorders. Here we report proof-of-concept evidence that, in participants undergoing intracranial epilepsy monitoring, closed-loop direct stimulation of the internal capsule or striatum, especially the dorsal sites, enhances the participants’ cognitive control during a conflict task. We also show that closed-loop stimulation upon the detection of lapses in cognitive control produced larger behavioural changes than open-loop stimulation, and that task performance for single trials can be directly decoded from the activity of a small number of electrodes via neural features that are compatible with existing closed-loop brain implants. Closed-loop enhancement of cognitive control might remediate underlying cognitive deficits and aid the treatment of severe mental disorders.

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ER -

Closed-loop enhancement and neural decoding of cognitive control in humans

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