Closed-loop stimulation of temporal cortex rescues functional networks and improves memory

Youssef Ezzyat; Paul A. Wanda; Deborah F. Levy; Allison Kadel; Ada Aka; Isaac Pedisich; Michael R. Sperling; Ashwini D. Sharan; Bradley C. Lega; Alexis Burks; Robert E. Gross; Cory S. Inman; Barbara C. Jobst; Mark A. Gorenstein; Kathryn A. Davis; Gregory A. Worrell; Michal T. Kucewicz; Joel M. Stein; Richard Gorniak; Sandhitsu R. Das; Daniel S. Rizzuto; Michael J. Kahana

doi:10.1038/s41467-017-02753-0

Closed-loop stimulation of temporal cortex rescues functional networks and improves memory

Youssef Ezzyat, Paul A. Wanda, Deborah F. Levy, Allison Kadel, Ada Aka, Isaac Pedisich, Michael R. Sperling, Ashwini D. Sharan, Bradley C. Lega, Alexis Burks, Robert E. Gross, Cory S. Inman, Barbara C. Jobst, Mark A. Gorenstein, Kathryn A. Davis, Gregory A. Worrell, Michal T. Kucewicz, Joel M. Stein, Richard Gorniak, Sandhitsu R. DasDaniel S. Rizzuto, Michael J. Kahana

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147 Scopus citations

Abstract

Memory failures are frustrating and often the result of ineffective encoding. One approach to improving memory outcomes is through direct modulation of brain activity with electrical stimulation. Previous efforts, however, have reported inconsistent effects when using open-loop stimulation and often target the hippocampus and medial temporal lobes. Here we use a closed-loop system to monitor and decode neural activity from direct brain recordings in humans. We apply targeted stimulation to lateral temporal cortex and report that this stimulation rescues periods of poor memory encoding. This system also improves later recall, revealing that the lateral temporal cortex is a reliable target for memory enhancement. Taken together, our results suggest that such systems may provide a therapeutic approach for treating memory dysfunction.

Original language	English (US)
Article number	365
Journal	Nature communications
Volume	9
Issue number	1
DOIs	https://doi.org/10.1038/s41467-017-02753-0
State	Published - Dec 1 2018

ASJC Scopus subject areas

Chemistry(all)
Biochemistry, Genetics and Molecular Biology(all)
Physics and Astronomy(all)

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10.1038/s41467-017-02753-0

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Ezzyat, Y., Wanda, P. A., Levy, D. F., Kadel, A., Aka, A., Pedisich, I., Sperling, M. R., Sharan, A. D., Lega, B. C., Burks, A., Gross, R. E., Inman, C. S., Jobst, B. C., Gorenstein, M. A., Davis, K. A., Worrell, G. A., Kucewicz, M. T., Stein, J. M., Gorniak, R., ... Kahana, M. J. (2018). Closed-loop stimulation of temporal cortex rescues functional networks and improves memory. Nature communications, 9(1), [365]. https://doi.org/10.1038/s41467-017-02753-0

Ezzyat, Y, Wanda, PA, Levy, DF, Kadel, A, Aka, A, Pedisich, I, Sperling, MR, Sharan, AD, Lega, BC, Burks, A, Gross, RE, Inman, CS, Jobst, BC, Gorenstein, MA, Davis, KA, Worrell, GA, Kucewicz, MT, Stein, JM, Gorniak, R, Das, SR, Rizzuto, DS & Kahana, MJ 2018, 'Closed-loop stimulation of temporal cortex rescues functional networks and improves memory', Nature communications, vol. 9, no. 1, 365. https://doi.org/10.1038/s41467-017-02753-0

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title = "Closed-loop stimulation of temporal cortex rescues functional networks and improves memory",

abstract = "Memory failures are frustrating and often the result of ineffective encoding. One approach to improving memory outcomes is through direct modulation of brain activity with electrical stimulation. Previous efforts, however, have reported inconsistent effects when using open-loop stimulation and often target the hippocampus and medial temporal lobes. Here we use a closed-loop system to monitor and decode neural activity from direct brain recordings in humans. We apply targeted stimulation to lateral temporal cortex and report that this stimulation rescues periods of poor memory encoding. This system also improves later recall, revealing that the lateral temporal cortex is a reliable target for memory enhancement. Taken together, our results suggest that such systems may provide a therapeutic approach for treating memory dysfunction.",

author = "Youssef Ezzyat and Wanda, {Paul A.} and Levy, {Deborah F.} and Allison Kadel and Ada Aka and Isaac Pedisich and Sperling, {Michael R.} and Sharan, {Ashwini D.} and Lega, {Bradley C.} and Alexis Burks and Gross, {Robert E.} and Inman, {Cory S.} and Jobst, {Barbara C.} and Gorenstein, {Mark A.} and Davis, {Kathryn A.} and Worrell, {Gregory A.} and Kucewicz, {Michal T.} and Stein, {Joel M.} and Richard Gorniak and Das, {Sandhitsu R.} and Rizzuto, {Daniel S.} and Kahana, {Michael J.}",

note = "Funding Information: We dedicate this paper in loving memory of Anastasia Lyalenko, without whose contributions this work would not have been possible (http://memory.psych.upenn.edu/ Anastasia_Lyalenko_Memorial_Fund). This work was supported by the DARPA Restoring Active Memory (RAM) program (Cooperative Agreement N66001-14-2-4032). We thank Blackrock Microsystems for providing neural recording and stimulation equipment. We are indebted to the patients and their families for their participation and support. The views, opinions, and/or findings contained in this material are those of the authors and should not be interpreted as representing the official views or policies of the Department of Defense or the U.S. Government. Publisher Copyright: {\textcopyright} 2018 The Author(s).",

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doi = "10.1038/s41467-017-02753-0",

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AU - Ezzyat, Youssef

AU - Wanda, Paul A.

AU - Levy, Deborah F.

AU - Kadel, Allison

AU - Aka, Ada

AU - Pedisich, Isaac

AU - Sperling, Michael R.

AU - Sharan, Ashwini D.

AU - Lega, Bradley C.

AU - Burks, Alexis

AU - Gross, Robert E.

AU - Inman, Cory S.

AU - Jobst, Barbara C.

AU - Gorenstein, Mark A.

AU - Davis, Kathryn A.

AU - Worrell, Gregory A.

AU - Kucewicz, Michal T.

AU - Stein, Joel M.

AU - Gorniak, Richard

AU - Das, Sandhitsu R.

AU - Rizzuto, Daniel S.

AU - Kahana, Michael J.

N1 - Funding Information: We dedicate this paper in loving memory of Anastasia Lyalenko, without whose contributions this work would not have been possible (http://memory.psych.upenn.edu/ Anastasia_Lyalenko_Memorial_Fund). This work was supported by the DARPA Restoring Active Memory (RAM) program (Cooperative Agreement N66001-14-2-4032). We thank Blackrock Microsystems for providing neural recording and stimulation equipment. We are indebted to the patients and their families for their participation and support. The views, opinions, and/or findings contained in this material are those of the authors and should not be interpreted as representing the official views or policies of the Department of Defense or the U.S. Government. Publisher Copyright: © 2018 The Author(s).

PY - 2018/12/1

Y1 - 2018/12/1

N2 - Memory failures are frustrating and often the result of ineffective encoding. One approach to improving memory outcomes is through direct modulation of brain activity with electrical stimulation. Previous efforts, however, have reported inconsistent effects when using open-loop stimulation and often target the hippocampus and medial temporal lobes. Here we use a closed-loop system to monitor and decode neural activity from direct brain recordings in humans. We apply targeted stimulation to lateral temporal cortex and report that this stimulation rescues periods of poor memory encoding. This system also improves later recall, revealing that the lateral temporal cortex is a reliable target for memory enhancement. Taken together, our results suggest that such systems may provide a therapeutic approach for treating memory dysfunction.

AB - Memory failures are frustrating and often the result of ineffective encoding. One approach to improving memory outcomes is through direct modulation of brain activity with electrical stimulation. Previous efforts, however, have reported inconsistent effects when using open-loop stimulation and often target the hippocampus and medial temporal lobes. Here we use a closed-loop system to monitor and decode neural activity from direct brain recordings in humans. We apply targeted stimulation to lateral temporal cortex and report that this stimulation rescues periods of poor memory encoding. This system also improves later recall, revealing that the lateral temporal cortex is a reliable target for memory enhancement. Taken together, our results suggest that such systems may provide a therapeutic approach for treating memory dysfunction.

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Closed-loop stimulation of temporal cortex rescues functional networks and improves memory

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