A nonlinear model for hippocampal cognitive prosthesis: Memory facilitation by hippocampal ensemble stimulation

Robert E. Hampson; Dong Song; Rosa H.M. Chan; Andrew J. Sweatt; Mitchell R. Riley; Gregory A. Gerhardt; Dae C. Shin; Vasilis Z. Marmarelis; Theodore W. Berger; Samuel A. Deadwyler

doi:10.1109/TNSRE.2012.2189163

A nonlinear model for hippocampal cognitive prosthesis: Memory facilitation by hippocampal ensemble stimulation

Robert E. Hampson, Dong Song, Rosa H.M. Chan, Andrew J. Sweatt, Mitchell R. Riley, Gregory A. Gerhardt, Dae C. Shin, Vasilis Z. Marmarelis, Theodore W. Berger, Samuel A. Deadwyler

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

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Abstract

Collaborative investigations have characterized how multineuron hippocampal ensembles encode memory necessary for subsequent successful performance by rodents in a delayed nonmatch to sample (DNMS) task and utilized that information to provide the basis for a memory prosthesis to enhance performance. By employing a unique nonlinear dynamic multi-input/multi-output (MIMO) model, developed and adapted to hippocampal neural ensemble firing patterns derived from simultaneous recorded CA1 and CA3 activity, it was possible to extract information encoded in the sample phase necessary for successful performance in the nonmatch phase of the task. The extension of this MIMO model to online delivery of electrical stimulation delivered to the same recording loci that mimicked successful CA1 firing patterns, provided the means to increase levels of performance on a trial-by-trial basis. Inclusion of several control procedures provides evidence for the specificity of effective MIMO model generated patterns of electrical stimulation. Increased utility of the MIMO model as a prosthesis device was exhibited by the demonstration of cumulative increases in DNMS task performance with repeated MIMO stimulation over many sessions on both stimulation and nonstimulation trials, suggesting overall system modification with continued exposure. Results reported here are compatible with and extend prior demonstrations and further support the candidacy of the MIMO model as an effective cortical prosthesis.

Original language	English
Article number	6171069
Pages (from-to)	184-197
Number of pages	14
Journal	IEEE Transactions on Neural Systems and Rehabilitation Engineering
Volume	20
Issue number	2
DOIs	https://doi.org/10.1109/TNSRE.2012.2189163
State	Published - Mar 2012

Bibliographical note

Funding Information:
Manuscript received September 11, 2011. Date of current version March 16, 2012. This work was supported by The Defense Advanced Research Projects Agency (Contract N66601-09-C-2080 to S. A. Deadwyler and N66601-09-C-2081 to T. W. Berger). The views, opinions, and/or findings contained in this paper are those of the author and should not be interpreted as representing the official views or policies, either expressed or implied, of the Defense Advanced Research Projects Agency or the Department of Defense. This work was also supported in part by grants National Science Foundation (NSF) EEC-0310723 to University of Southern California (USC) (T. W. Berger), National Institutes of Health/National Institute of Biomedical Imaging and Bioengineering (NIH/NIBIB) under Grant P41-EB001978 to the Biomedical Simulations Resource at USC (V. Z. Marmarelis and T. W. Berger), and NIH R01DA07625 (S. A. Deadwyler).

Funding

Manuscript received September 11, 2011. Date of current version March 16, 2012. This work was supported by The Defense Advanced Research Projects Agency (Contract N66601-09-C-2080 to S. A. Deadwyler and N66601-09-C-2081 to T. W. Berger). The views, opinions, and/or findings contained in this paper are those of the author and should not be interpreted as representing the official views or policies, either expressed or implied, of the Defense Advanced Research Projects Agency or the Department of Defense. This work was also supported in part by grants National Science Foundation (NSF) EEC-0310723 to University of Southern California (USC) (T. W. Berger), National Institutes of Health/National Institute of Biomedical Imaging and Bioengineering (NIH/NIBIB) under Grant P41-EB001978 to the Biomedical Simulations Resource at USC (V. Z. Marmarelis and T. W. Berger), and NIH R01DA07625 (S. A. Deadwyler).

Funders	Funder number
National Science Foundation (NSF)	EEC-0310723
National Institutes of Health (NIH)
National Institute on Drug Abuse	R01DA007625
National Institute of Biomedical Imaging and Bioengineering	P41-EB001978
Defense Advanced Research Projects Agency	N66601-09-C-2080, N66601-09-C-2081
University of Southern California

Keywords

Closed-loop feedback
cortical neural prosthesis
delayed memory task
hippocampal ensemble activity
neural stimulation
nonlinear mathematical model
performance enhancement

ASJC Scopus subject areas

Rehabilitation
General Neuroscience
Internal Medicine
Biomedical Engineering

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10.1109/TNSRE.2012.2189163

Cite this

Hampson, R. E., Song, D., Chan, R. H. M., Sweatt, A. J., Riley, M. R., Gerhardt, G. A., Shin, D. C., Marmarelis, V. Z., Berger, T. W., & Deadwyler, S. A. (2012). A nonlinear model for hippocampal cognitive prosthesis: Memory facilitation by hippocampal ensemble stimulation. IEEE Transactions on Neural Systems and Rehabilitation Engineering, 20(2), 184-197. Article 6171069. https://doi.org/10.1109/TNSRE.2012.2189163

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title = "A nonlinear model for hippocampal cognitive prosthesis: Memory facilitation by hippocampal ensemble stimulation",

abstract = "Collaborative investigations have characterized how multineuron hippocampal ensembles encode memory necessary for subsequent successful performance by rodents in a delayed nonmatch to sample (DNMS) task and utilized that information to provide the basis for a memory prosthesis to enhance performance. By employing a unique nonlinear dynamic multi-input/multi-output (MIMO) model, developed and adapted to hippocampal neural ensemble firing patterns derived from simultaneous recorded CA1 and CA3 activity, it was possible to extract information encoded in the sample phase necessary for successful performance in the nonmatch phase of the task. The extension of this MIMO model to online delivery of electrical stimulation delivered to the same recording loci that mimicked successful CA1 firing patterns, provided the means to increase levels of performance on a trial-by-trial basis. Inclusion of several control procedures provides evidence for the specificity of effective MIMO model generated patterns of electrical stimulation. Increased utility of the MIMO model as a prosthesis device was exhibited by the demonstration of cumulative increases in DNMS task performance with repeated MIMO stimulation over many sessions on both stimulation and nonstimulation trials, suggesting overall system modification with continued exposure. Results reported here are compatible with and extend prior demonstrations and further support the candidacy of the MIMO model as an effective cortical prosthesis.",

keywords = "Closed-loop feedback, cortical neural prosthesis, delayed memory task, hippocampal ensemble activity, neural stimulation, nonlinear mathematical model, performance enhancement",

author = "Hampson, {Robert E.} and Dong Song and Chan, {Rosa H.M.} and Sweatt, {Andrew J.} and Riley, {Mitchell R.} and Gerhardt, {Gregory A.} and Shin, {Dae C.} and Marmarelis, {Vasilis Z.} and Berger, {Theodore W.} and Deadwyler, {Samuel A.}",

note = "Funding Information: Manuscript received September 11, 2011. Date of current version March 16, 2012. This work was supported by The Defense Advanced Research Projects Agency (Contract N66601-09-C-2080 to S. A. Deadwyler and N66601-09-C-2081 to T. W. Berger). The views, opinions, and/or findings contained in this paper are those of the author and should not be interpreted as representing the official views or policies, either expressed or implied, of the Defense Advanced Research Projects Agency or the Department of Defense. This work was also supported in part by grants National Science Foundation (NSF) EEC-0310723 to University of Southern California (USC) (T. W. Berger), National Institutes of Health/National Institute of Biomedical Imaging and Bioengineering (NIH/NIBIB) under Grant P41-EB001978 to the Biomedical Simulations Resource at USC (V. Z. Marmarelis and T. W. Berger), and NIH R01DA07625 (S. A. Deadwyler).",

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Hampson, RE, Song, D, Chan, RHM, Sweatt, AJ, Riley, MR, Gerhardt, GA, Shin, DC, Marmarelis, VZ, Berger, TW & Deadwyler, SA 2012, 'A nonlinear model for hippocampal cognitive prosthesis: Memory facilitation by hippocampal ensemble stimulation', IEEE Transactions on Neural Systems and Rehabilitation Engineering, vol. 20, no. 2, 6171069, pp. 184-197. https://doi.org/10.1109/TNSRE.2012.2189163

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T1 - A nonlinear model for hippocampal cognitive prosthesis

T2 - Memory facilitation by hippocampal ensemble stimulation

AU - Hampson, Robert E.

AU - Song, Dong

AU - Chan, Rosa H.M.

AU - Sweatt, Andrew J.

AU - Riley, Mitchell R.

AU - Gerhardt, Gregory A.

AU - Shin, Dae C.

AU - Marmarelis, Vasilis Z.

AU - Berger, Theodore W.

AU - Deadwyler, Samuel A.

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A nonlinear model for hippocampal cognitive prosthesis: Memory facilitation by hippocampal ensemble stimulation

Abstract

Bibliographical note

Funding

Keywords

ASJC Scopus subject areas

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