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Structural controllability predicts functional patterns and brain stimulation benefits associated with working memory

View ORCID ProfileL. Beynel, View ORCID ProfileL. Deng, View ORCID ProfileC.A. Crowell, View ORCID ProfileM. Dannhauer, H. Palmer, S. Hilbig, View ORCID ProfileA.V. Peterchev, B. Luber, View ORCID ProfileS.H. Lisanby, View ORCID ProfileR. Cabeza, View ORCID ProfileL.G. Appelbaum, View ORCID ProfileS.W. Davis
doi: https://doi.org/10.1101/794388
L. Beynel
1Department of Psychiatry and Behavioral Science, Duke University School of Medicine, Durham, North Carolina, United States of America
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  • ORCID record for L. Beynel
L. Deng
3Center for Cognitive Neuroscience, Duke University, Durham, North Carolina, United States of America
8Department of Psychology & Neuroscience, Duke University, Durham, North Carolina, United States of America
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C.A. Crowell
1Department of Psychiatry and Behavioral Science, Duke University School of Medicine, Durham, North Carolina, United States of America
3Center for Cognitive Neuroscience, Duke University, Durham, North Carolina, United States of America
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M. Dannhauer
1Department of Psychiatry and Behavioral Science, Duke University School of Medicine, Durham, North Carolina, United States of America
4Department of Biomedical Engineering, Duke University, Durham, North Carolina, United States of America
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H. Palmer
1Department of Psychiatry and Behavioral Science, Duke University School of Medicine, Durham, North Carolina, United States of America
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S. Hilbig
1Department of Psychiatry and Behavioral Science, Duke University School of Medicine, Durham, North Carolina, United States of America
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A.V. Peterchev
1Department of Psychiatry and Behavioral Science, Duke University School of Medicine, Durham, North Carolina, United States of America
4Department of Biomedical Engineering, Duke University, Durham, North Carolina, United States of America
5Department of Electrical and Computer Engineering, Duke University, Durham, North Carolina, United States of America
6Department of Neurosurgery, Duke University School of Medicine, Durham, North Carolina, United States of America
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B. Luber
7National Institute of Mental Health, Bethesda, Maryland, United States of America
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S.H. Lisanby
1Department of Psychiatry and Behavioral Science, Duke University School of Medicine, Durham, North Carolina, United States of America
7National Institute of Mental Health, Bethesda, Maryland, United States of America
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R. Cabeza
3Center for Cognitive Neuroscience, Duke University, Durham, North Carolina, United States of America
8Department of Psychology & Neuroscience, Duke University, Durham, North Carolina, United States of America
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L.G. Appelbaum
1Department of Psychiatry and Behavioral Science, Duke University School of Medicine, Durham, North Carolina, United States of America
3Center for Cognitive Neuroscience, Duke University, Durham, North Carolina, United States of America
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S.W. Davis
2Department of Neurology, Duke University School of Medicine, Durham, North Carolina, United States of America
3Center for Cognitive Neuroscience, Duke University, Durham, North Carolina, United States of America
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  • For correspondence: simon.davis@duke.edu
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Summary

The brain is an inherently dynamic system, and much work has focused on the ability to modify neural activity through both local perturbations and changes in the function of global network ensembles. Network controllability is a recent concept in network science that purports to predict the influence of individual cortical sites on global network states and state changes, thereby creating a unifying account of local influences on global brain dynamics. Here, we present an integrated set of multimodal brain–behavior relationships, acquired from functional magnetic resonance imaging during a transcranial magnetic stimulation intervention, that demonstrate how network controllability influences network function, as well as behavior. This work helps to outline a clear technique for integrating structural network topology and functional activity to predict the influence of a potential stimulation target on subsequent behaviors and prescribes next steps towards predicting neuromodulatory and behavioral responses after brain stimulation.

Highlights

  • - This study tested the strength of network controllability using fMRI and rTMS

  • - Controllability correlates with functional modulation of working memory demand load

  • - Controllability is also correlated with the memory improvement from applied rTMS

  • - These findings link network control theory with physiology and behavior.

In brief Beynel et al. show that the benefits of functionally targeted brain stimulation on working memory performance can be predicted by network control properties at the stimulated site. Structural controllability and functional activity independently predict this cognitive benefit.

Author Contributions Conceptualization & Methodology: L.B, S.W.D., B.L., R.C., L.G.A.; Investigation: L.B., L.D., S.W.D., C.A.C., M.D., H.P., S.H.; Writing—Original Draft: L.B., L.D., S.W.D.; Writing—Review & Editing: L.B., L.D., S.W.D., L.G.A., A.V.P.; Funding Acquisition: S.W.D., R.C., B.L., S.H.L., A.V.P.; Resources: L.G.A., B.L., R.C.; Supervision: L.G.A., S.W.D.

Footnotes

  • Funding: This research was funded by grant support from the National Institute of Aging grant # U01 AG050618 and was supported in part by the Intramural Research Program of the NIMH. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted October 18, 2019.
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Structural controllability predicts functional patterns and brain stimulation benefits associated with working memory
L. Beynel, L. Deng, C.A. Crowell, M. Dannhauer, H. Palmer, S. Hilbig, A.V. Peterchev, B. Luber, S.H. Lisanby, R. Cabeza, L.G. Appelbaum, S.W. Davis
bioRxiv 794388; doi: https://doi.org/10.1101/794388
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Structural controllability predicts functional patterns and brain stimulation benefits associated with working memory
L. Beynel, L. Deng, C.A. Crowell, M. Dannhauer, H. Palmer, S. Hilbig, A.V. Peterchev, B. Luber, S.H. Lisanby, R. Cabeza, L.G. Appelbaum, S.W. Davis
bioRxiv 794388; doi: https://doi.org/10.1101/794388

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