TY - JOUR
T1 - Time-evolving controllability of effective connectivity networks during seizure progression
AU - Scheid, Brittany H.
AU - Ashourvan, Arian
AU - Stiso, Jennifer
AU - Davis, Kathryn A.
AU - Mikhail, Fadi
AU - Pasqualetti, Fabio
AU - Litt, Brian
AU - Bassett, Danielle S.
N1 - Funding Information:
We thank both Jason Z. Kim for helpful discussions regarding control theory and Dr. Xiaosong He for helpful discussions regarding structural and EC model comparison. This work was primarily funded by NSF award BCS-1631550 (to D.S.B.) and National Institute of Neurological Disorders and Stroke award R01 NS099348 (to B.L. and D.S.B.). D.S.B. acknowledges additional support from the John D. and Catherine T. MacArthur Foundation, the Alfred P. Sloan Foundation, the Institute for Scientific Interchange Foundation, the Paul Allen Foundation, the Army Research Laboratory (W911NF-10-2-0022), and the Army Research Office (Bassett-W911NF-14-1-0679 and Grafton-W911NF-16-1-0474). B.L. acknowledges additional support from the Mirowski Family Foundation, the Pennsylvania Health Research Formula Fund, Johnathan and Bonnie Rothberg, and Neil and Barbara Smit. The content is solely the responsibility of the authors and does not necessarily represent the official views of any of the funding agencies.
Funding Information:
ACKNOWLEDGMENTS. We thank both Jason Z. Kim for helpful discussions regarding control theory and Dr. Xiaosong He for helpful discussions regarding structural and EC model comparison. This work was primarily funded by NSF award BCS-1631550 (to D.S.B.) and National Institute of Neurological Disorders and Stroke award R01 NS099348 (to B.L. and D.S.B.). D.S.B. acknowledges additional support from the John D. and Catherine T. MacArthur Foundation, the Alfred P. Sloan Foundation, the Institute for Scientific Interchange Foundation, the Paul Allen Foundation, the Army Research Laboratory (W911NF-10-2-0022), and the Army Research Office (Bassett-W911NF-14-1-0679 and Grafton-W911NF-16-1-0474). B.L. acknowledges additional support from the Mirowski Family Foundation, the Pennsylvania Health Research Formula Fund, Johnathan and Bonnie Rothberg, and Neil and Barbara Smit. The content is solely the responsibility of the authors and does not necessarily represent the official views of any of the funding agencies.
Publisher Copyright:
© 2021 National Academy of Sciences. All rights reserved.
PY - 2021/2/2
Y1 - 2021/2/2
N2 - Over one third of the estimated 3 million people with epilepsy in the United States are medication resistant. Responsive neurostimulation from chronically implanted electrodes provides a promising treatment alternative to resective surgery. However, determining optimal personalized stimulation parameters, including when and where to intervene to guarantee a positive patient outcome, is a major open challenge. Network neuroscience and control theory offer useful tools that may guide improvements in parameter selection for control of anomalous neural activity. Here we use a method to characterize dynamic controllability across consecutive effective connectivity (EC) networks based on regularized partial correlations between implanted electrodes during the onset, propagation, and termination regimes of 34 seizures. We estimate regularized partial correlation adjacency matrices from 1-s time windows of intracranial electrocorticography recordings using the Graphical Least Absolute Shrinkage and Selection Operator (GLASSO). Average and modal controllability metrics calculated from each resulting EC network track the time-varying controllability of the brain on an evolving landscape of conditionally dependent network interactions. We show that average controllability increases throughout a seizure and is negatively correlated with modal controllability throughout. Our results support the hypothesis that the energy required to drive the brain to a seizure-free state from an ictal state is smallest during seizure onset, yet we find that applying control energy at electrodes in the seizure onset zone may not always be energetically favorable. Our work suggests that a low-complexity model of time-evolving controllability may offer insights for developing and improving control strategies targeting seizure suppression.
AB - Over one third of the estimated 3 million people with epilepsy in the United States are medication resistant. Responsive neurostimulation from chronically implanted electrodes provides a promising treatment alternative to resective surgery. However, determining optimal personalized stimulation parameters, including when and where to intervene to guarantee a positive patient outcome, is a major open challenge. Network neuroscience and control theory offer useful tools that may guide improvements in parameter selection for control of anomalous neural activity. Here we use a method to characterize dynamic controllability across consecutive effective connectivity (EC) networks based on regularized partial correlations between implanted electrodes during the onset, propagation, and termination regimes of 34 seizures. We estimate regularized partial correlation adjacency matrices from 1-s time windows of intracranial electrocorticography recordings using the Graphical Least Absolute Shrinkage and Selection Operator (GLASSO). Average and modal controllability metrics calculated from each resulting EC network track the time-varying controllability of the brain on an evolving landscape of conditionally dependent network interactions. We show that average controllability increases throughout a seizure and is negatively correlated with modal controllability throughout. Our results support the hypothesis that the energy required to drive the brain to a seizure-free state from an ictal state is smallest during seizure onset, yet we find that applying control energy at electrodes in the seizure onset zone may not always be energetically favorable. Our work suggests that a low-complexity model of time-evolving controllability may offer insights for developing and improving control strategies targeting seizure suppression.
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U2 - 10.1073/pnas.2006436118
DO - 10.1073/pnas.2006436118
M3 - Article
C2 - 33495341
AN - SCOPUS:85100049487
SN - 0027-8424
VL - 118
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 5
M1 - e2006436118
ER -