Thalamic deep brain stimulation modulates cycles of seizure risk in epilepsy

Nicholas M. Gregg; Vladimir Sladky; Petr Nejedly; Filip Mivalt; Inyong Kim; Irena Balzekas; Beverly K. Sturges; Chelsea Crowe; Edward E. Patterson; Jamie J. Van Gompel; Brian N. Lundstrom; Kent Leyde; Timothy J. Denison; Benjamin H. Brinkmann; Vaclav Kremen; Gregory A. Worrell

doi:10.1038/s41598-021-03555-7

Thalamic deep brain stimulation modulates cycles of seizure risk in epilepsy

Nicholas M. Gregg, Vladimir Sladky, Petr Nejedly, Filip Mivalt, Inyong Kim, Irena Balzekas, Beverly K. Sturges, Chelsea Crowe, Edward E. Patterson, Jamie J. Van Gompel, Brian N. Lundstrom, Kent Leyde, Timothy J. Denison, Benjamin H. Brinkmann, Vaclav Kremen, Gregory A. Worrell

Veterinary Clinical Sciences

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

23 Scopus citations

Abstract

Chronic brain recordings suggest that seizure risk is not uniform, but rather varies systematically relative to daily (circadian) and multiday (multidien) cycles. Here, one human and seven dogs with naturally occurring epilepsy had continuous intracranial EEG (median 298 days) using novel implantable sensing and stimulation devices. Two pet dogs and the human subject received concurrent thalamic deep brain stimulation (DBS) over multiple months. All subjects had circadian and multiday cycles in the rate of interictal epileptiform spikes (IES). There was seizure phase locking to circadian and multiday IES cycles in five and seven out of eight subjects, respectively. Thalamic DBS modified circadian (all 3 subjects) and multiday (analysis limited to the human participant) IES cycles. DBS modified seizure clustering and circadian phase locking in the human subject. Multiscale cycles in brain excitability and seizure risk are features of human and canine epilepsy and are modifiable by thalamic DBS.

Original language	English (US)
Article number	24250
Journal	Scientific reports
Volume	11
Issue number	1
DOIs	https://doi.org/10.1038/s41598-021-03555-7
State	Published - Dec 2021

Bibliographical note

Funding Information:
This research was supported by the American Epilepsy Society Research & Training Fellowship for Clinicians (N.M.G.), National Institutes of Health (NIH; U01-NS073557, R01-NS92882, UH2&3-NS95495), and Epilepsy Foundation Epilepsy Innovation Institute My Seizure Gauge. V.K. was partially supported by institutional support from Czech Technical University in Prague. We thank CertiCon a.s. for the use of the Cyber PSG tool. This work benefited from the community expertise and resources made available by the NIH Open Mind Consortium (NIH U24-NS113637; https://openmindconsortium.github.io/).

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© 2021, The Author(s).

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Gregg, N. M., Sladky, V., Nejedly, P., Mivalt, F., Kim, I., Balzekas, I., Sturges, B. K., Crowe, C., Patterson, E. E., Van Gompel, J. J., Lundstrom, B. N., Leyde, K., Denison, T. J., Brinkmann, B. H., Kremen, V., & Worrell, G. A. (2021). Thalamic deep brain stimulation modulates cycles of seizure risk in epilepsy. Scientific reports, 11(1), Article 24250. https://doi.org/10.1038/s41598-021-03555-7

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abstract = "Chronic brain recordings suggest that seizure risk is not uniform, but rather varies systematically relative to daily (circadian) and multiday (multidien) cycles. Here, one human and seven dogs with naturally occurring epilepsy had continuous intracranial EEG (median 298 days) using novel implantable sensing and stimulation devices. Two pet dogs and the human subject received concurrent thalamic deep brain stimulation (DBS) over multiple months. All subjects had circadian and multiday cycles in the rate of interictal epileptiform spikes (IES). There was seizure phase locking to circadian and multiday IES cycles in five and seven out of eight subjects, respectively. Thalamic DBS modified circadian (all 3 subjects) and multiday (analysis limited to the human participant) IES cycles. DBS modified seizure clustering and circadian phase locking in the human subject. Multiscale cycles in brain excitability and seizure risk are features of human and canine epilepsy and are modifiable by thalamic DBS.",

author = "Gregg, {Nicholas M.} and Vladimir Sladky and Petr Nejedly and Filip Mivalt and Inyong Kim and Irena Balzekas and Sturges, {Beverly K.} and Chelsea Crowe and Patterson, {Edward E.} and {Van Gompel}, {Jamie J.} and Lundstrom, {Brian N.} and Kent Leyde and Denison, {Timothy J.} and Brinkmann, {Benjamin H.} and Vaclav Kremen and Worrell, {Gregory A.}",

note = "Funding Information: This research was supported by the American Epilepsy Society Research & Training Fellowship for Clinicians (N.M.G.), National Institutes of Health (NIH; U01-NS073557, R01-NS92882, UH2&3-NS95495), and Epilepsy Foundation Epilepsy Innovation Institute My Seizure Gauge. V.K. was partially supported by institutional support from Czech Technical University in Prague. We thank CertiCon a.s. for the use of the Cyber PSG tool. This work benefited from the community expertise and resources made available by the NIH Open Mind Consortium (NIH U24-NS113637; https://openmindconsortium.github.io/). Publisher Copyright: {\textcopyright} 2021, The Author(s).",

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AU - Balzekas, Irena

AU - Sturges, Beverly K.

AU - Crowe, Chelsea

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AU - Leyde, Kent

AU - Denison, Timothy J.

AU - Brinkmann, Benjamin H.

AU - Kremen, Vaclav

AU - Worrell, Gregory A.

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N2 - Chronic brain recordings suggest that seizure risk is not uniform, but rather varies systematically relative to daily (circadian) and multiday (multidien) cycles. Here, one human and seven dogs with naturally occurring epilepsy had continuous intracranial EEG (median 298 days) using novel implantable sensing and stimulation devices. Two pet dogs and the human subject received concurrent thalamic deep brain stimulation (DBS) over multiple months. All subjects had circadian and multiday cycles in the rate of interictal epileptiform spikes (IES). There was seizure phase locking to circadian and multiday IES cycles in five and seven out of eight subjects, respectively. Thalamic DBS modified circadian (all 3 subjects) and multiday (analysis limited to the human participant) IES cycles. DBS modified seizure clustering and circadian phase locking in the human subject. Multiscale cycles in brain excitability and seizure risk are features of human and canine epilepsy and are modifiable by thalamic DBS.

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Thalamic deep brain stimulation modulates cycles of seizure risk in epilepsy

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