Uncovering spatiotemporal dynamics of the corticothalamic network at ictal onset

Author:

Panchavati Saarang12,Daida Atsuro3ORCID,Edmonds Benjamin3ORCID,Miyakoshi Makoto45,Oana Shingo3,Ahn Samuel S.3ORCID,Arnold Corey12,Salamon Noriko6,Sankar Raman37,Fallah Aria8ORCID,Speier William12,Nariai Hiroki36ORCID

Affiliation:

1. Department of Bioengineering University of California, Los Angeles Los Angeles California USA

2. Department of Radiological Sciences University of California, Los Angeles Los Angeles California USA

3. Division of Pediatric Neurology, Department of Pediatrics UCLA Mattel Children's Hospital, David Geffen School of Medicine Los Angeles California USA

4. Department of Psychiatry and Behavioral Neuroscience Cincinnati Children's Hospital Medical Center Cincinnati Ohio USA

5. Department of Psychiatry University of Cincinnati College of Medicine Cincinnati Ohio USA

6. Department of Radiology, UCLA Medical Center David Geffen School of Medicine Los Angeles California USA

7. UCLA Children's Discovery and Innovation Institute Los Angeles California USA

8. Department of Neurosurgery, UCLA Medical Center David Geffen School of Medicine Los Angeles California USA

Abstract

AbstractObjectiveAlthough the clinical efficacy of deep brain stimulation targeting the anterior nucleus (AN) and centromedian nucleus (CM) of the thalamus has been actively investigated for the treatment of medication‐resistant epilepsy, few studies have investigated dynamic ictal changes in corticothalamic connectivity in human electroencephalographic (EEG) recording. This study aims to establish the complex spatiotemporal dynamics of the ictal corticothalamic network associated with various seizure foci.MethodsWe analyzed 10 patients (aged 2.7–28.1 years) with medication‐resistant focal epilepsy who underwent stereotactic EEG evaluation with thalamic sampling. We examined both undirected and directed connectivity, incorporating coherence and spectral Granger causality analysis (GCA) between the diverse seizure foci and thalamic nuclei (AN and CM) at ictal onset.ResultsIn our analysis of 36 seizures, coherence between seizure onset and thalamic nuclei increased across all frequencies, especially in slower bands (delta, theta, alpha). GCA showed increased information flow from seizure onset to the thalamus across all frequency bands, but outflows from the thalamus were mainly in slower frequencies, particularly delta. In the subgroup analysis based on various seizure foci, the delta coherence showed a more pronounced increase at CM than at AN during frontal lobe seizures. Conversely, in limbic seizures, the delta coherence increase was greater at AN compared to CM.SignificanceIt appears that the delta frequency plays a pivotal role in modulating the corticothalamic network during seizures. Our results underscore the significance of comprehending the spatiotemporal dynamics of the corticothalamic network at ictal onset, and this knowledge could guide personalized responsive neuromodulation treatment strategies.

Funder

National Institute of Neurological Disorders and Stroke

Uehara Memorial Foundation

SENSHIN Medical Research Foundation

Publisher

Wiley

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