Developmental atlas of phase-amplitude coupling between physiologic high-frequency oscillations and slow waves

Kazuki Sakakura; Naoto Kuroda; Masaki Sonoda; Takumi Mitsuhashi; Ethan Firestone; Aimee F Luat; Neena I Marupudi; Sandeep Sood; Eishi Asano

doi:10.1038/s41467-023-42091-y

Developmental atlas of phase-amplitude coupling between physiologic high-frequency oscillations and slow waves

Nat Commun. 2023 Oct 13;14(1):6435. doi: 10.1038/s41467-023-42091-y.

Authors

Kazuki Sakakura^{1

2

3}, Naoto Kuroda^{1

4}, Masaki Sonoda^{1

5}, Takumi Mitsuhashi^{1

6}, Ethan Firestone^{1

7}, Aimee F Luat^{1

8

9}, Neena I Marupudi¹⁰, Sandeep Sood¹⁰, Eishi Asano^{11

12}

Affiliations

¹ Department of Pediatrics, Children's Hospital of Michigan, Detroit Medical Center, Wayne State University, Detroit, MI, 48201, USA.
² Department of Neurosurgery, Rush University Medical Center, Chicago, IL, 60612, USA.
³ Department of Neurosurgery, University of Tsukuba, Tsukuba, 3058575, Japan.
⁴ Department of Epileptology, Tohoku University Graduate School of Medicine, Sendai, 9808575, Japan.
⁵ Department of Neurosurgery, Yokohama City University, Yokohama-shi, 2360004, Japan.
⁶ Department of Neurosurgery, Juntendo University, Tokyo, 1138421, Japan.
⁷ Department of Physiology, Wayne State University, Detroit, MI, 48201, USA.
⁸ Department of Neurology, Children's Hospital of Michigan, Detroit Medical Center, Wayne State University, Detroit, MI, 48201, USA.
⁹ Department of Pediatrics, Central Michigan University, Mount Pleasant, MI, 48858, USA.
¹⁰ Department of Neurosurgery, Children's Hospital of Michigan, Detroit Medical Center, Wayne State University, Detroit, MI, 48201, USA.
¹¹ Department of Pediatrics, Children's Hospital of Michigan, Detroit Medical Center, Wayne State University, Detroit, MI, 48201, USA. easano@med.wayne.edu.
¹² Department of Neurology, Children's Hospital of Michigan, Detroit Medical Center, Wayne State University, Detroit, MI, 48201, USA. easano@med.wayne.edu.

Abstract

We investigated the developmental changes in high-frequency oscillation (HFO) and Modulation Index (MI) - the coupling measure between HFO and slow-wave phase. We generated normative brain atlases, using subdural EEG signals from 8251 nonepileptic electrode sites in 114 patients (ages 1.0-41.5 years) who achieved seizure control following resective epilepsy surgery. We observed a higher MI in the occipital lobe across all ages, and occipital MI increased notably during early childhood. The cortical areas exhibiting MI co-growth were connected via the vertical occipital fasciculi and posterior callosal fibers. While occipital HFO rate showed no significant age-association, the temporal, frontal, and parietal lobes exhibited an age-inversed HFO rate. Assessment of 1006 seizure onset sites revealed that z-score normalized MI and HFO rate were higher at seizure onset versus nonepileptic electrode sites. We have publicly shared our intracranial EEG data to enable investigators to validate MI and HFO-centric presurgical evaluations to identify the epileptogenic zone.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Ascomycota*
Brain Mapping
Brain Waves* / physiology
Child, Preschool
Electroencephalography
Epilepsy* / surgery
Humans
Seizures

Grants and funding

R01 NS064033/NS/NINDS NIH HHS/United States