Intra– and inter–hemispheric network dynamics supporting object recognition and speech production

Kitazawa, Yu; Sonoda, Masaki; Sakakura, Kazuki; Mitsuhashi, Takumi; Firestone, Ethan; Ueda, Riyo; Kambara, Tomihito; Iwaki, Hirotaka; Luat, Aimee F.; Marupudi, Neena I.; Sood, Sandeep; Asano, Eishi

doi:10.1016/j.neuroimage.2023.119954

Cited by 9 publications

(11 citation statements)

References 139 publications

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“…Visualization of the direct white matter streamlines connecting cortical regions with a developmental enhancement of MI is an application of dynamic tractography technology 33 , 48 . We interpret the visualized streamlines, including vertical occipital fasciculi and posterior callosal fibers, to reflect the ongoing development of large-scale neural communications based on slow wave-nested HFO before reaching the adult level.…”

Section: Discussionmentioning

confidence: 99%

“…To this end, we used the regression slope of MI ≥80 Hz & 0.5-1 Hz as a function of √age at each cortical mesh point, as computed in a regression analysis mentioned above. We declared that the developmental enhancement (or reduction) of nested HFO-based neural communications took place between two cortical mesh points if [1] two distinct mesh points showed significantly positive (or negative) regression slopes, and [2] these mesh points were accompanied by direct tractography streamlines on diffusion-weighted imaging (DWI) analysis 48 .…”

Section: Methodsmentioning

confidence: 99%

“…We delineated white matter DWI streamlines using open-source data from 1065 healthy participants ( http://brain.labsolver.org/diffusion-mri-templates/hcp-842-hcp-1021 ) 69 , as previously reported 33 , 48 . Our group validated the use of open-source DWI data by demonstrating that the inferred velocity of neural propagations induced by single-pulse electrical stimulation was similar whether using open-source or individual patient DWI data 33 .…”

Section: Methodsmentioning

confidence: 99%

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

Sakakura,

Kuroda,

Sonoda

et al. 2023

Nat Commun

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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.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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

Sakakura,

Kuroda,

Sonoda

et al. 2023

Nat Commun

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“…In addition to modeling cortical ontogenic changes, the present study also visualized white matter pathways supporting the development of neural communications via delta-nested HFO (as rated by MI ≥ 80 Hz & 0.5−1 Hz ), during slow-wave sleep. To accomplish this, we utilized our novel imaging technique, dynamic tractography, which combines iEEG signals with MRI tractography (Sonoda et al, 2021;Kitazawa et al, 2023;Ono et al, 2023). Previous studies in animal models and patients with focal epilepsy have demonstrated that neural circuits engaging in high-frequency communication are susceptible to use-dependent modi cations of synaptic transmission that enhance effective connectivity via monosynaptic white matter tracts in the developing brain (Buonomano and Merzenich, 1998;Singer, 2018;Sonoda et al, 2021).…”

Section: White Matter Pathways Supporting Network Communications By S...mentioning

confidence: 99%

“…Visualization of the direct white matter streamlines connecting cortical regions with a developmental enhancement of MI is an innovative application of dynamic tractography technology (Sonoda et al, 2021;Kitazawa et al, 2023;Ono et al, 2023). We interpret the visualized streamlines, including vertical occipital fasciculi and posterior callosal bers, to re ect the ongoing development of large-scale neural communications based on slow wave-nested HFO before reaching the adult level.…”

Section: Innovationmentioning

confidence: 99%

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

Asano

Sakakura

Sonoda

et al. 2023

Preprint

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The cortex generates high-frequency oscillations (HFO) nested in slow waves during sleep, and these signals are especially elevated in the seizure onset zone. Thus, HFO occurrence rate and Modulation Index (MI), which quantifies the strength of coupling between HFO amplitude and slow-wave phase, represent promising epilepsy biomarkers. However, their diagnostic utility may be suboptimal because the endogenous developmental distributions are unknown. To improve age-appropriate localization of the epileptogenic zone, we hence constructed normative brain atlases demonstrating the developmental changes in MI and HFO rate. Our study investigated extraoperative, intracranial EEG data from 114 patients with focal epilepsy (ages 1.0 to 41.5 years) who achieved International League Against Epilepsy class I outcomes following resective surgery. We analyzed 20-minute slow-wave sleep epochs at 8,251 nonepileptic electrode sites (those outside the seizure onset zone, interictal spike zone, or MRI-visible lesions). Each electrode was transposed onto a standard brain template, and we then calculated its MI and HFO occurrence rate using four different detector toolboxes. Linear and nonlinear regression models determined the developmental slope of MI and HFO rate at each cortical mesh point. Mixed model analysis established the significance of MI and HFO rate developmental changes in each region of interest, while accounting for the independent effects of patient and epilepsy profiles. Finally, we created a dynamic tractography movie visualizing white matter pathways connecting cortical regions showing developmental co-growth in MI. We found that the occipital lobe exhibited enhanced MI compared to other lobes in both children and adults. Increased age, square root of age, and log base 10 of age were independently associated with elevated MI exclusively in the occipital lobe. The cortical regions showing developmental co-growth in MI were connected via the vertical occipital fasciculi and posterior callosal fibers. In contrast, we did not observe any significant association between age measures and HFO rate in the occipital lobe, but rather noted an inverse relationship between age and HFO rate in the temporal, frontal, and parietal lobes. Our study suggests that phase-amplitude coupling between physiologic HFO and delta waves, as rated by MI, is strengthened during development, in the occipital lobe particularly during toddlerhood and preschool. Given that occipital delta-nested HFO are believed to support visual memory consolidation, our observations imply that process may be significantly strengthened during early childhood. The data is publicly available to provide investigators with a crucial reference for MI and HFO-based presurgical evaluation of the epileptogenic zone.

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Remission of startle epilepsy provoked by acoustic stimuli following complete callosotomy: A case study

Ukishiro,

Osawa,

Kakisaka

et al. 2024

Epileptic Disorders

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Herein, we present the case of a 21‐year‐old man with a history of generalized tonic seizures since the age of 4 years. These seizures occurred either spontaneously or could be provoked by auditory stimuli such as the sounds of a vacuum cleaner or an electric shaver. Despite trials with 10 different anti‐seizure medications, his seizures remained refractory. Interictal electroencephalography (EEG) revealed generalized epileptiform activity, whereas ictal EEG showed a generalized attenuation pattern. Magnetic resonance imaging revealed extensive chronic infarctions, predominantly in the bilateral cerebral watershed areas. At the age of 17, the patient underwent a one‐stage complete callosotomy, which only achieved remission of auditory‐provoked seizures. Based on this experience and published reports, we propose that the posterior corpus callosum, particularly the isthmus and anterior splenium, may be involved in seizures caused by unexpected sound stimuli.

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Intra– and inter–hemispheric network dynamics supporting object recognition and speech production

Cited by 9 publications

References 139 publications

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

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

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

Remission of startle epilepsy provoked by acoustic stimuli following complete callosotomy: A case study

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