Subject-based assessment of large-scale integration dynamics in epileptic brain networks: insights from the intrinsic ignition framework

Antonio Donaire; Nelly Padilla; Anira Escrichs; Mariam Khawja; Xavier Setoain; Jordi Rumia; Pedro Roldan; Nuria Bargallo; Teresa Boget; Luis Pintor; María Centeno; Estefanía Conde; Oriol Vernet; Javier Buendía; Isabel Manzanares; Ulrika Ådén; Mar Carreño; Morten Kringelbach; Gustavo Deco

doi:10.1093/cercor/bhae419

Subject-based assessment of large-scale integration dynamics in epileptic brain networks: insights from the intrinsic ignition framework

Antonio Donaire, Nelly Padilla, Anira Escrichs, Mariam Khawja, Xavier Setoain, Jordi Rumia, Pedro Roldan, Nuria Bargallo, Teresa Boget, Luis Pintor, María Centeno, Estefanía Conde, Oriol Vernet, Javier Buendía, Isabel Manzanares, Ulrika Ådén, Mar Carreño, Morten Kringelbach, Gustavo Deco

Department of Clinical Medicine - Center for Music In the Brain

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

Abstract

This study examined the dynamic properties of brain regions involved in the genesis and spread of seizures in 10 individuals diagnosed with pharmacoresistant focal epilepsy. The patients and 30 healthy controls underwent resting-state functional magnetic resonance imaging scans and the brain's functional network dynamics were analyzed using the intrinsic ignition framework. Comparative statistical analyses examined the differences in the integration and metastability measures in both groups in the whole brain and specific local brain regions. Invasive electroencephalography evaluations validated the findings of significant global and regional changes in the patient's brain network dynamics. There was a marked increase in global integration and metastability across the brain, reflecting substantial alterations in the overall connectivity and flexibility of the functional networks. Specific brain regions exhibited paradoxical dynamics within the seizure onset zone, with decreased intrinsic ignition and increased metastability. Increased intrinsic ignition was observed in remote brain regions, suggesting a reorganization of the brain network hubs and potential pathways for seizure propagation. Using the intrinsic ignition framework provided insights into dynamic alterations in the brain networks of patients with epilepsy. These have increased our understanding of the mechanisms underlying epileptic seizures and may guide the development of diagnostic biomarkers and targeted therapeutic interventions.

Original language	English
Article number	bhae419
Journal	Cerebral cortex (New York, N.Y. : 1991)
Volume	34
Issue	10
ISSN	1047-3211
DOIs	https://doi.org/10.1093/cercor/bhae419
Publication status	Published - 1 Oct 2024

Keywords

epilepsy
functional connectivity
functional magnetic resonance imaging
integration dynamics
intrinsic ignition framework

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10.1093/cercor/bhae419

Cite this

Donaire, A., Padilla, N., Escrichs, A., Khawja, M., Setoain, X., Rumia, J., Roldan, P., Bargallo, N., Boget, T., Pintor, L., Centeno, M., Conde, E., Vernet, O., Buendía, J., Manzanares, I., Ådén, U., Carreño, M., Kringelbach, M., & Deco, G. (2024). Subject-based assessment of large-scale integration dynamics in epileptic brain networks: insights from the intrinsic ignition framework. Cerebral cortex (New York, N.Y. : 1991), 34(10), Article bhae419. https://doi.org/10.1093/cercor/bhae419

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abstract = "This study examined the dynamic properties of brain regions involved in the genesis and spread of seizures in 10 individuals diagnosed with pharmacoresistant focal epilepsy. The patients and 30 healthy controls underwent resting-state functional magnetic resonance imaging scans and the brain's functional network dynamics were analyzed using the intrinsic ignition framework. Comparative statistical analyses examined the differences in the integration and metastability measures in both groups in the whole brain and specific local brain regions. Invasive electroencephalography evaluations validated the findings of significant global and regional changes in the patient's brain network dynamics. There was a marked increase in global integration and metastability across the brain, reflecting substantial alterations in the overall connectivity and flexibility of the functional networks. Specific brain regions exhibited paradoxical dynamics within the seizure onset zone, with decreased intrinsic ignition and increased metastability. Increased intrinsic ignition was observed in remote brain regions, suggesting a reorganization of the brain network hubs and potential pathways for seizure propagation. Using the intrinsic ignition framework provided insights into dynamic alterations in the brain networks of patients with epilepsy. These have increased our understanding of the mechanisms underlying epileptic seizures and may guide the development of diagnostic biomarkers and targeted therapeutic interventions.",

keywords = "epilepsy, functional connectivity, functional magnetic resonance imaging, integration dynamics, intrinsic ignition framework",

author = "Antonio Donaire and Nelly Padilla and Anira Escrichs and Mariam Khawja and Xavier Setoain and Jordi Rumia and Pedro Roldan and Nuria Bargallo and Teresa Boget and Luis Pintor and Mar{\'i}a Centeno and Estefan{\'i}a Conde and Oriol Vernet and Javier Buend{\'i}a and Isabel Manzanares and Ulrika {\AA}d{\'e}n and Mar Carre{\~n}o and Morten Kringelbach and Gustavo Deco",

year = "2024",

month = oct,

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doi = "10.1093/cercor/bhae419",

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Donaire, A, Padilla, N, Escrichs, A, Khawja, M, Setoain, X, Rumia, J, Roldan, P, Bargallo, N, Boget, T, Pintor, L, Centeno, M, Conde, E, Vernet, O, Buendía, J, Manzanares, I, Ådén, U, Carreño, M, Kringelbach, M & Deco, G 2024, 'Subject-based assessment of large-scale integration dynamics in epileptic brain networks: insights from the intrinsic ignition framework', Cerebral cortex (New York, N.Y. : 1991), vol. 34, no. 10, bhae419. https://doi.org/10.1093/cercor/bhae419

Subject-based assessment of large-scale integration dynamics in epileptic brain networks: insights from the intrinsic ignition framework. / Donaire, Antonio; Padilla, Nelly; Escrichs, Anira et al.
In: Cerebral cortex (New York, N.Y. : 1991), Vol. 34, No. 10, bhae419, 01.10.2024.

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

TY - JOUR

T1 - Subject-based assessment of large-scale integration dynamics in epileptic brain networks

T2 - insights from the intrinsic ignition framework

AU - Donaire, Antonio

AU - Padilla, Nelly

AU - Escrichs, Anira

AU - Khawja, Mariam

AU - Setoain, Xavier

AU - Rumia, Jordi

AU - Roldan, Pedro

AU - Bargallo, Nuria

AU - Boget, Teresa

AU - Pintor, Luis

AU - Centeno, María

AU - Conde, Estefanía

AU - Vernet, Oriol

AU - Buendía, Javier

AU - Manzanares, Isabel

AU - Ådén, Ulrika

AU - Carreño, Mar

AU - Kringelbach, Morten

AU - Deco, Gustavo

PY - 2024/10/1

Y1 - 2024/10/1

N2 - This study examined the dynamic properties of brain regions involved in the genesis and spread of seizures in 10 individuals diagnosed with pharmacoresistant focal epilepsy. The patients and 30 healthy controls underwent resting-state functional magnetic resonance imaging scans and the brain's functional network dynamics were analyzed using the intrinsic ignition framework. Comparative statistical analyses examined the differences in the integration and metastability measures in both groups in the whole brain and specific local brain regions. Invasive electroencephalography evaluations validated the findings of significant global and regional changes in the patient's brain network dynamics. There was a marked increase in global integration and metastability across the brain, reflecting substantial alterations in the overall connectivity and flexibility of the functional networks. Specific brain regions exhibited paradoxical dynamics within the seizure onset zone, with decreased intrinsic ignition and increased metastability. Increased intrinsic ignition was observed in remote brain regions, suggesting a reorganization of the brain network hubs and potential pathways for seizure propagation. Using the intrinsic ignition framework provided insights into dynamic alterations in the brain networks of patients with epilepsy. These have increased our understanding of the mechanisms underlying epileptic seizures and may guide the development of diagnostic biomarkers and targeted therapeutic interventions.

AB - This study examined the dynamic properties of brain regions involved in the genesis and spread of seizures in 10 individuals diagnosed with pharmacoresistant focal epilepsy. The patients and 30 healthy controls underwent resting-state functional magnetic resonance imaging scans and the brain's functional network dynamics were analyzed using the intrinsic ignition framework. Comparative statistical analyses examined the differences in the integration and metastability measures in both groups in the whole brain and specific local brain regions. Invasive electroencephalography evaluations validated the findings of significant global and regional changes in the patient's brain network dynamics. There was a marked increase in global integration and metastability across the brain, reflecting substantial alterations in the overall connectivity and flexibility of the functional networks. Specific brain regions exhibited paradoxical dynamics within the seizure onset zone, with decreased intrinsic ignition and increased metastability. Increased intrinsic ignition was observed in remote brain regions, suggesting a reorganization of the brain network hubs and potential pathways for seizure propagation. Using the intrinsic ignition framework provided insights into dynamic alterations in the brain networks of patients with epilepsy. These have increased our understanding of the mechanisms underlying epileptic seizures and may guide the development of diagnostic biomarkers and targeted therapeutic interventions.

KW - epilepsy

KW - functional connectivity

KW - functional magnetic resonance imaging

KW - integration dynamics

KW - intrinsic ignition framework

UR - http://www.scopus.com/inward/record.url?scp=85207179719&partnerID=8YFLogxK

U2 - 10.1093/cercor/bhae419

DO - 10.1093/cercor/bhae419

M3 - Journal article

C2 - 39441026

AN - SCOPUS:85207179719

SN - 1047-3211

VL - 34

JO - Cerebral cortex (New York, N.Y. : 1991)

JF - Cerebral cortex (New York, N.Y. : 1991)

IS - 10

M1 - bhae419

ER -

Subject-based assessment of large-scale integration dynamics in epileptic brain networks: insights from the intrinsic ignition framework

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