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Networks of cortical activity in infants with epilepsy

Epilepsy in infancy links to a significant risk of neurodevelopmental delay, calling for a better understanding of its underlying mechanisms. Here, we studied cortical activity networks in infants with early-onset epilepsy to identify network properties that could pre-empt infants’ neurodevelopmenta...

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Autores principales: Auno, Sami, Jonsson, Henna, Linnankivi, Tarja, Tokariev, Anton, Vanhatalo, Sampsa
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9692198/
https://www.ncbi.nlm.nih.gov/pubmed/36447560
http://dx.doi.org/10.1093/braincomms/fcac295
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author Auno, Sami
Jonsson, Henna
Linnankivi, Tarja
Tokariev, Anton
Vanhatalo, Sampsa
author_facet Auno, Sami
Jonsson, Henna
Linnankivi, Tarja
Tokariev, Anton
Vanhatalo, Sampsa
author_sort Auno, Sami
collection PubMed
description Epilepsy in infancy links to a significant risk of neurodevelopmental delay, calling for a better understanding of its underlying mechanisms. Here, we studied cortical activity networks in infants with early-onset epilepsy to identify network properties that could pre-empt infants’ neurodevelopmental course. We studied high-density (64 channel) electroencephalogram during non-rapid eye movement (N2) sleep in n = 49 infants at 1 year of age after being diagnosed with epilepsy during their first year of life. We computed frequency-specific networks in the cortical source space for two intrinsic brain modes: amplitude–amplitude and phase–phase correlations. Cortical activity networks of all frequency bands and connectivity modes were compared between the syndrome groups as well as between the three categories of neurocognitive development. The group differences were studied at three spatial levels: global, regional, and individual connections. Cortical mechanisms related to infant epilepsy were further compared with physiological networks using an automatic spindle detection algorithm. Our results show that global connectivity does not significantly differ between epilepsy syndromes; however, it co-varies with neurocognitive development. The largest network differences were observed at the lowest (<1 Hz) and mid-range (10–15 Hz) frequency bands. An algorithmic removal of sleep spindles from the data partially reduced the mid-range frequency network’s strength. The centrocentral and frontocentral networks at the spindle frequencies were found to be strongest in infants with a persistent age-typical neurocognitive performance, while their low-frequency (< 1 Hz) networks were weaker for both amplitude-amplitude [P = 0.008, effect size = 0.61] and phase–phase correlations (P = 0.02, effect size = 0.54) at low (< 1 Hz). However, subjects with persistent mild neurocognitive delay from 1 to 2 years of age had higher amplitude–amplitude (P = 0.02, effect size = 0.73) and phase–phase (P = 0.06, effect size = 0.59) at low frequencies than those that deteriorated from mild to severely delayed from 1 to 2 years of age. Our findings suggest that cortical activity networks reflect the underlying clinical course of infants’ epilepsy, and measures of spectrally and spatially resolved networks might become useful in better understanding infantile epilepsy as a network disease.
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spelling pubmed-96921982022-11-28 Networks of cortical activity in infants with epilepsy Auno, Sami Jonsson, Henna Linnankivi, Tarja Tokariev, Anton Vanhatalo, Sampsa Brain Commun Original Article Epilepsy in infancy links to a significant risk of neurodevelopmental delay, calling for a better understanding of its underlying mechanisms. Here, we studied cortical activity networks in infants with early-onset epilepsy to identify network properties that could pre-empt infants’ neurodevelopmental course. We studied high-density (64 channel) electroencephalogram during non-rapid eye movement (N2) sleep in n = 49 infants at 1 year of age after being diagnosed with epilepsy during their first year of life. We computed frequency-specific networks in the cortical source space for two intrinsic brain modes: amplitude–amplitude and phase–phase correlations. Cortical activity networks of all frequency bands and connectivity modes were compared between the syndrome groups as well as between the three categories of neurocognitive development. The group differences were studied at three spatial levels: global, regional, and individual connections. Cortical mechanisms related to infant epilepsy were further compared with physiological networks using an automatic spindle detection algorithm. Our results show that global connectivity does not significantly differ between epilepsy syndromes; however, it co-varies with neurocognitive development. The largest network differences were observed at the lowest (<1 Hz) and mid-range (10–15 Hz) frequency bands. An algorithmic removal of sleep spindles from the data partially reduced the mid-range frequency network’s strength. The centrocentral and frontocentral networks at the spindle frequencies were found to be strongest in infants with a persistent age-typical neurocognitive performance, while their low-frequency (< 1 Hz) networks were weaker for both amplitude-amplitude [P = 0.008, effect size = 0.61] and phase–phase correlations (P = 0.02, effect size = 0.54) at low (< 1 Hz). However, subjects with persistent mild neurocognitive delay from 1 to 2 years of age had higher amplitude–amplitude (P = 0.02, effect size = 0.73) and phase–phase (P = 0.06, effect size = 0.59) at low frequencies than those that deteriorated from mild to severely delayed from 1 to 2 years of age. Our findings suggest that cortical activity networks reflect the underlying clinical course of infants’ epilepsy, and measures of spectrally and spatially resolved networks might become useful in better understanding infantile epilepsy as a network disease. Oxford University Press 2022-11-05 /pmc/articles/PMC9692198/ /pubmed/36447560 http://dx.doi.org/10.1093/braincomms/fcac295 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of the Guarantors of Brain. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Article
Auno, Sami
Jonsson, Henna
Linnankivi, Tarja
Tokariev, Anton
Vanhatalo, Sampsa
Networks of cortical activity in infants with epilepsy
title Networks of cortical activity in infants with epilepsy
title_full Networks of cortical activity in infants with epilepsy
title_fullStr Networks of cortical activity in infants with epilepsy
title_full_unstemmed Networks of cortical activity in infants with epilepsy
title_short Networks of cortical activity in infants with epilepsy
title_sort networks of cortical activity in infants with epilepsy
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9692198/
https://www.ncbi.nlm.nih.gov/pubmed/36447560
http://dx.doi.org/10.1093/braincomms/fcac295
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