Gradients in signal complexity of sleep-wake intracerebral EEG.

Spatial variation in the morphology of the electroencephalogram (EEG) over the head is classically described. Ultimately, location-dependent variation in EEG must arise from the cytoarchitectural and network structure of the portion of cortex sensed. In previous work, we demonstrated that over the l...

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Main Authors: Giridhar Kalamangalam, Ioan Mircea Chelaru, Abbas Babajani-Feremi
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0320648
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author Giridhar Kalamangalam
Ioan Mircea Chelaru
Abbas Babajani-Feremi
author_facet Giridhar Kalamangalam
Ioan Mircea Chelaru
Abbas Babajani-Feremi
author_sort Giridhar Kalamangalam
collection DOAJ
description Spatial variation in the morphology of the electroencephalogram (EEG) over the head is classically described. Ultimately, location-dependent variation in EEG must arise from the cytoarchitectural and network structure of the portion of cortex sensed. In previous work, we demonstrated that over the lateral frontal lobe, sample entropy (SE) of intracerebral EEG (iEEG) over a subdural recording contact was predictive of that contact's connectivity to other contacts. In this work, we used a publicly available repository (the Montreal Neurological Institute Atlas; MNIA) of whole-brain normative iEEG to calculate SE over the entire cortical surface. SE was averaged region-wise and classified by the state of arousal (awake, N2, N3 and REM). SE averages were transformed to a linear scale between zero and unity, mapped to continuous color scale and overlaid on segmented cortical surface models, one for each sleep-wake state. Wake SE followed a rostro-caudal gradient (RCG), with high values anteriorly and a global minimum in the posterior cortex. Superimposed on the RCG were other gradients radiating away from primary somatic sensorimotor, visual and auditory regions to their association areas. All gradients were attenuated in deep (N3) sleep. In REM, the majority of the cortex exhibited wake-like SE, with the prominent exception of primary cortical sensory and motor areas. Normative human intracerebral EEG exhibits rich spatial structure - cortical gradients - in the distribution of SE. SE in the wake state tracks temporal processing hierarchies in cerebral cortex, concordant to the distribution of several other cortical attributes of structure (e.g., cortical thickness, myelin content). Sleep disrupts these gradients, with REM sleep bringing out unusual discordances between primary sensory and their association areas. Our results deepen the interpretation of EEG from conventional descriptors such as Berger bands to a spatial perspective related to cortical biology.
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spelling doaj-art-e1bf337cf9634c21a7fe486d4fa616212025-08-20T02:08:23ZengPublic Library of Science (PLoS)PLoS ONE1932-62032025-01-01203e032064810.1371/journal.pone.0320648Gradients in signal complexity of sleep-wake intracerebral EEG.Giridhar KalamangalamIoan Mircea ChelaruAbbas Babajani-FeremiSpatial variation in the morphology of the electroencephalogram (EEG) over the head is classically described. Ultimately, location-dependent variation in EEG must arise from the cytoarchitectural and network structure of the portion of cortex sensed. In previous work, we demonstrated that over the lateral frontal lobe, sample entropy (SE) of intracerebral EEG (iEEG) over a subdural recording contact was predictive of that contact's connectivity to other contacts. In this work, we used a publicly available repository (the Montreal Neurological Institute Atlas; MNIA) of whole-brain normative iEEG to calculate SE over the entire cortical surface. SE was averaged region-wise and classified by the state of arousal (awake, N2, N3 and REM). SE averages were transformed to a linear scale between zero and unity, mapped to continuous color scale and overlaid on segmented cortical surface models, one for each sleep-wake state. Wake SE followed a rostro-caudal gradient (RCG), with high values anteriorly and a global minimum in the posterior cortex. Superimposed on the RCG were other gradients radiating away from primary somatic sensorimotor, visual and auditory regions to their association areas. All gradients were attenuated in deep (N3) sleep. In REM, the majority of the cortex exhibited wake-like SE, with the prominent exception of primary cortical sensory and motor areas. Normative human intracerebral EEG exhibits rich spatial structure - cortical gradients - in the distribution of SE. SE in the wake state tracks temporal processing hierarchies in cerebral cortex, concordant to the distribution of several other cortical attributes of structure (e.g., cortical thickness, myelin content). Sleep disrupts these gradients, with REM sleep bringing out unusual discordances between primary sensory and their association areas. Our results deepen the interpretation of EEG from conventional descriptors such as Berger bands to a spatial perspective related to cortical biology.https://doi.org/10.1371/journal.pone.0320648
spellingShingle Giridhar Kalamangalam
Ioan Mircea Chelaru
Abbas Babajani-Feremi
Gradients in signal complexity of sleep-wake intracerebral EEG.
PLoS ONE
title Gradients in signal complexity of sleep-wake intracerebral EEG.
title_full Gradients in signal complexity of sleep-wake intracerebral EEG.
title_fullStr Gradients in signal complexity of sleep-wake intracerebral EEG.
title_full_unstemmed Gradients in signal complexity of sleep-wake intracerebral EEG.
title_short Gradients in signal complexity of sleep-wake intracerebral EEG.
title_sort gradients in signal complexity of sleep wake intracerebral eeg
url https://doi.org/10.1371/journal.pone.0320648
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