Electroencephalographic Microstates as Novel Functional Biomarkers for Adult Attention-Deficit/Hyperactivity Disorder

Victor Férat; Martijn Arns; Marie Pierre Deiber; Roland Hasler; Nader Perroud; Christoph M. Michel; Tomas Ros

doi:10.1016/j.bpsc.2021.11.006

Electroencephalographic Microstates as Novel Functional Biomarkers for Adult Attention-Deficit/Hyperactivity Disorder

Victor Férat, Martijn Arns, Marie Pierre Deiber, Roland Hasler, Nader Perroud, Christoph M. Michel, Tomas Ros

Research output: Contribution to journal › Article › peer-review

26 Citations (Scopus)

Abstract

Background: Research on the electroencephalographic (EEG) signatures of attention-deficit/hyperactivity disorder (ADHD) has historically concentrated on its frequency spectrum or event-related evoked potentials. In this work, we investigate EEG microstates (MSs), an alternative framework defined by the clustering of recurring topographical patterns, as a novel approach for examining large-scale cortical dynamics in ADHD. Methods: Using k-means clustering, we studied the spatiotemporal dynamics of ADHD during the rest condition by comparing the MS segmentations between adult patients with ADHD and neurotypical control subjects across two independent datasets: the first dataset consisted of 66 patients with ADHD and 66 control subjects, and the second dataset comprised 22 patients with ADHD and 22 control subjects and was used for out-of-sample validation. Results: Spatially, patients with ADHD and control subjects displayed equivalent MS topographies (canonical maps), indicating the preservation of prototypical EEG generators in patients with ADHD. However, this concordance was accompanied by significant differences in temporal dynamics. At the group level, and across both datasets, ADHD diagnosis was associated with longer mean durations of a frontocentral topography (MS D), indicating that its electrocortical generator(s) could be acting as pronounced attractors of global cortical dynamics. In addition, its spatiotemporal metrics were correlated with sleep disturbance, the latter being known to have a strong relationship with ADHD. Finally, in the first (larger) dataset, we also found evidence of decreased time coverage and mean duration of a left-right diagonal topography (MS A), which inversely correlated with ADHD scores. Conclusions: Overall, our study underlines the value of EEG MSs as promising functional biomarkers for ADHD, offering an additional lens through which to examine its neurophysiological mechanisms.

Original language	English
Journal	Biological Psychiatry: Cognitive Neuroscience and Neuroimaging
DOIs	https://doi.org/10.1016/j.bpsc.2021.11.006
Publication status	Accepted/In press - 2022
Externally published	Yes

Bibliographical note

Funding Information:
This study was supported by the Swiss National Science Foundation, Switzerland (NCCR Synapsy Grant No. 51NF40 – 185897 and Grant No. 320030_184677 [to CMM]).

Funding Information:
This study was supported by the Swiss National Science Foundation, Switzerland (NCCR Synapsy Grant No. 51NF40 ? 185897 and Grant No. 320030_184677 [to CMM]). MA is the unpaid chairman of the nonprofit Brainclinics Foundation, a minority shareholder in neuroCare Group (Munich, Germany), and a coinventor on four patent applications related to electroencephalographic, neuromodulation, and psychophysiology, but receives no royalties related to these patents. All other authors report no biomedical financial interests or potential conflicts of interest.

Publisher Copyright:
© 2021 Society of Biological Psychiatry

ASJC Scopus Subject Areas

Radiology Nuclear Medicine and imaging
Clinical Neurology
Cognitive Neuroscience
Biological Psychiatry

PubMed: MeSH publication types

Journal Article
Research Support, Non-U.S. Gov't

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10.1016/j.bpsc.2021.11.006

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@article{9c697c37e2b6407ab4bebfa968a5681b,

title = "Electroencephalographic Microstates as Novel Functional Biomarkers for Adult Attention-Deficit/Hyperactivity Disorder",

abstract = "Background: Research on the electroencephalographic (EEG) signatures of attention-deficit/hyperactivity disorder (ADHD) has historically concentrated on its frequency spectrum or event-related evoked potentials. In this work, we investigate EEG microstates (MSs), an alternative framework defined by the clustering of recurring topographical patterns, as a novel approach for examining large-scale cortical dynamics in ADHD. Methods: Using k-means clustering, we studied the spatiotemporal dynamics of ADHD during the rest condition by comparing the MS segmentations between adult patients with ADHD and neurotypical control subjects across two independent datasets: the first dataset consisted of 66 patients with ADHD and 66 control subjects, and the second dataset comprised 22 patients with ADHD and 22 control subjects and was used for out-of-sample validation. Results: Spatially, patients with ADHD and control subjects displayed equivalent MS topographies (canonical maps), indicating the preservation of prototypical EEG generators in patients with ADHD. However, this concordance was accompanied by significant differences in temporal dynamics. At the group level, and across both datasets, ADHD diagnosis was associated with longer mean durations of a frontocentral topography (MS D), indicating that its electrocortical generator(s) could be acting as pronounced attractors of global cortical dynamics. In addition, its spatiotemporal metrics were correlated with sleep disturbance, the latter being known to have a strong relationship with ADHD. Finally, in the first (larger) dataset, we also found evidence of decreased time coverage and mean duration of a left-right diagonal topography (MS A), which inversely correlated with ADHD scores. Conclusions: Overall, our study underlines the value of EEG MSs as promising functional biomarkers for ADHD, offering an additional lens through which to examine its neurophysiological mechanisms.",

author = "Victor F{\'e}rat and Martijn Arns and Deiber, {Marie Pierre} and Roland Hasler and Nader Perroud and Michel, {Christoph M.} and Tomas Ros",

note = "Funding Information: This study was supported by the Swiss National Science Foundation, Switzerland (NCCR Synapsy Grant No. 51NF40 – 185897 and Grant No. 320030_184677 [to CMM]). Funding Information: This study was supported by the Swiss National Science Foundation, Switzerland (NCCR Synapsy Grant No. 51NF40 ? 185897 and Grant No. 320030_184677 [to CMM]). MA is the unpaid chairman of the nonprofit Brainclinics Foundation, a minority shareholder in neuroCare Group (Munich, Germany), and a coinventor on four patent applications related to electroencephalographic, neuromodulation, and psychophysiology, but receives no royalties related to these patents. All other authors report no biomedical financial interests or potential conflicts of interest. Publisher Copyright: {\textcopyright} 2021 Society of Biological Psychiatry",

year = "2022",

doi = "10.1016/j.bpsc.2021.11.006",

language = "English",

journal = "Biological Psychiatry: Cognitive Neuroscience and Neuroimaging",

issn = "2451-9022",

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T1 - Electroencephalographic Microstates as Novel Functional Biomarkers for Adult Attention-Deficit/Hyperactivity Disorder

AU - Férat, Victor

AU - Arns, Martijn

AU - Deiber, Marie Pierre

AU - Hasler, Roland

AU - Perroud, Nader

AU - Michel, Christoph M.

AU - Ros, Tomas

N1 - Funding Information: This study was supported by the Swiss National Science Foundation, Switzerland (NCCR Synapsy Grant No. 51NF40 – 185897 and Grant No. 320030_184677 [to CMM]). Funding Information: This study was supported by the Swiss National Science Foundation, Switzerland (NCCR Synapsy Grant No. 51NF40 ? 185897 and Grant No. 320030_184677 [to CMM]). MA is the unpaid chairman of the nonprofit Brainclinics Foundation, a minority shareholder in neuroCare Group (Munich, Germany), and a coinventor on four patent applications related to electroencephalographic, neuromodulation, and psychophysiology, but receives no royalties related to these patents. All other authors report no biomedical financial interests or potential conflicts of interest. Publisher Copyright: © 2021 Society of Biological Psychiatry

PY - 2022

Y1 - 2022

N2 - Background: Research on the electroencephalographic (EEG) signatures of attention-deficit/hyperactivity disorder (ADHD) has historically concentrated on its frequency spectrum or event-related evoked potentials. In this work, we investigate EEG microstates (MSs), an alternative framework defined by the clustering of recurring topographical patterns, as a novel approach for examining large-scale cortical dynamics in ADHD. Methods: Using k-means clustering, we studied the spatiotemporal dynamics of ADHD during the rest condition by comparing the MS segmentations between adult patients with ADHD and neurotypical control subjects across two independent datasets: the first dataset consisted of 66 patients with ADHD and 66 control subjects, and the second dataset comprised 22 patients with ADHD and 22 control subjects and was used for out-of-sample validation. Results: Spatially, patients with ADHD and control subjects displayed equivalent MS topographies (canonical maps), indicating the preservation of prototypical EEG generators in patients with ADHD. However, this concordance was accompanied by significant differences in temporal dynamics. At the group level, and across both datasets, ADHD diagnosis was associated with longer mean durations of a frontocentral topography (MS D), indicating that its electrocortical generator(s) could be acting as pronounced attractors of global cortical dynamics. In addition, its spatiotemporal metrics were correlated with sleep disturbance, the latter being known to have a strong relationship with ADHD. Finally, in the first (larger) dataset, we also found evidence of decreased time coverage and mean duration of a left-right diagonal topography (MS A), which inversely correlated with ADHD scores. Conclusions: Overall, our study underlines the value of EEG MSs as promising functional biomarkers for ADHD, offering an additional lens through which to examine its neurophysiological mechanisms.

AB - Background: Research on the electroencephalographic (EEG) signatures of attention-deficit/hyperactivity disorder (ADHD) has historically concentrated on its frequency spectrum or event-related evoked potentials. In this work, we investigate EEG microstates (MSs), an alternative framework defined by the clustering of recurring topographical patterns, as a novel approach for examining large-scale cortical dynamics in ADHD. Methods: Using k-means clustering, we studied the spatiotemporal dynamics of ADHD during the rest condition by comparing the MS segmentations between adult patients with ADHD and neurotypical control subjects across two independent datasets: the first dataset consisted of 66 patients with ADHD and 66 control subjects, and the second dataset comprised 22 patients with ADHD and 22 control subjects and was used for out-of-sample validation. Results: Spatially, patients with ADHD and control subjects displayed equivalent MS topographies (canonical maps), indicating the preservation of prototypical EEG generators in patients with ADHD. However, this concordance was accompanied by significant differences in temporal dynamics. At the group level, and across both datasets, ADHD diagnosis was associated with longer mean durations of a frontocentral topography (MS D), indicating that its electrocortical generator(s) could be acting as pronounced attractors of global cortical dynamics. In addition, its spatiotemporal metrics were correlated with sleep disturbance, the latter being known to have a strong relationship with ADHD. Finally, in the first (larger) dataset, we also found evidence of decreased time coverage and mean duration of a left-right diagonal topography (MS A), which inversely correlated with ADHD scores. Conclusions: Overall, our study underlines the value of EEG MSs as promising functional biomarkers for ADHD, offering an additional lens through which to examine its neurophysiological mechanisms.

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Electroencephalographic Microstates as Novel Functional Biomarkers for Adult Attention-Deficit/Hyperactivity Disorder

Abstract

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