Sleep Spindle-Related EEG Connectivity in Children with Attention-Deficit/Hyperactivity Disorder: An Exploratory Study

Overview

Journal Entropy (Basel)

Publisher MDPI

Date 2023 Sep 28

PMID 37761543

Authors

Caterina Zanus

Aleksandar Miladinovic

Federica De Dea

Aldo Skabar

Matteo Stecca

Milos Ajcevic

Agostino Accardo

Marco Carrozzi

Affiliations

Soon will be listed here.

Abstract

Attention-deficit/hyperactivity disorder (ADHD) is a neurobehavioral disorder with known brain abnormalities but no biomarkers to support clinical diagnosis. Recently, EEG analysis methods such as functional connectivity have rekindled interest in using EEG for ADHD diagnosis. Most studies have focused on resting-state EEG, while connectivity during sleep and spindle activity has been underexplored. Here we present the results of a preliminary study exploring spindle-related connectivity as a possible biomarker for ADHD. We compared sensor-space connectivity parameters in eight children with ADHD and nine age/sex-matched healthy controls during sleep, before, during, and after spindle activity in various frequency bands. All connectivity parameters were significantly different between the two groups in the delta and gamma bands, and Principal Component Analysis (PCA) in the gamma band distinguished ADHD from healthy subjects. Cluster coefficient and path length values in the sigma band were also significantly different between epochs, indicating different spindle-related brain activity in ADHD.

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References

Gruber R, Cassoff J . The interplay between sleep and emotion regulation: conceptual framework empirical evidence and future directions. Curr Psychiatry Rep. 2014; 16(11):500. DOI: 10.1007/s11920-014-0500-x. View

Ueda R, Takeichi H, Kaga Y, Oguri M, Saito Y, Nakagawa E . Atypical gamma functional connectivity pattern during light sleep in children with attention deficit hyperactivity disorder. Brain Dev. 2019; 42(2):129-139. DOI: 10.1016/j.braindev.2019.11.001. View

Valderrama M, Crepon B, Botella-Soler V, Martinerie J, Hasboun D, Alvarado-Rojas C . Human gamma oscillations during slow wave sleep. PLoS One. 2012; 7(4):e33477. PMC: 3319559. DOI: 10.1371/journal.pone.0033477. View

Steriade M, Contreras D, Amzica F . Synchronized sleep oscillations and their paroxysmal developments. Trends Neurosci. 1994; 17(5):199-208. DOI: 10.1016/0166-2236(94)90105-8. View

Telesford Q, Simpson S, Burdette J, Hayasaka S, Laurienti P . The brain as a complex system: using network science as a tool for understanding the brain. Brain Connect. 2012; 1(4):295-308. PMC: 3621511. DOI: 10.1089/brain.2011.0055. View

Mikoteit T, Brand S, Perren S, von Wyl A, von Klitzing K, Kurath J . Visually detected non-rapid eye movement stage 2 sleep spindle density at age five years predicted prosocial behavior positively and hyperactivity scores negatively at age nine years. Sleep Med. 2018; 48:101-106. DOI: 10.1016/j.sleep.2018.03.028. View

Liu T, Chen Y, Lin P, Wang J . Small-World Brain Functional Networks in Children With Attention-Deficit/Hyperactivity Disorder Revealed by EEG Synchrony. Clin EEG Neurosci. 2014; 46(3):183-91. DOI: 10.1177/1550059414523959. View

von Bunau P, Meinecke F, Scholler S, Muller K . Finding stationary brain sources in EEG data. Annu Int Conf IEEE Eng Med Biol Soc. 2010; 2010:2810-3. DOI: 10.1109/IEMBS.2010.5626537. View

Astolfi L, Cincotti F, Mattia D, Marciani M, Baccala L, Fallani F . Assessing cortical functional connectivity by partial directed coherence: simulations and application to real data. IEEE Trans Biomed Eng. 2006; 53(9):1802-12. DOI: 10.1109/TBME.2006.873692. View

10.

Alba G, Pereda E, Manas S, Mendez L, Gonzalez A, Gonzalez J . Electroencephalography signatures of attention-deficit/hyperactivity disorder: clinical utility. Neuropsychiatr Dis Treat. 2015; 11:2755-69. PMC: 4622521. DOI: 10.2147/NDT.S51783. View

11.

Furlong S, Cohen J, Hopfinger J, Snyder J, Robertson M, Sheridan M . Resting-state EEG Connectivity in Young Children with ADHD. J Clin Child Adolesc Psychol. 2020; 50(6):746-762. PMC: 7889746. DOI: 10.1080/15374416.2020.1796680. View

12.

Arpaia P, Covino A, Cristaldi L, Frosolone M, Gargiulo L, Mancino F . A Systematic Review on Feature Extraction in Electroencephalography-Based Diagnostics and Therapy in Attention Deficit Hyperactivity Disorder. Sensors (Basel). 2022; 22(13). PMC: 9269717. DOI: 10.3390/s22134934. View

13.

Titone S, Samogin J, Peigneux P, Swinnen S, Mantini D, Albouy G . Frequency-dependent connectivity in large-scale resting-state brain networks during sleep. Eur J Neurosci. 2023; 59(4):686-702. DOI: 10.1111/ejn.16080. View

14.

Chiarenza G . Quantitative EEG in Childhood Attention Deficit Hyperactivity Disorder and Learning Disabilities. Clin EEG Neurosci. 2020; 52(2):144-155. DOI: 10.1177/1550059420962343. View

15.

Chang M, Ouyang C, Chiang C, Yang R, Wu R, Wu H . A New Method of Diagnosing Attention-Deficit Hyperactivity Disorder in Male Patients by Quantitative EEG Analysis. Clin EEG Neurosci. 2019; 50(5):339-347. DOI: 10.1177/1550059419859164. View

16.

Vecchio F, Miraglia F, Gorgoni M, Ferrara M, Iberite F, Bramanti P . Cortical connectivity modulation during sleep onset: A study via graph theory on EEG data. Hum Brain Mapp. 2017; 38(11):5456-5464. PMC: 6866973. DOI: 10.1002/hbm.23736. View

17.

Lenartowicz A, Loo S . Use of EEG to diagnose ADHD. Curr Psychiatry Rep. 2014; 16(11):498. PMC: 4633088. DOI: 10.1007/s11920-014-0498-0. View

18.

McVoy M, Lytle S, Fulchiero E, Aebi M, Adeleye O, Sajatovic M . A systematic review of quantitative EEG as a possible biomarker in child psychiatric disorders. Psychiatry Res. 2019; 279:331-344. DOI: 10.1016/j.psychres.2019.07.004. View

19.

Ahmadi M, Kazemi K, Kuc K, Cybulska-Klosowicz A, Zakrzewska M, Racicka-Pawlukiewicz E . Cortical source analysis of resting state EEG data in children with attention deficit hyperactivity disorder. Clin Neurophysiol. 2020; 131(9):2115-2130. DOI: 10.1016/j.clinph.2020.05.028. View

20.

Castelnovo A, Lividini A, Bernardi G, Pezzoli V, Foderaro G, Ramelli G . Sleep Power Topography in Children with Attention Deficit Hyperactivity Disorder (ADHD). Children (Basel). 2022; 9(2). PMC: 8870029. DOI: 10.3390/children9020197. View