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Abnormalities in both stimulus-induced and baseline MEG alpha oscillations in the auditory cortex of children with Autism Spectrum Disorder

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Vardan Arutiunian at Seattle Children’s Research Institute
Vardan Arutiunian
Giorgio Arcara at IRCCS Ospedale San Camillo
Giorgio Arcara
Irina Buyanova at University of Otago
Irina Buyanova
Makar Fedorov at Ural Federal University
Makar Fedorov
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Abstract and Figures

The neurobiology of Autism Spectrum Disorder (ASD) is hypothetically related to the imbalance between neural excitation (E) and inhibition (I). Different studies have revealed that alpha-band (8–12 Hz) activity in magneto- and electroencephalography (MEG and EEG) may reflect E and I processes and, thus, can be of particular interest in ASD research. Previous findings indicated alterations in event-related and baseline alpha activity in different cortical systems in individuals with ASD, and these abnormalities were associated with core and co-occurring conditions of ASD. However, the knowledge on auditory alpha oscillations in this population is limited. This MEG study investigated stimulus-induced (Event-Related Desynchronization, ERD) and baseline alpha-band activity (both periodic and aperiodic) in the auditory cortex and also the relationships between these neural activities and behavioral measures of children with ASD. Ninety amplitude-modulated tones were presented to two groups of children: 20 children with ASD (5 girls, Mage = 10.03, SD = 1.7) and 20 typically developing controls (9 girls, Mage = 9.11, SD = 1.3). Children with ASD had a bilateral reduction of alpha-band ERD, reduced baseline aperiodic-adjusted alpha power, and flattened aperiodic exponent in comparison to TD children. Moreover, lower raw baseline alpha power and aperiodic offset in the language-dominant left auditory cortex were associated with better language skills of children with ASD measured in formal assessment. The findings highlighted the alterations of E / I balance metrics in response to basic auditory stimuli in children with ASD and also provided evidence for the contribution of low-level processing to language difficulties in ASD.
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ORIGINAL ARTICLE
Brain Structure and Function (2024) 229:1225–1242
https://doi.org/10.1007/s00429-024-02802-7
Vardan Arutiunian
vardan.arutyunyan89@gmail.com
1 Center for Child Health, Behavior and Development, Seattle
Children’s Research Institute, 1920 Terry Ave, Seattle,
WA 98101, United States of America
2 Center for Language and Brain, HSE University, Moscow,
Russia
3 IRCCS San Camillo Hospital, Venice, Italy
4 Center for Language and Brain, HSE University, Nizhny
Novgorod, Russia
5 Federal Resource Center for ASD, Moscow State University
of Psychology and Education, Moscow, Russia
6 Haskins Laboratories, New Haven, CT, United States of
America
7 Institute of Linguistics, Russian Academy of Sciences,
Moscow, Russia
8 ChairofDierentialPsychologyandPsychophysiology,
Moscow State University of Psychology and Education,
Moscow, Russia
9 ScienticResearchandPracticalCenterofPediatric
Psychoneurology, Moscow, Russia
10 University of Otago, Dunedin, New Zealand
Abstract
The neurobiology of Autism Spectrum Disorder (ASD) is hypothetically related to the imbalance between neural excitation
(E)andinhibition(I).Dierentstudieshaverevealedthatalpha-band(8–12Hz)activityinmagneto-andelectroencepha-
lography(MEGandEEG)mayreectEandIprocessesand,thus,canbeofparticularinterestinASDresearch.Previous
ndingsindicatedalterationsinevent-relatedandbaselinealphaactivityindierentcorticalsystemsinindividualswith
ASD,and these abnormalities were associatedwith core and co-occurring conditionsofASD. However,the knowledge
onauditoryalphaoscillationsinthispopulationislimited.ThisMEGstudyinvestigatedstimulus-induced(Event-Related
Desynchronization,ERD)andbaselinealpha-bandactivity(bothperiodicandaperiodic)intheauditorycortexandalsothe
relationshipsbetweentheseneuralactivitiesandbehavioral measuresofchildren withASD.Ninetyamplitude-modulated
tones were presented to two groups of children: 20 children with ASD (5 girls, Mage = 10.03, SD = 1.7) and 20 typically
developing controls (9 girls, Mage = 9.11, SD =1.3). Children with ASD had a bilateral reduction of alpha-band ERD,
reducedbaselineaperiodic-adjustedalphapower,and attened aperiodic exponent incomparisontoTD children. More-
over,lower raw baselinealphapowerandaperiodicosetinthe language-dominant left auditory cortex wereassociated
withbetter languageskillsofchildren withASD measuredinformal assessment.Thendings highlightedthealterations
of E / I balance metrics in response to basic auditory stimuli in children with ASD and also provided evidence for the
contributionof low-level processing tolanguagedicultiesinASD.
Keywords AutismSpectrum Disorder·Auditorycortex·Event-relateddesynchronization (ERD)·Excitation(E)/
inhibition (I) balance · Language abilities · Periodic and aperiodic activity
Received: 8 July 2023 / Accepted: 22 April 2024 / Published online: 29 April 2024
© The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2024
Abnormalities in both stimulus-induced and baseline MEG alpha
oscillations in the auditory cortex of children with Autism Spectrum
Disorder
VardanArutiunian1· GiorgioArcara3· IrinaBuyanova2,10· MakarFedorov4· ElizavetaDavydova5,8·
DaryaPereverzeva5· AlexanderSorokin5,6· SvetlanaTyushkevich5· UlianaMamokhina5· KamillaDanilina5,9·
OlgaDragoy2,7
1 3
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