Atypical Functional Connectivity During Unfamiliar Music Listening in Children With Autism

Carina Freitas; Benjamin A E Hunt; Simeon M Wong; Leanne Ristic; Susan Fragiadakis; Stephanie Chow; Alana Iaboni; Jessica Brian; Latha Soorya; Joyce L Chen; Russell Schachar; Benjamin T Dunkley; Margot J Taylor; Jason P Lerch; Evdokia Anagnostou

doi:10.3389/fnins.2022.829415

Atypical Functional Connectivity During Unfamiliar Music Listening in Children With Autism

Front Neurosci. 2022 Apr 19:16:829415. doi: 10.3389/fnins.2022.829415. eCollection 2022.

Authors

Carina Freitas^{1

2}, Benjamin A E Hunt^{3

4}, Simeon M Wong^{3

4}, Leanne Ristic², Susan Fragiadakis², Stephanie Chow², Alana Iaboni², Jessica Brian^{2

5}, Latha Soorya⁶, Joyce L Chen⁷, Russell Schachar⁸, Benjamin T Dunkley^{3

4}, Margot J Taylor^{1

3

4

9}, Jason P Lerch^{4

10

11}, Evdokia Anagnostou^{1

2

4

5}

Affiliations

¹ Institute of Medical Science, Faculty of Medicine, University of Toronto, Toronto, ON, Canada.
² Bloorview Research Institute, Holland Bloorview Kids Rehabilitation Hospital, Toronto, ON, Canada.
³ Department of Diagnostic Imaging, Hospital for Sick Children, Toronto, ON, Canada.
⁴ Neuroscience and Mental Health Program, Hospital for Sick Children Research Institute, Toronto, ON, Canada.
⁵ Department of Paediatrics, University of Toronto, Toronto, ON, Canada.
⁶ Department of Psychiatry, Rush University Medical Center, Chicago, IL, United States.
⁷ Faculty of Kinesiology and Physical Education and Rehabilitation Sciences Institute, University of Toronto, Toronto, ON, Canada.
⁸ Department of Psychiatry Research, Hospital for Sick Children, Toronto, ON, Canada.
⁹ Departments of Psychology and Medical Imaging, University of Toronto, Toronto, ON, Canada.
¹⁰ Department of Medical Biophysics, University of Toronto, Toronto, ON, Canada.
¹¹ Wellcome Centre for Integrative Neuroimaging, University of Oxford, Oxford, United Kingdom.

Abstract

Background: Atypical processing of unfamiliar, but less so familiar, stimuli has been described in Autism Spectrum Disorder (ASD), in particular in relation to face processing. We examined the construct of familiarity in ASD using familiar and unfamiliar songs, to investigate the link between familiarity and autism symptoms, such as repetitive behavior.

Methods: Forty-eight children, 24 with ASD (21 males, mean age = 9.96 years ± 1.54) and 24 typically developing (TD) controls (21 males, mean age = 10.17 ± 1.90) completed a music familiarity task using individually identified familiar compared to unfamiliar songs, while magnetoencephalography (MEG) was recorded. Each song was presented for 30 s. We used both amplitude envelope correlation (AEC) and the weighted phase lag index (wPLI) to assess functional connectivity between specific regions of interest (ROI) and non-ROI parcels, as well as at the whole brain level, to understand what is preserved and what is impaired in familiar music listening in this population.

Results: Increased wPLI synchronization for familiar vs. unfamiliar music was found for typically developing children in the gamma frequency. There were no significant differences within the ASD group for this comparison. During the processing of unfamiliar music, we demonstrated left lateralized increased theta and beta band connectivity in children with ASD compared to controls. An interaction effect found greater alpha band connectivity in the TD group compared to ASD to unfamiliar music only, anchored in the left insula.

Conclusion: Our results revealed atypical processing of unfamiliar songs in children with ASD, consistent with previous studies in other modalities reporting that processing novelty is a challenge for ASD. Relatively typical processing of familiar stimuli may represent a strength and may be of interest to strength-based intervention planning.

Keywords: autism spectrum disorder; familiarity processing; functional connectivity; magnetoencephalography; music; neural oscillation.