Atypical cortical processing of bottom-up speech binding cues in children with autism spectrum disorders.

Autism Functional connectivity Magnetoencephalography Phase-amplitude coupling Speech

Journal

NeuroImage. Clinical
ISSN: 2213-1582
Titre abrégé: Neuroimage Clin
Pays: Netherlands
ID NLM: 101597070

Informations de publication

Date de publication:
2023
Historique:
received: 13 06 2022
revised: 10 01 2023
accepted: 20 01 2023
pubmed: 2 2 2023
medline: 22 3 2023
entrez: 1 2 2023
Statut: ppublish

Résumé

Individuals with autism spectrum disorder (ASD) commonly display speech processing abnormalities. Binding of acoustic features of speech distributed across different frequencies into coherent speech objects is fundamental in speech perception. Here, we tested the hypothesis that the cortical processing of bottom-up acoustic cues for speech binding may be anomalous in ASD. We recorded magnetoencephalography while ASD children (ages 7-17) and typically developing peers heard sentences of sine-wave speech (SWS) and modulated SWS (MSS) where binding cues were restored through increased temporal coherence of the acoustic components and the introduction of harmonicity. The ASD group showed increased long-range feedforward functional connectivity from left auditory to parietal cortex with concurrent decreased local functional connectivity within the parietal region during MSS relative to SWS. As the parietal region has been implicated in auditory object binding, our findings support our hypothesis of atypical bottom-up speech binding in ASD. Furthermore, the long-range functional connectivity correlated with behaviorally measured auditory processing abnormalities, confirming the relevance of these atypical cortical signatures to the ASD phenotype. Lastly, the group difference in the local functional connectivity was driven by the youngest participants, suggesting that impaired speech binding in ASD might be ameliorated upon entering adolescence.

Identifiants

pubmed: 36724734
pii: S2213-1582(23)00025-6
doi: 10.1016/j.nicl.2023.103336
pmc: PMC9898310
pii:
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

103336

Subventions

Organisme : NIMH NIH HHS
ID : R01 MH117998
Pays : United States
Organisme : NICHD NIH HHS
ID : R01 HD073254
Pays : United States
Organisme : NIMH NIH HHS
ID : R21 MH116517
Pays : United States
Organisme : NIDCD NIH HHS
ID : R01 DC015989
Pays : United States
Organisme : NIBIB NIH HHS
ID : P41 EB030006
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS104585
Pays : United States

Informations de copyright

Copyright © 2023. Published by Elsevier Inc.

Déclaration de conflit d'intérêts

Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Auteurs

Jussi Alho (J)

Department of Neurology, Massachusetts General Hospital, Harvard Medical School, 149 13th St, Boston, MA 02129, USA; Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, 149 13th St, Boston, MA 02129, USA. Electronic address: jalho@mgh.harvard.edu.

Sheraz Khan (S)

Department of Neurology, Massachusetts General Hospital, Harvard Medical School, 149 13th St, Boston, MA 02129, USA; Department of Radiology, Massachusetts General Hospital, Harvard Medical School, 149 13th St, Boston, MA 02129, USA; Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, 149 13th St, Boston, MA 02129, USA.

Fahimeh Mamashli (F)

Department of Neurology, Massachusetts General Hospital, Harvard Medical School, 149 13th St, Boston, MA 02129, USA; Department of Radiology, Massachusetts General Hospital, Harvard Medical School, 149 13th St, Boston, MA 02129, USA; Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, 149 13th St, Boston, MA 02129, USA.

Tyler K Perrachione (TK)

Department of Speech, Language, and Hearing Sciences, Boston University, 635 Commonwealth Ave, Boston, MA 02215, USA.

Ainsley Losh (A)

Department of Neurology, Massachusetts General Hospital, Harvard Medical School, 149 13th St, Boston, MA 02129, USA.

Nicole M McGuiggan (NM)

Department of Neurology, Massachusetts General Hospital, Harvard Medical School, 149 13th St, Boston, MA 02129, USA.

Steven Graham (S)

Department of Neurology, Massachusetts General Hospital, Harvard Medical School, 149 13th St, Boston, MA 02129, USA.

Zein Nayal (Z)

Department of Neurology, Massachusetts General Hospital, Harvard Medical School, 149 13th St, Boston, MA 02129, USA.

Robert M Joseph (RM)

Department of Anatomy and Neurobiology, Boston University School of Medicine, 72 East Concord St, Boston, MA 02118, USA.

Matti S Hämäläinen (MS)

Department of Radiology, Massachusetts General Hospital, Harvard Medical School, 149 13th St, Boston, MA 02129, USA; Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, 149 13th St, Boston, MA 02129, USA.

Hari Bharadwaj (H)

Department of Neurology, Massachusetts General Hospital, Harvard Medical School, 149 13th St, Boston, MA 02129, USA; Department of Speech, Language, and Hearing Sciences, and Weldon School of Biomedical Engineering, Purdue University, 715 Clinic Drive, West Lafayette, IN 47907, USA.

Tal Kenet (T)

Department of Neurology, Massachusetts General Hospital, Harvard Medical School, 149 13th St, Boston, MA 02129, USA; Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, 149 13th St, Boston, MA 02129, USA. Electronic address: tal.kenet@mgh.harvard.edu.

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