Altered maturation and atypical cortical processing of spoken sentences in autism spectrum disorder.


Journal

Progress in neurobiology
ISSN: 1873-5118
Titre abrégé: Prog Neurobiol
Pays: England
ID NLM: 0370121

Informations de publication

Date de publication:
08 2021
Historique:
received: 15 01 2021
revised: 14 04 2021
accepted: 19 05 2021
pubmed: 26 5 2021
medline: 15 2 2022
entrez: 25 5 2021
Statut: ppublish

Résumé

Autism spectrum disorder (ASD) is associated with widespread receptive language impairments, yet the neural mechanisms underlying these deficits are poorly understood. Neuroimaging has shown that processing of socially-relevant sounds, including speech and non-speech, is atypical in ASD. However, it is unclear how the presence of lexical-semantic meaning affects speech processing in ASD. Here, we recorded magnetoencephalography data from individuals with ASD (N = 22, ages 7-17, 4 females) and typically developing (TD) peers (N = 30, ages 7-17, 5 females) during unattended listening to meaningful auditory speech sentences and meaningless jabberwocky sentences. After adjusting for age, ASD individuals showed stronger responses to meaningless jabberwocky sentences than to meaningful speech sentences in the same left temporal and parietal language regions where TD individuals exhibited stronger responses to meaningful speech. Maturational trajectories of meaningful speech responses were atypical in temporal, but not parietal, regions in ASD. Temporal responses were associated with ASD severity, while parietal responses were associated with aberrant involuntary attentional shifting in ASD. Our findings suggest a receptive speech processing dysfunction in ASD, wherein unattended meaningful speech elicits abnormal engagement of the language system, while unattended meaningless speech, filtered out in TD individuals, engages the language system through involuntary attention capture.

Identifiants

pubmed: 34033856
pii: S0301-0082(21)00091-5
doi: 10.1016/j.pneurobio.2021.102077
pmc: PMC8500341
mid: NIHMS1709682
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

102077

Subventions

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

Informations de copyright

Copyright © 2021 Elsevier Ltd. All rights reserved.

Références

Arch Pediatr Adolesc Med. 2007 Apr;161(4):378-83
pubmed: 17404135
J Child Psychol Psychiatry. 2002 Sep;43(6):807-21
pubmed: 12236615
Proc Natl Acad Sci U S A. 2016 Oct 11;113(41):E6256-E6262
pubmed: 27671642
J Neurosci Methods. 2007 Aug 15;164(1):177-90
pubmed: 17517438
Science. 1975 Jul 18;189(4198):226-8
pubmed: 17733889
Med Biol Eng Comput. 1994 Jan;32(1):35-42
pubmed: 8182960
Neuroimage Clin. 2015 Mar 06;7:732-41
pubmed: 25844325
J Autism Dev Disord. 2008 Sep;38(8):1426-38
pubmed: 18188685
Dev Neurosci. 2017;39(5):430-441
pubmed: 28772264
Autism Res. 2021 Jun;14(6):1101-1114
pubmed: 33709531
Trends Cogn Sci. 2014 Mar;18(3):120-6
pubmed: 24440115
Clin Psychol Rev. 2014 Feb;34(1):73-86
pubmed: 24424351
Am J Psychiatry. 2003 Nov;160(11):2057-60
pubmed: 14594758
Am J Psychiatry. 2004 Nov;161(11):2117-20
pubmed: 15514415
Phys Med Biol. 2006 Apr 7;51(7):1759-68
pubmed: 16552102
Sci Rep. 2017 Dec 7;7(1):17116
pubmed: 29215027
Biol Psychiatry. 2007 Feb 15;61(4):474-81
pubmed: 16650833
J Autism Dev Disord. 2009 Jan;39(1):1-11
pubmed: 18512135
Neuroimage. 2009 Jan 1;44(1):83-98
pubmed: 18501637
J Speech Lang Hear Res. 2007 Oct;50(5):1350-64
pubmed: 17905916
Brain Res Dev Brain Res. 2003 Sep 10;144(2):201-9
pubmed: 12935917
Nat Neurosci. 2009 Jun;12(6):718-24
pubmed: 19471271
J Child Psychol Psychiatry. 2006 Jan;47(1):88-98
pubmed: 16405645
Int J Psychophysiol. 2008 May;68(2):170-5
pubmed: 18304666
Ann Neurol. 2017 Feb;81(2):199-211
pubmed: 27977875
J Autism Dev Disord. 2000 Jun;30(3):205-23
pubmed: 11055457
Cortex. 2015 Jul;68:100-10
pubmed: 25444577
J Child Lang. 2003 Feb;30(1):213-36
pubmed: 12718299
Proc Natl Acad Sci U S A. 2011 Feb 8;108(6):2522-7
pubmed: 21224415
J Neurophysiol. 2010 Aug;104(2):1177-94
pubmed: 20410363
J Neurosci Methods. 2015 Jul 30;250:85-93
pubmed: 25128255
Soc Cogn Affect Neurosci. 2015 Oct;10(10):1413-23
pubmed: 25809403
Proc Natl Acad Sci U S A. 2012 Feb 21;109(8):E505-14
pubmed: 22308358
Brain. 2010 Dec;133(Pt 12):3745-54
pubmed: 20926367
Phys Med Biol. 1987 Jan;32(1):91-7
pubmed: 3823145
Autism Res. 2019 Aug;12(8):1225-1235
pubmed: 31136103
Hum Brain Mapp. 2018 Oct;39(10):4094-4104
pubmed: 29947148
Nat Neurosci. 2004 Aug;7(8):801-2
pubmed: 15258587
Hum Brain Mapp. 2006 Jan;27(1):1-13
pubmed: 16082624
Psychiatry Clin Neurosci. 2020 Jan;74(1):1-11
pubmed: 31472015
Neurosci Biobehav Rev. 2008;32(1):123-42
pubmed: 17706781
Neurosci Lett. 2007 Mar 6;414(2):136-40
pubmed: 17197079
Mol Autism. 2015 Dec 30;6:69
pubmed: 26719787
Hum Brain Mapp. 2010 Jan;31(1):140-9
pubmed: 19639553
Biol Psychiatry. 2011 Aug 1;70(3):263-9
pubmed: 21392733
Neuropsychologia. 2010 Aug;48(10):2940-51
pubmed: 20542048
Neuroimage. 2001 Dec;14(6):1424-31
pubmed: 11707098
Dev Sci. 2005 Jan;8(1):F1-F12
pubmed: 15647058
Int J Lang Commun Disord. 2010 Nov-Dec;45(6):681-90
pubmed: 20102259
Nature. 1976 Dec 23-30;264(5588):705-12
pubmed: 189195
Brain Res. 2005 Dec 20;1066(1-2):147-57
pubmed: 16325159
Neuroimage. 2019 Feb 1;186:586-594
pubmed: 30481591
Mol Autism. 2019 Aug 15;10:34
pubmed: 31428297
Neuroimage. 1999 Feb;9(2):179-94
pubmed: 9931268
Proc Natl Acad Sci U S A. 2003 Apr 29;100(9):5567-72
pubmed: 12702776
Eur J Neurosci. 2008 Feb;27(4):1026-36
pubmed: 18333970
Behav Res Methods Instrum Comput. 2004 Aug;36(3):481-7
pubmed: 15641436
J Child Psychol Psychiatry. 2012 Mar;53(3):219-33
pubmed: 22188468
Biol Psychiatry. 2015 May 1;77(9):794-804
pubmed: 25064418
Front Hum Neurosci. 2013 Aug 07;7:458
pubmed: 23966925
Neurosci Biobehav Rev. 2013 May;37(4):697-704
pubmed: 23313648
Nat Rev Neurosci. 2016 May;17(5):323-32
pubmed: 27040907
J Autism Dev Disord. 2013 Sep;43(9):2114-20
pubmed: 23334808
Neuron. 2007 Jan 4;53(1):9-16
pubmed: 17196526
Cognition. 2004 May-Jun;92(1-2):145-77
pubmed: 15037129
J Child Psychol Psychiatry. 2004 Sep;45(6):1107-14
pubmed: 15257667
PLoS One. 2012;7(8):e44062
pubmed: 22937153
Neuron. 2015 Apr 22;86(2):567-77
pubmed: 25864635
Dev Cogn Neurosci. 2019 Apr;36:100640
pubmed: 30974225
Brain. 2015 May;138(Pt 5):1394-409
pubmed: 25765326
Radiology. 2011 Aug;260(2):521-30
pubmed: 21628495
Neuroimage. 2006 May 15;31(1):160-71
pubmed: 16520063
IEEE Trans Neural Netw. 1999;10(3):626-34
pubmed: 18252563
Nat Rev Neurosci. 2007 May;8(5):393-402
pubmed: 17431404
Neuroimage Clin. 2016 Apr 06;11:566-577
pubmed: 27158589
Neuropsychologia. 2008;46(7):1828-51
pubmed: 18471837
Mol Autism. 2013 Oct 08;4(1):38
pubmed: 24103585
Dev Cogn Neurosci. 2016 Feb;17:46-56
pubmed: 26708773
Front Hum Neurosci. 2020 Jul 10;14:267
pubmed: 32754020
Neuroimage. 1999 Feb;9(2):195-207
pubmed: 9931269

Auteurs

Jussi Alho (J)

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

Hari Bharadwaj (H)

Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA; Department of Speech, Language, and Hearing Sciences, and Weldon School of Biomedical Engineering, Purdue University, West Lafayette, IN, USA.

Sheraz Khan (S)

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

Fahimeh Mamashli (F)

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

Tyler K Perrachione (TK)

Department of Speech, Language, and Hearing Sciences, Boston University, Boston, MA, USA.

Ainsley Losh (A)

Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA; Graduate School of Education, University of California, Riverside, CA, USA.

Nicole M McGuiggan (NM)

Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.

Robert M Joseph (RM)

Department of Anatomy and Neurobiology, Boston University School of Medicine, Boston, MA, USA.

Matti S Hämäläinen (MS)

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

Tal Kenet (T)

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

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH