Atypical early neural responses to native and non-native language in infants at high likelihood for developing autism

Abstract Background Language difficulties are common in autism spectrum disorder (ASD), a neurodevelopmental condition characterized by impairments in social communication as well as restricted and repetitive behaviors. Amongst infant siblings of children with an ASD diagnosis – who are at higher li...

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Main Authors: Lauren Wagner, Megan Banchik, Tawny Tsang, Nana J. Okada, Rebecca Altshuler, Nicole McDonald, Susan Y. Bookheimer, Shafali S. Jeste, Shulamite Green, Mirella Dapretto
Format: Article
Language:English
Published: BMC 2025-02-01
Series:Molecular Autism
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Online Access:https://doi.org/10.1186/s13229-025-00640-w
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author Lauren Wagner
Megan Banchik
Tawny Tsang
Nana J. Okada
Rebecca Altshuler
Nicole McDonald
Susan Y. Bookheimer
Shafali S. Jeste
Shulamite Green
Mirella Dapretto
author_facet Lauren Wagner
Megan Banchik
Tawny Tsang
Nana J. Okada
Rebecca Altshuler
Nicole McDonald
Susan Y. Bookheimer
Shafali S. Jeste
Shulamite Green
Mirella Dapretto
author_sort Lauren Wagner
collection DOAJ
description Abstract Background Language difficulties are common in autism spectrum disorder (ASD), a neurodevelopmental condition characterized by impairments in social communication as well as restricted and repetitive behaviors. Amongst infant siblings of children with an ASD diagnosis – who are at higher likelihood for developing ASD – a high proportion also show difficulties and delays in language acquisition. Methods In this study, we used functional magnetic resonance imaging (fMRI) to examine differences in language processing in 9-month-old infants at high (HL) and typical (TL) familial likelihood for ASD. Infants were presented with native (English) and novel (Japanese) speech while sleeping naturally in the scanner. Whole-brain and a priori region-of-interest analyses were conducted to evaluate neural differences in language processing based on likelihood group and language condition. Results HL infants showed attenuated responses to speech in general, particularly in left temporal language areas, as well as a lack of neural discrimination between the native and novel languages compared to the TL group. Importantly, we also demonstrate that HL infants show distinctly atypical patterns of lateralization for speech processing, particularly during native speech processing, suggesting a failure to left-lateralize. Limitations: The sample size, particularly for the TL group, is relatively modest because of the challenges inherent to collecting auditory stimulus-evoked data from sleeping participants, as well as retention and follow-up difficulties posed by the COVID-19 pandemic. The groups were not matched on some demographic variables, but the present findings held even after accounting for these differences. Conclusions To our knowledge, this is the first fMRI study to directly measure autism-associated atypicalities in native language uptake during infancy. These findings provide a better understanding of the neurodevelopmental underpinnings of language delay in ASD, which is a prerequisite step for developing earlier and more effective interventions for autistic children and HL siblings who experience language impairments.
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spelling doaj-art-1d18851e142b431182e4eeeed7636b682025-02-09T12:39:59ZengBMCMolecular Autism2040-23922025-02-0116111910.1186/s13229-025-00640-wAtypical early neural responses to native and non-native language in infants at high likelihood for developing autismLauren Wagner0Megan Banchik1Tawny Tsang2Nana J. Okada3Rebecca Altshuler4Nicole McDonald5Susan Y. Bookheimer6Shafali S. Jeste7Shulamite Green8Mirella Dapretto9Neuroscience Interdepartmental Program, University of California Los AngelesDepartment of Psychiatry and Biobehavioral Sciences, University of California Los AngelesAhmanson-Lovelace Brain Mapping Center, University of California, Los AngelesDepartment of Epidemiology, Harvard Medical School, Harvard School of Public HealthUniversity of Colorado School of MedicineDepartment of Psychiatry and Biobehavioral Sciences, University of California Los AngelesDepartment of Psychiatry and Biobehavioral Sciences, University of California Los AngelesDivision of Neurology, Children’s Hospital Los AngelesDepartment of Psychiatry and Biobehavioral Sciences, University of California Los AngelesDepartment of Psychiatry and Biobehavioral Sciences, University of California Los AngelesAbstract Background Language difficulties are common in autism spectrum disorder (ASD), a neurodevelopmental condition characterized by impairments in social communication as well as restricted and repetitive behaviors. Amongst infant siblings of children with an ASD diagnosis – who are at higher likelihood for developing ASD – a high proportion also show difficulties and delays in language acquisition. Methods In this study, we used functional magnetic resonance imaging (fMRI) to examine differences in language processing in 9-month-old infants at high (HL) and typical (TL) familial likelihood for ASD. Infants were presented with native (English) and novel (Japanese) speech while sleeping naturally in the scanner. Whole-brain and a priori region-of-interest analyses were conducted to evaluate neural differences in language processing based on likelihood group and language condition. Results HL infants showed attenuated responses to speech in general, particularly in left temporal language areas, as well as a lack of neural discrimination between the native and novel languages compared to the TL group. Importantly, we also demonstrate that HL infants show distinctly atypical patterns of lateralization for speech processing, particularly during native speech processing, suggesting a failure to left-lateralize. Limitations: The sample size, particularly for the TL group, is relatively modest because of the challenges inherent to collecting auditory stimulus-evoked data from sleeping participants, as well as retention and follow-up difficulties posed by the COVID-19 pandemic. The groups were not matched on some demographic variables, but the present findings held even after accounting for these differences. Conclusions To our knowledge, this is the first fMRI study to directly measure autism-associated atypicalities in native language uptake during infancy. These findings provide a better understanding of the neurodevelopmental underpinnings of language delay in ASD, which is a prerequisite step for developing earlier and more effective interventions for autistic children and HL siblings who experience language impairments.https://doi.org/10.1186/s13229-025-00640-wInfantAutismfMRILanguageNative language
spellingShingle Lauren Wagner
Megan Banchik
Tawny Tsang
Nana J. Okada
Rebecca Altshuler
Nicole McDonald
Susan Y. Bookheimer
Shafali S. Jeste
Shulamite Green
Mirella Dapretto
Atypical early neural responses to native and non-native language in infants at high likelihood for developing autism
Molecular Autism
Infant
Autism
fMRI
Language
Native language
title Atypical early neural responses to native and non-native language in infants at high likelihood for developing autism
title_full Atypical early neural responses to native and non-native language in infants at high likelihood for developing autism
title_fullStr Atypical early neural responses to native and non-native language in infants at high likelihood for developing autism
title_full_unstemmed Atypical early neural responses to native and non-native language in infants at high likelihood for developing autism
title_short Atypical early neural responses to native and non-native language in infants at high likelihood for developing autism
title_sort atypical early neural responses to native and non native language in infants at high likelihood for developing autism
topic Infant
Autism
fMRI
Language
Native language
url https://doi.org/10.1186/s13229-025-00640-w
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