Impaired voice processing in reward and salience circuits predicts social communication in children with autism
Open accessAbstract
Engaging with vocal sounds is critical for children’s social-emotional learning, and children with autism spectrum disorder (ASD) often ‘tune out’ voices in their environment. Little is known regarding the neurobiological basis of voice processing and its link to social impairments in ASD. Here, we perform the first comprehensive brain network analysis of voice processing in children with ASD. We examined neural responses elicited by unfamiliar voices and mother’s voice, a biologically salient voice for social learning, and identified a striking relationship between social communication abilities in children with ASD and activation in key structures of reward and salience processing regions. Functional connectivity between voice-selective and reward regions during voice processing predicted social communication in children with ASD and distinguished them from typically developing children. Results support the Social Motivation Theory of ASD by showing reward system deficits associated with the processing of a critical social stimulus, mother’s voice, in children with ASD. Editorial note: This article has been through an editorial process in which the authors decide how to respond to the issues raised during peer review. The Reviewing Editor's assessment is that minor issues remain unresolved (see decision letter).
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Brain imaging studies in individuals with ASD have found auditory discrimination deficits.
“Brain imaging studies in individuals with ASD have found auditory discrimination deficits (Matsuzaki et al. 2019a; Abrams et al. 2019), as well as increased neural responsiveness upon repeated stimuli, with larger fMRI response in the auditory cortex that seems specific to temporal patterns of stimulation (Millin et al. 2018).”
From Autism Spectrum Disorder and auditory sensory alterations: a systematic review on the integrity of cognitive and neuronal functions related to auditory processing (2023) · cites this paper as Abrams et al. 2019
The Results section on unfamiliar voices reports weaker auditory-association-cortex responses in children with ASD for unfamiliar voices compared with environmental sounds, supporting altered neural differentiation of those sounds. The paper does not establish a general auditory discrimination deficit: its imaging findings concern voice processing, and Figure 1 reports that most children with ASD identified their mother’s voice accurately. The indexed copy provides no page numbers for these passages. (LLM, conf=0.82)
Experimental — accuracy not yet measuredDeficits in auditory discrimination have been found in MEG and brain imaging studies in ASD.
“Deficits in auditory discrimination have also been found both in MEG and brain imaging studies (Ganesan et al. 2016; Claesdotter-Knutsson et al. 2019; Abrams et al. 2019).”
From Autism Spectrum Disorder and auditory sensory alterations: a systematic review on the integrity of cognitive and neuronal functions related to auditory processing (2023) · cites this paper as Abrams et al. 2019
Children with ASD show reduced activity in right-hemisphere planum polare for unfamiliar voices, reduced activity in a broad extent of fusiform gyrus bilaterally, and less activity in the right-hemisphere posterior hippocampus.
“Differences in response to sound familiarity have also been reported in children with ASD, with reduced activity in right-hemisphere planum polare for unfamiliar voices, reduced activity in a broad extent of fusiform gyrus bilaterally, and less activity in the right-hemisphere posterior hippocampus (Abrams et al. 2019).”
From Autism Spectrum Disorder and auditory sensory alterations: a systematic review on the integrity of cognitive and neuronal functions related to auditory processing (2023) · cites this paper as Abrams et al. 2019
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Gonçalves, A. M., & Monteiro, P. (2023) · Journal of Neural Transmission · doi:10.1007/s00702-023-02595-9 · Cited by 88 · see citing works
Altered processing of communication signals in the subcortical auditory sensory pathway in autism
Schelinski, S., Tabas, A., & von Kriegstein, K. (2022) · Human Brain Mapping · doi:10.1002/hbm.25766 · Cited by 24 · see citing works
- Authors
- Abrams, D. A., Padmanabhan, A., Chen, T., Odriozola, P., Baker, A. E., Kochalka, J., Phillips, J. M., & Menon, V.
- Affiliations
- Stanford Medicine (US)
- Corresponding author
- Abrams, Daniel Arthur
- Menon, Vinod
- ORCID
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2019-02-26
- Volume
- 8
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC6391069
- OpenAlex
- W2917434510
- Cited by
- 46
- References
- 22
- Citations by year
- 2026: 7 · 2025: 8 · 2024: 8 · 2023: 3 · 2022: 11 · 2021: 3 · 2020: 5 · 2019: 1
- FWCI
- 2.91
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- Funders
- National Institute of Mental Health (MH102428, MH084164)
- Brain and Behavior Research Foundation (NARSAD Young Investigator Grant)
- Stanford School of Medicine, Stanford Medicine, Stanford University (UL1TR001085)
- National Center for Advancing Translational Sciences (UL1TR001085)
- National Institute on Deafness and Other Communication Disorders (DC011095)
- Singer Family Foundation
- Simons Foundation (308939)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- autism spectrum disorder, voice processing, social communication, reward systems, salience processing, maternal voice, functional connectivity, brain networks, social motivation theory, children
- MeSH terms
- Auditory Perception, Autistic Disorder, Child, Female, Humans, Interpersonal Relations, Learning, Magnetic Resonance Imaging, Male, Nerve Net, Reward, Speech Perception
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