Abstract
Background
Emotional prosody provides acoustical cues that reflect a communication partner’s
emotional state and is crucial for successful social interactions. Many children with
autism have deficits in recognizing emotions from voices; however, the neural basis
for these impairments is unknown. We examined brain circuit features underlying emotional
prosody processing deficits and their relationship to clinical symptoms of autism.
Methods
We used an event-related functional magnetic resonance imaging task to measure neural
activity and connectivity during processing of sad and happy emotional prosody and
neutral speech in 22 children with autism and 21 matched control children (7–12 years
old). We employed functional connectivity analyses to test competing theoretical accounts
that attribute emotional prosody impairments to either sensory processing deficits
in auditory cortex or theory of mind deficits instantiated in the temporoparietal
junction (TPJ).
Results
Children with autism showed specific behavioral impairments for recognizing emotions
from voices. They also showed aberrant functional connectivity between voice-sensitive
auditory cortex and the bilateral TPJ during emotional prosody processing. Neural
activity in the bilateral TPJ during processing of both sad and happy emotional prosody
stimuli was associated with social communication impairments in children with autism.
In contrast, activity and decoding of emotional prosody in auditory cortex was comparable
between autism and control groups and did not predict social communication impairments.
Conclusions
Our findings support a social-cognitive deficit model of autism by identifying a role
for TPJ dysfunction during emotional prosody processing. Our study underscores the
importance of tuning in to vocal-emotional cues for building social connections in
children with autism.
Keywords
To read this article in full you will need to make a payment
Purchase one-time access:
Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online accessOne-time access price info
- For academic or personal research use, select 'Academic and Personal'
- For corporate R&D use, select 'Corporate R&D Professionals'
Subscribe:
Subscribe to Biological Psychiatry: Cognitive Neuroscience and NeuroimagingAlready a print subscriber? Claim online access
Already an online subscriber? Sign in
Register: Create an account
Institutional Access: Sign in to ScienceDirect
References
- Comment: The next frontier: Prosody research gets interpersonal.Emot Rev. 2021; 13: 51-56
- Social functions of emotions at four levels of analysis.Cogn Emot. 1999; 13: 505-521
- How emotions regulate social life: The Emotions as Social Information (EASI) model.Curr Dir Psychol Sci. 2009; 18: 184-188
- Acoustical correlates of affective prosody.J Voice. 2007; 21: 531-540
- Beyond the right hemisphere: Brain mechanisms mediating vocal emotional processing.Trends Cogn Sci. 2006; 10: 24-30
- Acoustic profiles in vocal emotion expression.J Pers Soc Psychol. 1996; 70: 614-636
- Maturation of vocal emotion recognition: Insights from the developmental and neuroimaging literature.Neurosci Biobehav Rev. 2018; 90: 221-230
- Diagnostic and Statistical Manual of Mental Disorders.5th ed. American Psychiatric Publishing, Arlington, VA2013
- Autistic disturbances of affective contact.Nervous Child. 1943; 2: 217-250
- Prosodic development in normal and autistic children.in: Schopler E. Mesibov G.B. Communication Problems in Autism. Springer, Boston1985: 95-125
- Prosody in autism spectrum disorders: A critical review.Int J Lang Commun Disord. 2003; 38: 325-350
- Speech and prosody characteristics of adolescents and adults with high-functioning autism and Asperger syndrome.J Speech Lang Hear Res. 2001; 44: 1097-1115
- Perception and production of prosody by speakers with autism spectrum disorders.J Autism Dev Disord. 2005; 35: 205-220
- Emotion perception in Asperger’s syndrome and high-functioning autism: The importance of diagnostic criteria and cue intensity.J Autism Dev Disord. 2007; 37: 1086-1095
- Reading the mind in the voice: A study with normal adults and adults with Asperger syndrome and high functioning autism.J Autism Dev Disord. 2002; 32: 189-194
- The ‘Reading the Mind in the Voice’ Test-Revised: A study of complex emotion recognition in adults with and without autism spectrum conditions.J Autism Dev Disord. 2007; 37: 1096-1106
- Decoding of emotion through facial expression, prosody and verbal content in children and adolescents with Asperger’s syndrome.J Autism Dev Disord. 2006; 36: 769-777
- Co-segregation of Social Cognition, Executive Function and Local Processing Style in Children with ASD, their Siblings and Normal Controls.J Autism Dev Disord. 2013; 43: 2764-2778
- Evidence for shared deficits in identifying emotions from faces and from voices in autism spectrum disorders and specific language impairment.Int J Lang Commun Disord. 2015; 50: 452-466
- Recognition of facial emotion and affective prosody in children with ASD (+ADHD) and their unaffected siblings.Eur Child Adolesc Psychiatry. 2014; 23: 257-271
- Basic and complex emotion recognition in children with autism: Cross-cultural findings.Mol Autism. 2016; 7: 52
- Prosody and its relationship to language in school-aged children with high-functioning autism.Int J Lang Commun Disord. 2007; 42: 682-702
- Receptive and expressive prosodic ability in children with high-functioning autism.J Speech Lang Hear Res. 2007; 50: 1015-1028
- Affective prosody perception and the relation to social competence in autistic and typically developing children.J Abnorm Child Psychol. 2020; 48: 965-975
- Sensory perception in autism.Nat Rev Neurosci. 2017; 18: 671-684
- Behavioral, perceptual, and neural alterations in sensory and multisensory function in autism spectrum disorder.Prog Neurobiol. 2015; 134: 140-160
- Emotional voices in context: A neurobiological model of multimodal affective information processing.Phys Life Rev. 2011; 8: 383-403
- Neural decoding of emotional prosody in voice-sensitive auditory cortex predicts social communication abilities in children [published online ahead of print Mar 16].Cerebral Cortex. 2022;
- Voice-selective areas in human auditory cortex.Nature. 2000; 403: 309-312
- Abnormal cortical voice processing in autism.Nat Neurosci. 2004; 7: 801-802
- Does the autistic child have a “theory of mind”?.Cognition. 1985; 21: 37-46
- Communicative competence and theory of mind in autism: A test of relevance theory.Cognition. 1993; 48: 101-119
- Does the chimpanzee have a theory of mind?.Behav Brain Sci. 1978; 1: 515-526
- People thinking about thinking people: The role of the temporo-parietal junction in “theory of mind.”.Neuroimage. 2003; 19: 1835-1842
- It’s the thought that counts: Specific brain regions for one component of theory of mind.Psychol Sci. 2006; 17: 692-699
- Fractionating theory of mind: A meta-analysis of functional brain imaging studies.Neurosci Biobehav Rev. 2014; 42: 9-34
- Left temporoparietal junction is necessary for representing someone else’s belief.Nat Neurosci. 2004; 7: 499-500
- Connectivity-based subdivisions of the human right “temporoparietal junction area”: Evidence for different areas participating in different cortical networks.Cerebral Cortex. 2012; 22: 1894-1903
- The social brain: Neural basis of social knowledge.Annu Rev Psychol. 2009; 60: 693-716
- Specialization of right temporo-parietal junction for mentalizing and its relation to social impairments in autism.Neuroimage. 2011; 56: 1832-1838
- Neural bases of theory of mind in children with autism spectrum disorders and children with conduct problems and callous-unemotional traits.Dev Sci. 2014; 17: 786-796
- Perception of dynamic changes in facial affect and identity in autism.Soc Cogn Affect Neurosci. 2007; 2: 140-149
- Research review: Constraining heterogeneity: The social brain and its development in autism spectrum disorder.J Child Psychol Psychiatry. 2011; 52: 631-644
- A pivotal response treatment package for children with autism spectrum disorder: An RCT.Pediatrics. 2019; 144e20190178
- Pivotal Response Treatments For Autism: Communication, Social, and Academic Development.Paul H Brookes Publishing, Baltimore2006
- Editorial: The importance of early intervention.J Autism Dev Disord. 2014; 44: 2979-2980
- Brain correlates of emotional prosodic change detection in autism spectrum disorder.Neuroimage Clin. 2020; 28102512
- Atypical perception of affective prosody in autism spectrum disorder.Neuroimage Clin. 2014; 6: 370-378
- Emotional prosody processing in autism spectrum disorder.Soc Cogn Affect Neurosci. 2017; 12: 224-239
- The neural underpinnings of prosody in autism.Child Neuropsychol. 2012; 18: 600-617
- Combining information from multiple sources in the diagnosis of autism spectrum disorders.J Am Acad Child Adolesc Psychiatry. 2006; 45: 1094-1103
- The Autism Diagnostic Observation Schedule–Generic: A standard measure of social and communication deficits associated with the spectrum of autism.J Autism Dev Disord. 2000; 30: 205-223
- Autism Diagnostic Interview–Revised: A revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders.J Autism Dev Disord. 1994; 24: 659-685
- Intrinsic functional architecture of the human speech processing network.Cortex. 2020; 129: 41-56
- A generalized form of context-dependent psychophysiological interactions (gPPI): A comparison to standard approaches.Neuroimage. 2012; 61: 1277-1286
- Perception of emotion: Measuring decoding accuracy of adult prosodic cues varying in intensity.J Nonverbal Behav. 1998; 22: 89-107
- Individual differences in the nonverbal communication of affect: The diagnostic analysis of nonverbal accuracy scale.J Nonverbal Behav. 1994; 18: 9-35
- A primer on pattern-based approaches to fMRI: Principles, pitfalls, and perspectives.Neuron. 2015; 87: 257-270
- Decoding of emotional information in voice-sensitive cortices.Curr Biol. 2009; 19: 1028-1033
- A nexus model of the temporal-parietal junction.Trends Cogn Sci. 2013; 17: 328-336
- Differential role of temporoparietal junction and medial prefrontal cortex in causal inference in autism: An independent component analysis.Neurosci Lett. 2014; 568: 50-55
- Functional brain networks and white matter underlying theory-of-mind in autism.Soc Cogn Affect Neurosci. 2014; 9: 98-105
- Thinking the voice: Neural correlates of voice perception.Trends Cogn Sci. 2004; 8: 129-135
- Neural circuits underlying mother’s voice perception predict social communication abilities in children.Proc Natl Acad Sci U S A. 2016; 113: 6295-6300
- Auditory cortical micro-networks show differential connectivity during voice and speech processing in humans.Commun Biol. 2021; 4: 801
- Cerebral pathways in processing of affective prosody: A dynamic causal modeling study.Neuroimage. 2006; 30: 580-587
- Impaired voice processing in reward and salience circuits predicts social communication in children with autism.Elife. 2019; 8e39906
- Underconnectivity between voice-selective cortex and reward circuitry in children with autism.Proc Natl Acad Sci U S A. 2013; 110: 12060-12065
- Phase-IIa randomized, double-blind, sham-controlled, parallel group trial on anodal transcranial direct current stimulation (tDCS) over the left and right tempo-parietal junction in autism spectrum disorder—StimAT: Study protocol for a clinical trial.Trials. 2021; 22: 248
- Quantification of head motion in children during various fMRI language tasks.Hum Brain Mapp. 2009; 30: 1481-1489
- fMRI replicability depends upon sufficient individual-level data.Commun Biol. 2019; 2: 1-4
- Puzzlingly high correlations in fMRI studies of emotion, personality, and social cognition.Perspect Psychol Sci. 2009; 4: 274-290
- Social Responsiveness Scale.Second Edition (SRS-2). Western Psychological Services, Torrance, CA2012
Article info
Publication history
Published online: October 12, 2022
Accepted:
September 30,
2022
Received in revised form:
August 25,
2022
Received:
April 13,
2022
Publication stage
In Press Journal Pre-ProofIdentification
Copyright
© 2022 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.
