Intact brain processing of musical emotions in autism spectrum disorder, but more cognitive load and arousal in happy vs. sad music

Music is a potent source for eliciting emotions, but not everybody experience emotions in the same way. Individuals with autism spectrum disorder (ASD) show difficulties with social and emotional cognition. Impairments in emotion recognition are widely studied in ASD, and have been associated with atypical brain activation in response to emotional expressions in faces and speech. Whether these impairments and atypical brain responses generalize to other domains, such as emotional processing of music, is less clear. Using functional magnetic resonance imaging, we investigated neural correlates of emotion recognition in music in high-functioning adults with ASD and neurotypical adults. Both groups engaged similar neural networks during processing of emotional music, and individuals with ASD rated emotional music comparable to the group of neurotypical individuals. However, in the ASD group, increased activity in response to happy compared to sad music was observed in dorsolateral prefrontal regions and in the rolandic operculum/insula, and we propose that this reflects increased cognitive processing and physiological arousal in response to emotional musical stimuli in this group.

[1]  A. Gabrielsson.  Emotion perceived and emotion felt: Same or different? , 2001 .

[2]  B. Dubois,et al.  Functions of the left superior frontal gyrus in humans: a lesion study. , 2006, Brain : a journal of neurology.

[3]  B. Leventhal,et al.  The Autism Diagnostic Observation Schedule—Generic: A Standard Measure of Social and Communication Deficits Associated with the Spectrum of Autism , 2000, Journal of autism and developmental disorders.

[4]  D. Koshland.  Frontiers in neuroscience. , 1988, Science.

[5]  José Donoso,et al.  Of " Understanding , 2015 .

[6]  E. Hill,et al.  `Hath charms to soothe . . .' , 2009, Autism : the international journal of research and practice.

[7]  Vladimir J. Konečni,et al.  Does music induce emotion? A theoretical and methodological analysis. , 2008 .

[8]  J. Ashburner,et al.  Nonlinear spatial normalization using basis functions , 1999, Human brain mapping.

[9]  B. Hermelin,et al.  A pseudo-savant: A case of exceptional musical splinter skills , 1999 .

[10]  D. Tulsky,et al.  WAIS-III WMS-III Technical manual , 1977 .

[11]  Michael Fitzgerald,et al.  THE OVERLAP BETWEEN ALEXITHYMIA AND ASPERGER’S SYNDROME , 2006, The American journal of psychiatry.

[12]  P. Laukka,et al.  Expression, Perception, and Induction of Musical Emotions: A Review and a Questionnaire Study of Everyday Listening , 2004 .

[13]  Laurette Dubé,et al.  The content and structure of laypeople's concept of pleasure , 2003, Cognition & emotion.

[14]  M. Dapretto,et al.  Reading affect in the face and voice: neural correlates of interpreting communicative intent in children and adolescents with autism spectrum disorders. , 2007, Archives of general psychiatry.

[15]  R. Zatorre,et al.  Intensely pleasurable responses to music correlate with activity in brain regions implicated in reward and emotion , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[16]  R. Hobson.  The autistic child's appraisal of expressions of emotion. , 1986, Journal of child psychology and psychiatry, and allied disciplines.

[17]  Yan Bao,et al.  Personality traits modulate neural responses to emotions expressed in music , 2013, Brain Research.

[18]  I. Peretz,et al.  Enhanced Pitch Sensitivity in Individuals with Autism: A Signal Detection Analysis , 2003, Journal of Cognitive Neuroscience.

[19]  Inge-Marie Eigsti,et al.  The neural underpinnings of prosody in autism , 2012, Child neuropsychology : a journal on normal and abnormal development in childhood and adolescence.

[20]  D. Berlyne,et al.  Aesthetics and Psychobiology , 1975 .

[21]  C. Gillberg,et al.  AUTISM AND MEDICAL DISORDERS: A REVIEW OF THE LITERATURE , 1996, Developmental medicine and child neurology.

[22]  H. Critchley,et al.  The functional neuroanatomy of social behaviour: changes in cerebral blood flow when people with autistic disorder process facial expressions. , 2000, Brain : a journal of neurology.

[23]  P. Gasquoine,et al.  Contributions of the Insula to Cognition and Emotion , 2014, Neuropsychology Review.

[24]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[25]  E. Bullmore,et al.  The amygdala theory of autism , 2000, Neuroscience & Biobehavioral Reviews.

[26]  P. Heaton,et al.  Pitch memory, labelling and disembedding in autism. , 2003, Journal of child psychology and psychiatry, and allied disciplines.

[27]  Eric Courchesne,et al.  A failure of left temporal cortex to specialize for language is an early emerging and fundamental property of autism. , 2012, Brain : a journal of neurology.

[28]  Satrajit S. Ghosh,et al.  Optimized Design and Analysis of Sparse-Sampling fMRI Experiments , 2013, Front. Neurosci..

[29]  P. Heaton.  Interval and Contour Processing in Autism , 2005, Journal of autism and developmental disorders.

[30]  A. Friederici,et al.  Investigating emotion with music: An fMRI study , 2006, Human brain mapping.

[31]  Elisabeth Hill,et al.  The Effects of Autism and Alexithymia on Physiological and Verbal Responsiveness to Music , 2013, Journal of autism and developmental disorders.

[32]  Thomas Fritz,et al.  Investigating brain response to music: A comparison of different fMRI acquisition schemes , 2011, NeuroImage.

[33]  Andreas Højlund Nielsen,et al.  The Musical Ear Test, a new reliable test for measuring musical competence , 2010 .

[34]  A L Alexander,et al.  Decreased Left Posterior Insular Activity during Auditory Language in Autism , 2010, American Journal of Neuroradiology.

[35]  R. Peter Hobson.  Autism and Emotion , 2005 .

[36]  Scott T. Grafton,et al.  Swinging in the brain: shared neural substrates for behaviors related to sequencing and music , 2003, Nature Neuroscience.

[37]  S. Koelsch.  Towards a neural basis of music-evoked emotions , 2010, Trends in Cognitive Sciences.

[38]  E. Redcay.  The superior temporal sulcus performs a common function for social and speech perception: Implications for the emergence of autism , 2008, Neuroscience & Biobehavioral Reviews.

[39]  T. Egner,et al.  Emotional processing in anterior cingulate and medial prefrontal cortex , 2011, Trends in Cognitive Sciences.

[40]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[41]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

[42]  G. Schlaug,et al.  Amygdala activity can be modulated by unexpected chord functions during music listening , 2008, Neuroreport.

[43]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[44]  R. Adolphs.  Neural systems for recognizing emotion , 2002, Current Opinion in Neurobiology.

[45]  Eckart Altenmüller,et al.  How Does Music Arouse “Chills”? , 2005, Annals of the New York Academy of Sciences.

[46]  S. Gosling,et al.  PERSONALITY PROCESSES AND INDIVIDUAL DIFFERENCES The Do Re Mi’s of Everyday Life: The Structure and Personality Correlates of Music Preferences , 2003 .

[47]  Robert J. Zatorre,et al.  Familiarity mediates the relationship between emotional arousal and pleasure during music listening , 2013, Front. Hum. Neurosci..

[48]  Daniel J. Levitin,et al.  This is your brain on music : the science of a human obsession , 2006 .

[49]  J. Boucher,et al.  Unfamiliar face recognition in relatively able autistic children. , 1992, Journal of child psychology and psychiatry, and allied disciplines.

[50]  Karl J. Friston,et al.  Detecting Activations in PET and fMRI: Levels of Inference and Power , 1996, NeuroImage.

[51]  G. Celani,et al.  The Understanding of the Emotional Meaning of Facial Expressions in People with Autism , 1999, Journal of autism and developmental disorders.

[52]  T. Griffiths,et al.  “When the feeling’s gone”: a selective loss of musical emotion , 2004, Journal of Neurology, Neurosurgery & Psychiatry.

[53]  D. Huron,et al.  Is Music an Evolutionary Adaptation? , 2001, Annals of the New York Academy of Sciences.

[54]  K. Overy.  Making music in a group: synchronization and shared experience , 2012, Annals of the New York Academy of Sciences.

[55]  H. Critchley.  Neural mechanisms of autonomic, affective, and cognitive integration , 2005, The Journal of comparative neurology.

[56]  D. Västfjäll,et al.  Emotional responses to music: the need to consider underlying mechanisms. , 2008, The Behavioral and brain sciences.

[57]  Alexander Hammers,et al.  Volumes, spatial extents and a probabilistic atlas of the human basal ganglia and thalamus , 2007, NeuroImage.

[58]  Nathalie Boddaert,et al.  Autism, the superior temporal sulcus and social perception , 2006, Trends in Neurosciences.

[59]  Giacomo Vivanti,et al.  Are emotion impairments unique to, universal, or specific in autism spectrum disorder? A comprehensive review , 2013, Cognition & emotion.

[60]  Paola Venuti,et al.  Functional and dysfunctional brain circuits underlying emotional processing of music in autism spectrum disorders. , 2011, Cerebral cortex.

[61]  A. Young,et al.  Deficits in facial, body movement and vocal emotional processing in autism spectrum disorders , 2010, Psychological Medicine.

[62]  R. Zatorre,et al.  The Rewarding Aspects of Music Listening Are Related to Degree of Emotional Arousal , 2009, PloS one.

[63]  B. Hubert,et al.  Brief Report: Recognition of Emotional and Non-emotional Biological Motion in Individuals with Autistic Spectrum Disorders , 2007 .

[64]  R. Zatorre,et al.  Interactions Between the Nucleus Accumbens and Auditory Cortices Predict Music Reward Value , 2013, Science.

[65]  W. Fitch.  The Evolution of Music in Comparative Perspective , 2005, Annals of the New York Academy of Sciences.

[66]  S. Baron-Cohen,et al.  The ‘Reading the Mind in the Voice’ Test-Revised: A Study of Complex Emotion Recognition in Adults with and Without Autism Spectrum Conditions , 2007, Journal of autism and developmental disorders.

[67]  C. Stevens,et al.  Sweet Anticipation: Music and the Psychology of Expectation, by David Huron . Cambridge, Massachusetts: MIT Press, 2006 , 2007 .

[68]  M. Dapretto,et al.  Neural basis of irony comprehension in children with autism: the role of prosody and context. , 2006, Brain : a journal of neurology.

[69]  E. Hill,et al.  Measuring the effects of alexithymia on perception of emotional vocalizations in autistic spectrum disorder and typical development , 2012, Psychological Medicine.

[70]  Daniel J. Levitin,et al.  The rewards of music listening: Response and physiological connectivity of the mesolimbic system , 2005, NeuroImage.

[71]  C. Mazefsky,et al.  Emotion Perception in Asperger’s Syndrome and High-functioning Autism: The Importance of Diagnostic Criteria and Cue Intensity , 2007, Journal of autism and developmental disorders.

[72]  R. Schultz,et al.  Reward system dysfunction in autism spectrum disorders. , 2013, Social cognitive and affective neuroscience.

[73]  R. Zatorre,et al.  Anatomically distinct dopamine release during anticipation and experience of peak emotion to music , 2011, Nature Neuroscience.

[74]  Andrea Bergmann,et al.  Statistical Parametric Mapping The Analysis Of Functional Brain Images , 2016 .

[75]  L. Kanner.  Autistic disturbances of affective contact. , 1968, Acta paedopsychiatrica.

[76]  G Bird,et al.  Mixed emotions: the contribution of alexithymia to the emotional symptoms of autism , 2013, Translational Psychiatry.

[77]  F. Happé,et al.  Do social and cognitive deficits curtail musical understanding? Evidence from autism and Down syndrome , 2008 .

[78]  J. Burack,et al.  Pitch discrimination and melodic memory in children with autism spectrum disorders , 2014, Autism : the international journal of research and practice.

[79]  E. Hill,et al.  The Subjective Experience of Music in Autism Spectrum Disorder , 2009, Annals of the New York Academy of Sciences.

[80]  Carter Wendelken,et al.  A functional and structural study of emotion and face processing in children with autism , 2009, Psychiatry Research: Neuroimaging.

[81]  Isabelle Peretz,et al.  Towards a Neurobiology of Musical Emotions , 1993 .

[82]  L. Rosén,et al.  Decoding of Emotion through Facial Expression, Prosody and Verbal Content in Children and Adolescents with Asperger’s Syndrome , 2006, Journal of autism and developmental disorders.

[83]  G. Baird,et al.  A multimodal approach to emotion recognition ability in autism spectrum disorders. , 2011, Journal of child psychology and psychiatry, and allied disciplines.

[84]  Michael J. Martinez,et al.  Passive music listening spontaneously engages limbic and paralimbic systems , 2004, Neuroreport.

[85]  A. Craig.  How do you feel? Interoception: the sense of the physiological condition of the body , 2002, Nature Reviews Neuroscience.

[86]  V. Menon,et al.  Saliency, switching, attention and control: a network model of insula function , 2010, Brain Structure and Function.

[87]  M. Tervaniemi,et al.  A Functional MRI Study of Happy and Sad Emotions in Music with and without Lyrics , 2011, Front. Psychology.

[88]  Eve-Marie Quintin,et al.  Emotion Perception in Music in High-Functioning Adolescents With Autism Spectrum Disorders , 2011, Journal of autism and developmental disorders.

[89]  Alan C. Evans,et al.  Emotional responses to pleasant and unpleasant music correlate with activity in paralimbic brain regions , 1999, Nature Neuroscience.

[90]  Laurent Mottron,et al.  Impaired Face Processing in Autism: Fact or Artifact? , 2006, Journal of autism and developmental disorders.

[91]  Stefan Koelsch,et al.  The roles of superficial amygdala and auditory cortex in music-evoked fear and joy , 2013, NeuroImage.

[92]  M. Zentner,et al.  Mapping Aesthetic Musical Emotions in the Brain , 2011, Cerebral cortex.

[93]  E. Bullmore,et al.  Differential activation of the amygdala and the ‘social brain’ during fearful face-processing in Asperger Syndrome , 2007, Neuropsychologia.

[94]  M. Kringelbach,et al.  Ever-changing cycles of musical pleasure: The role of dopamine and anticipation. , 2012 .

[95]  Pascal Belin,et al.  Abnormal cortical voice processing in autism , 2004, Nature Neuroscience.

[96]  Steven C. R. Williams,et al.  A functional MRI study of happy and sad affective states induced by classical music , 2007, Human brain mapping.

[97]  Garry Tamlyn,et al.  Music , 1993 .

[98]  Nouchine Hadjikhani,et al.  Body expressions of emotion do not trigger fear contagion in autism spectrum disorder. , 2009, Social cognitive and affective neuroscience.

[99]  Janet B W Williams,et al.  Diagnostic and Statistical Manual of Mental Disorders , 2013 .

[100]  M. Bauman,et al.  The Functional Neuroanatomy of Social Behavior , 2001 .

[101]  F. Volkmar,et al.  Abnormal ventral temporal cortical activity during face discrimination among individuals with autism and Asperger syndrome. , 2000, Archives of general psychiatry.

[102]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.

[103]  Craniofacial Identification: Unfamiliar face recognition , 2012 .

[104]  E. Brattico,et al.  Music and Emotions in the Brain: Familiarity Matters , 2011, PloS one.

[105]  Adrian C. North,et al.  Subjective complexity, familiarity, and liking for popular music. , 1995 .