Empathy and emotion recognition in people with autism, first-degree relatives, and controls

Empathy is the lens through which we view others’ emotion expressions, and respond to them. In this study, empathy and facial emotion recognition were investigated in adults with autism spectrum conditions (ASC; N=314), parents of a child with ASC (N=297) and IQ-matched controls (N=184). Participants completed a self-report measure of empathy (the Empathy Quotient [EQ]) and a modified version of the Karolinska Directed Emotional Faces Task (KDEF) using an online test interface. Results showed that mean scores on the EQ were significantly lower in fathers (p < 0.05) but not mothers (p > 0.05) of children with ASC compared to controls, whilst both males and females with ASC obtained significantly lower EQ scores (p < 0.001) than controls. On the KDEF, statistical analyses revealed poorer overall performance by adults with ASC (p < 0.001) compared to the control group. When the 6 distinct basic emotions were analysed separately, the ASC group showed impaired performance across five out of six expressions (happy, sad, angry, afraid and disgusted). Parents of a child with ASC were not significantly worse than controls at recognising any of the basic emotions, after controlling for age and non-verbal IQ (all p > 0.05). Finally, results indicated significant differences between males and females with ASC for emotion recognition performance (p < 0.05) but not for self-reported empathy (p > 0.05). These findings suggest that self-reported empathy deficits in fathers of autistic probands are part of the ‘broader autism phenotype’. This study also reports new findings of sex differences amongst people with ASC in emotion recognition, as well as replicating previous work demonstrating empathy difficulties in adults with ASC. The use of empathy measures as quantitative endophenotypes for ASC is discussed.

[1]  P. Rezaie,et al.  Researching the Autism Spectrum: Contemporary Perspectives , 2013 .

[2]  J. Buxbaum,et al.  Molecular Autism: accelerating and integrating research into neurodevelopmental conditions , 2010, Molecular autism.

[3]  S. Baron-Cohen,et al.  neurocognitive developmental mechanisms and individual differences. , 2006 .

[4]  Michael V. Lombardo,et al.  A Behavioral Comparison of Male and Female Adults with High Functioning Autism Spectrum Conditions , 2011, PloS one.

[5]  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.

[6]  John E. Cooper,et al.  Diagnostic and Statistical Manual of Mental Disorders (4th edn, text revision) (DSM-IV-TR) , 2001 .

[7]  M. D. Rutherford,et al.  Scan Path Differences and Similarities During Emotion Perception in those With and Without Autism Spectrum Disorders , 2008, Journal of autism and developmental disorders.

[8]  A. Bailey,et al.  Face processing abilities in relatives of individuals with ASD , 2010, Autism research : official journal of the International Society for Autism Research.

[9]  S. Gosling,et al.  Should we trust web-based studies? A comparative analysis of six preconceptions about internet questionnaires. , 2004, The American psychologist.

[10]  S. Baron-Cohen,et al.  Psychometric analysis of the Empathy Quotient (EQ) , 2011 .

[11]  S. Baron-Cohen,et al.  The Autism-Spectrum Quotient (AQ): Evidence from Asperger Syndrome/High-Functioning Autism, Malesand Females, Scientists and Mathematicians , 2001, Journal of autism and developmental disorders.

[12]  John M Opitz,et al.  American journal of medical genetics. Part B, Neuropsychiatric genetics , 2003 .

[13]  S. Hutton,et al.  Age differences in emotion recognition skills and the visual scanning of emotion faces. , 2007, The journals of gerontology. Series B, Psychological sciences and social sciences.

[14]  S. Baron-Cohen The extreme male brain theory of autism , 2002, Trends in Cognitive Sciences.

[15]  C. Darwin The Expression of the Emotions in Man and Animals , .

[16]  A. Leslie,et al.  Autistic children's understanding of seeing, knowing and believing , 1988 .

[17]  S. Baron-Cohen,et al.  Does the autistic child have a “theory of mind” ? , 1985, Cognition.

[18]  S. Baron-Cohen,et al.  Measuring empathy: reliability and validity of the Empathy Quotient , 2004, Psychological Medicine.

[19]  P Bolton,et al.  A case-control family history study of autism. , 1994, Journal of child psychology and psychiatry, and allied disciplines.

[20]  J. Piven,et al.  Neuropsychological profile of autism and the broad autism phenotype. , 2009, Archives of general psychiatry.

[21]  Jean Decety,et al.  The empathic brain and its dysfunction in psychiatric populations: implications for intervention across different clinical conditions , 2007, BioPsychoSocial medicine.

[22]  J. Winn,et al.  Brain , 1878, The Lancet.

[23]  H. Faras,et al.  Autism spectrum disorders , 2010, Annals of Saudi medicine.

[24]  U. Frith,et al.  Exploring the cognitive phenotype of autism: weak "central coherence" in parents and siblings of children with autism: I. Experimental tests. , 2001, Journal of child psychology and psychiatry, and allied disciplines.

[25]  Simon Baron-Cohen,et al.  Empathizing: neurocognitive developmental mechanisms and individual differences. , 2006, Progress in brain research.

[26]  Carmel Mevorach,et al.  Opposite biases in salience-based selection for the left and right posterior parietal cortex , 2006, Nature Neuroscience.

[27]  C. Lajonchere,et al.  Autistic social impairment in the siblings of children with pervasive developmental disorders. , 2006, The American journal of psychiatry.

[28]  David I. Perrett,et al.  The Emotion Recognition Task: A Paradigm to Measure the Perception of Facial Emotional Expressions at Different Intensities , 2007, Perceptual and motor skills.

[29]  J. Piven,et al.  Visual Scanning of Faces in Autism , 2002, Journal of autism and developmental disorders.

[30]  Simon Baron-Cohen,et al.  Empathizing with basic emotions: Common and discrete neural substrates , 2006, Social neuroscience.

[31]  K. Loveland,et al.  Emotion recognition in autism: Verbal and nonverbal information , 1997, Development and Psychopathology.

[32]  T. Field,et al.  Discrimination and imitation of facial expression by neonates. , 1982, Science.

[33]  S. Baron-Cohen Autism and symbolic play , 1987 .

[34]  A. Walker-Andrews Infants' perception of expressive behaviors: differentiation of multimodal information. , 1997, Psychological bulletin.

[35]  Simon Baron-Cohen,et al.  Imagining Real and Unreal Things: Evidence of a Dissociation in Autism , 1996, Journal of Cognitive Neuroscience.

[36]  S. Baron-Cohen,et al.  The Empathy Quotient: An Investigation of Adults with Asperger Syndrome or High Functioning Autism, and Normal Sex Differences , 2004, Journal of autism and developmental disorders.

[37]  I. Gottesman,et al.  The endophenotype concept in psychiatry: etymology and strategic intentions. , 2003, The American journal of psychiatry.

[38]  N. Minshew,et al.  The new neurobiology of autism: cortex, connectivity, and neuronal organization. , 2007, Archives of neurology.

[39]  S. Baron-Cohen,et al.  The Cambridge Mindreading (CAM) Face-Voice Battery: Testing Complex Emotion Recognition in Adults with and without Asperger Syndrome , 2006, Journal of autism and developmental disorders.

[40]  Meike Bartels,et al.  Twins and the study of rater (dis)agreement. , 2007, Psychological methods.

[41]  T. Walden,et al.  The development of social referencing. , 1988, Child development.

[42]  A. Leslie Pretense and representation: The origins of "theory of mind." , 1987 .

[43]  R. Holt,et al.  Links between genetics and pathophysiology in the autism spectrum disorders , 2011, EMBO molecular medicine.

[44]  Ilona Roth,et al.  Autistic Traits Below the Clinical Threshold: Re-examining the Broader Autism Phenotype in the 21st Century , 2011, Neuropsychology Review.

[45]  J. Piven,et al.  Abnormal Processing of Social Information from Faces in Autism , 2001, Journal of Cognitive Neuroscience.

[46]  Livia Colle,et al.  Impaired recognition of negative basic emotions in autism: A test of the amygdala theory , 2006, Social neuroscience.

[47]  P. Pasqualetti,et al.  Recognition of schematic facial displays of emotion in parents of children with autism , 2006, Autism : the international journal of research and practice.

[48]  A. Leslie,et al.  Exploration of the autistic child's theory of mind: knowledge, belief, and communication. , 1989, Child development.

[49]  S. Baron-Cohen Autism: The Empathizing–Systemizing (E‐S) Theory , 2009, Annals of the New York Academy of Sciences.

[50]  S. Bölte,et al.  Sex differences in cognitive domains and their clinical correlates in higher-functioning autism spectrum disorders , 2011, Autism : the international journal of research and practice.

[51]  S. Baron-Cohen,et al.  Defining the broader, medium and narrow autism phenotype among parents using the Autism Spectrum Quotient (AQ) , 2010, Molecular autism.

[52]  S. Baron-Cohen,et al.  Visual attention in autism families: 'unaffected' sibs share atypical frontal activation. , 2010, Journal of child psychology and psychiatry, and allied disciplines.

[53]  Alex Martin,et al.  Facial Emotion Recognition in Autism Spectrum Disorders: A Review of Behavioral and Neuroimaging Studies , 2010, Neuropsychology Review.

[54]  M. Rutter,et al.  Understanding intention in normal development and in autism , 1998 .

[55]  Steven Muncer,et al.  Psychometric analysis of the empathy quotient (EQ) scale. , 2006 .

[56]  A. Mayes,et al.  Convergent neuroanatomical and behavioural evidence of an amygdala hypothesis of autism , 2000, Neuroreport.

[57]  Tom Manly,et al.  Facial expression recognition across the adult life span , 2003, Neuropsychologia.

[58]  L. Leyman,et al.  The Karolinska Directed Emotional Faces: A validation study , 2008 .

[59]  D. Crewther,et al.  Magnocellular visual evoked potential delay with high autism spectrum quotient yields a neural mechanism for altered perception. , 2010, Brain : a journal of neurology.

[60]  P. Ekman,et al.  Constants across cultures in the face and emotion. , 1971, Journal of personality and social psychology.

[61]  M. R. Herbert,et al.  Reduced functional connectivity in visual evoked potentials in children with autism spectrum disorder , 2010, Clinical Neurophysiology.

[62]  D. Geschwind,et al.  Advances in autism genetics: on the threshold of a new neurobiology , 2008, Nature Reviews Genetics.

[63]  M. Sigman,et al.  Self-competence and emotional understanding in high-functioning children with autism , 1995, Development and Psychopathology.

[64]  S. Baron-Cohen,et al.  Parents of Children with Asperger Syndrome: What is the Cognitive Phenotype? , 1997, Journal of Cognitive Neuroscience.

[65]  E. Pellicano Psychological models of autism: An overview , 2011 .

[66]  S. Baron-Cohen,et al.  Genes related to sex steroids, neural growth, and social–emotional behavior are associated with autistic traits, empathy, and Asperger syndrome , 2009, Autism research : official journal of the International Society for Autism Research.

[67]  L. Brosgole,et al.  Visual and auditory affect recognition in singly diagnosed mentally retarded patients, mentally retarded patients with autism and normal young children. , 1988, The International journal of neuroscience.

[68]  E T Bullmore,et al.  A novel functional brain imaging endophenotype of autism: the neural response to facial expression of emotion , 2011, Translational Psychiatry.

[69]  S. Bölte,et al.  The recognition of facial affect in autistic and schizophrenic subjects and their first-degree relatives , 2003, Psychological Medicine.

[70]  U. Frith,et al.  Exploring the cognitive phenotype of autism: weak "central coherence" in parents and siblings of children with autism: II. Real-life skills and preferences. , 2001, Journal of child psychology and psychiatry, and allied disciplines.

[71]  J. Raven,et al.  Manual for Raven's progressive matrices and vocabulary scales , 1962 .

[72]  D. Perrett,et al.  Detecting subtle facial emotion recognition deficits in high-functioning Autism using dynamic stimuli of varying intensities , 2010, Neuropsychologia.

[73]  Wouter Staal,et al.  Genetics of autistic disorders: review and clinical implications , 2009, European Child & Adolescent Psychiatry.

[74]  Judith Piggot,et al.  Accuracy of phenotyping of autistic children based on internet implemented parent report , 2010, American journal of medical genetics. Part B, Neuropsychiatric genetics : the official publication of the International Society of Psychiatric Genetics.

[75]  R. Knabb,et al.  ANNALS OF THE NEW YORK ACADEMY OF SCIENCES , 2014, Annals of the New York Academy of Sciences.