An emotion recognition subtyping approach to studying the heterogeneity and comorbidity of autism spectrum disorders and attention-deficit/hyperactivity disorder

BackgroundEmotion recognition dysfunction has been reported in both autism spectrum disorders (ASD) and attention-deficit/hyperactivity disorder (ADHD). This suggests that emotion recognition is a cross-disorder trait that may be utilised to understand the heterogeneous psychopathology of ASD and ADHD. We aimed to identify emotion recognition subtypes and to examine their relation with quantitative and diagnostic measures of ASD and ADHD to gain further insight into disorder comorbidity and heterogeneity.MethodsFactor mixture modelling was used on speed and accuracy measures of auditory and visual emotion recognition tasks. These were administered to children and adolescents with ASD (N = 89), comorbid ASD + ADHD (N = 64), their unaffected siblings (N = 122), ADHD (N = 111), their unaffected siblings (N = 69), and controls (N = 220). Identified classes were compared on diagnostic and quantitative symptom measures.ResultsA four-class solution was revealed, with the following emotion recognition abilities: (1) average visual, impulsive auditory; (2) average-strong visual and auditory; (3) impulsive/imprecise visual, average auditory; (4) weak visual and auditory. The weakest performing class (4) contained the highest percentage of patients (66.07%) and the lowest percentage controls (10.09%), scoring the highest on ASD/ADHD measures. The best performing class (2) demonstrated the opposite: 48.98% patients, 15.26% controls with relatively low scores on ASD/ADHD measures.ConclusionsSubgroups of youths can be identified that differ both in quantitative and qualitative aspects of emotion recognition abilities. Weak emotion recognition abilities across sensory domains are linked to an increased risk for ASD as well as ADHD, although emotion recognition impairments alone are neither necessary nor sufficient parts of these disorders.

[1]  O. Dan,et al.  Response Patterns to Emotional Faces Among Adolescents Diagnosed With ADHD , 2018, Journal of attention disorders.

[2]  K. Cook,et al.  Chronic Multisymptom Illness in Gulf War Veterans: Case Definitions Reexamined , 2014 .

[3]  Jozsef Halasz,et al.  Emotion Recognition Pattern in Adolescent Boys with Attention-Deficit/Hyperactivity Disorder , 2014, BioMed research international.

[4]  Erik Willcutt,et al.  Towards an understanding of unique and shared pathways in the psychopathophysiology of ADHD. , 2005, Developmental science.

[5]  Peter Vuust,et al.  Atypical perception of affective prosody in Autism Spectrum Disorder , 2014, NeuroImage: Clinical.

[6]  J. Buitelaar,et al.  Recognition of facial emotion and affective prosody in children with ASD (+ADHD) and their unaffected siblings , 2013, European Child & Adolescent Psychiatry.

[7]  D. Skuse,et al.  Changing abilities in recognition of unfamiliar face photographs through childhood and adolescence: performance on a test of non-verbal immediate memory (Warrington RMF) from 6 to 16 years. , 2008, Journal of neuropsychology.

[8]  Matthew Garner,et al.  Emotion-recognition abilities and behavior problem dimensions in preschoolers: Evidence for a specific role for childhood hyperactivity , 2015, Child neuropsychology : a journal on normal and abnormal development in childhood and adolescence.

[9]  Jan K. Buitelaar,et al.  Cognitive Profiling Useful for Unraveling Cross-Disorder Mechanisms , 2016 .

[10]  Andreia Santos,et al.  Emotion Understanding in Children with ADHD , 2009, Child psychiatry and human development.

[11]  D. Skuse,et al.  Impaired sadness recognition is linked to social interaction deficit in autism , 2007, Neuropsychologia.

[12]  T. Kujala,et al.  Neurocognitive Functioning in Adolescents with Autism Spectrum Disorder , 2012, Journal of Autism and Developmental Disorders.

[13]  Virginie Laval,et al.  Emotional speech comprehension in children and adolescents with autism spectrum disorders. , 2013, Journal of communication disorders.

[14]  E. Taylor,et al.  The Epidemiology of Childhood Hyperactivity , 1991 .

[15]  N. Minshew,et al.  The development of emotion recognition in individuals with autism. , 2009, Child development.

[16]  L. Thorell,et al.  Multiple deficits in ADHD: executive dysfunction, delay aversion, reaction time variability, and emotional deficits , 2012, Journal of child psychology and psychiatry, and allied disciplines.

[17]  Laurence Chaby,et al.  A Multidimensional Approach to the Study of Emotion Recognition in Autism Spectrum Disorders , 2015, Front. Psychol..

[18]  A. Schienle,et al.  Processing of affective prosody in boys suffering from attention deficit hyperactivity disorder: A near-infrared spectroscopy study , 2015, Social neuroscience.

[19]  I. Moilanen,et al.  Processing of Affective Speech Prosody is Impaired in Asperger Syndrome , 2007, Journal of autism and developmental disorders.

[20]  Ellen Leibenluft,et al.  Emotion dysregulation in attention deficit hyperactivity disorder. , 2014, The American journal of psychiatry.

[21]  B. Franke,et al.  A review on cognitive and brain endophenotypes that may be common in autism spectrum disorder and attention-deficit/hyperactivity disorder and facilitate the search for pleiotropic genes , 2011, Neuroscience & Biobehavioral Reviews.

[22]  I. Kamp-Becker,et al.  Differential Diagnosis of Autism Spectrum Disorder and Attention Deficit Hyperactivity Disorder by Means of Inhibitory Control and ‘Theory of Mind’ , 2011, Journal of autism and developmental disorders.

[23]  Joanne Rovet,et al.  Social cognitive and emotion processing abilities of children with fetal alcohol spectrum disorders: a comparison with attention deficit hyperactivity disorder. , 2009, Alcoholism, clinical and experimental research.

[24]  F. Castelli,et al.  Understanding emotions from standardized facial expressions in autism and normal development , 2005, Autism : the international journal of research and practice.

[25]  E. Bora,et al.  Meta-analysis of social cognition in attention-deficit/hyperactivity disorder (ADHD): comparison with healthy controls and autistic spectrum disorder , 2015, Psychological Medicine.

[26]  Alex Martin,et al.  Diminished Sensitivity to Sad Facial Expressions in High Functioning Autism Spectrum Disorders is Associated with Symptomatology and Adaptive Functioning , 2011, Journal of autism and developmental disorders.

[27]  S. Durston,et al.  Distinct neuropsychological profiles within ADHD: a latent class analysis of cognitive control, reward sensitivity and timing , 2014, Psychological Medicine.

[28]  E. Gordon,et al.  Distinguishing symptom profiles in adolescent ADHD using an objective cognitive test battery , 2007, International journal of adolescent medicine and health.

[29]  B. Muthén,et al.  Models and Strategies for Factor Mixture Analysis: An Example Concerning the Structure Underlying Psychological Disorders , 2013, Structural equation modeling : a multidisciplinary journal.

[30]  Carly Demopoulos,et al.  A Comparison of Social Cognitive Profiles in children with Autism Spectrum Disorders and Attention-Deficit/Hyperactivity Disorder: A Matter of Quantitative but not Qualitative Difference? , 2013, Journal of autism and developmental disorders.

[31]  Mehdi Tehrani-Doost,et al.  Is Emotion Recognition Related to Core Symptoms of Childhood ADHD? , 2017, Journal of the Canadian Academy of Child and Adolescent Psychiatry = Journal de l'Academie canadienne de psychiatrie de l'enfant et de l'adolescent.

[32]  Yoshihiko Hayashi,et al.  Biological Safety of Fish (Tilapia) Collagen , 2014, BioMed research international.

[33]  Lutz Jäncke,et al.  Facial emotion recognition deficits in children with and without attention deficit hyperactivity disorder: a behavioral and neurophysiological approach , 2017, Neuroreport.

[34]  F. Rijsdijk,et al.  The Genetic Overlap of Attention-Deficit/Hyperactivity Disorder and Autistic-like Traits: an Investigation of Individual Symptom Scales and Cognitive markers , 2015, Journal of abnormal child psychology.

[35]  M. Gill,et al.  The impact of study design and diagnostic approach in a large multi-centre ADHD study: Part 2: Dimensional measures of psychopathology and intelligence , 2011, BMC psychiatry.

[36]  Deirdre Wilson,et al.  What's in a voice? Prosody as a test case for the Theory of Mind account of autism , 2011, Neuropsychologia.

[37]  Sven Bölte,et al.  Facial affect recognition in autism, ADHD and typical development , 2016, Cognitive neuropsychiatry.

[38]  J. Goldberg,et al.  Neurofunctional Underpinnings of Audiovisual Emotion Processing in Teens with Autism Spectrum Disorders , 2013, Front. Psychiatry.

[39]  B. Chakrabarti,et al.  Empathy and emotion recognition in people with autism, first-degree relatives, and controls , 2012, Neuropsychologia.

[40]  Valerie Sims,et al.  Facial Emotion Recognition in Children with High Functioning Autism and Children with Social Phobia , 2012, Child Psychiatry & Human Development.

[41]  Jan K Buitelaar,et al.  Are autism spectrum disorder and attention-deficit/hyperactivity disorder different manifestations of one overarching disorder? Cognitive and symptom evidence from a clinical and population-based sample. , 2012, Journal of the American Academy of Child and Adolescent Psychiatry.

[42]  John Suckling,et al.  Unsupervised data-driven stratification of mentalizing heterogeneity in autism , 2015, Scientific Reports.

[43]  Gerd Lehmkuhl,et al.  Do hyperactivity, impulsivity and inattention have an impact on the ability of facial affect recognition in children with autism and ADHD? , 2008, European Child & Adolescent Psychiatry.

[44]  J. VanMeter,et al.  Impairments in facial affect recognition associated with autism spectrum disorders: A meta-analysis , 2014, Development and Psychopathology.

[45]  Christopher Gillberg,et al.  Facial emotion recognition in child psychiatry: a systematic review. , 2013, Research in developmental disabilities.

[46]  Jeroen K. Vermunt,et al.  Multilevel Mixture Factor Models , 2012, Multivariate behavioral research.

[47]  Martijn Lappenschaar,et al.  Visual and auditory emotion recognition problems as familial cross-disorder phenomenon in ASD and ADHD , 2018, European Neuropsychopharmacology.

[48]  T. Seppänen,et al.  Perception of basic emotions from speech prosody in adolescents with Asperger's syndrome , 2010, Logopedics, phoniatrics, vocology.

[49]  Kyle Sterrett,et al.  An Item Response Theory Evaluation of the Autism Diagnostic Interview-Revised (ADI-R) , 2019 .

[50]  B. Franke,et al.  Changing ASD-ADHD symptom co-occurrence across the lifespan with adolescence as crucial time window: Illustrating the need to go beyond childhood , 2016, Neuroscience & Biobehavioral Reviews.

[51]  Deepti R. Bathula,et al.  Distinct neuropsychological subgroups in typically developing youth inform heterogeneity in children with ADHD , 2012, Proceedings of the National Academy of Sciences.

[52]  J. Buitelaar,et al.  Theory of mind and emotion-recognition functioning in autistic spectrum disorders and in psychiatric control and normal children , 1999, Development and Psychopathology.

[53]  J. Buitelaar,et al.  PDD Symptoms in ADHD, an Independent Familial Trait? , 2009, Journal of abnormal child psychology.

[54]  B. Corbett,et al.  Processing Affective Stimuli in Children with Attention-Deficit Hyperactivity Disorder , 2000, Child neuropsychology : a journal on normal and abnormal development in childhood and adolescence.

[55]  A. Chrisman,et al.  Mass trauma: disasters, terrorism, and war. , 2014, Child and adolescent psychiatric clinics of North America.

[56]  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.

[57]  Nicola Yuill,et al.  Selective difficulty in recognising facial expressions of emotion in boys with ADHD , 2007, European Child & Adolescent Psychiatry.

[58]  Ruth Campbell,et al.  Age, gender, and puberty influence the development of facial emotion recognition , 2015, Front. Psychol..

[59]  Peter S. Bearman,et al.  Six Developmental Trajectories Characterize Children With Autism , 2012, Pediatrics.

[60]  M. Pericak-Vance,et al.  Genetically meaningful phenotypic subgroups in autism spectrum disorders , 2014, Genes, brain, and behavior.

[61]  Jan K Buitelaar,et al.  The co-occurrence of autism spectrum disorder and attention-deficit/hyperactivity disorder symptoms in parents of children with ASD or ASD with ADHD. , 2012, Journal of child psychology and psychiatry, and allied disciplines.

[62]  Catherine Lord,et al.  The Social Communication Questionnaire Manual , 2003 .

[63]  N. Ryan,et al.  Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): initial reliability and validity data. , 1997, Journal of the American Academy of Child and Adolescent Psychiatry.

[64]  J. Brian,et al.  Examining and comparing social perception abilities across childhood-onset neurodevelopmental disorders. , 2015, Journal of the American Academy of Child and Adolescent Psychiatry.

[65]  N. Rommelse.  Executive Functioning in Attention-deficit–Hyperactivity Disorder – Crucial or Trivial? , 2009 .

[66]  M. Brosnan,et al.  Emotion Recognition in Animated Compared to Human Stimuli in Adolescents with Autism Spectrum Disorder , 2015, Journal of autism and developmental disorders.

[67]  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.

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

[69]  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.

[70]  Hauke R. Heekeren,et al.  Emotional prosody processing in autism spectrum disorder , 2016, Social cognitive and affective neuroscience.

[71]  M. Gill,et al.  The impact of study design and diagnostic approach in a large multi-centre ADHD study. Part 1: ADHD symptom patterns , 2011, BMC psychiatry.