Cortical deficits of emotional face processing in adults with ADHD: Its relation to social cognition and executive function

Although it has been shown that adults with attention-deficit hyperactivity disorder (ADHD) have impaired social cognition, no previous study has reported the brain correlates of face valence processing. This study looked for behavioral, neuropsychological, and electrophysiological markers of emotion processing for faces (N170) in adult ADHD compared to controls matched by age, gender, educational level, and handedness. We designed an event-related potential (ERP) study based on a dual valence task (DVT), in which faces and words were presented to test the effects of stimulus type (faces, words, or face-word stimuli) and valence (positive versus negative). Individual signatures of cognitive functioning in participants with ADHD and controls were assessed with a comprehensive neuropsychological evaluation, including executive functioning (EF) and theory of mind (ToM). Compared to controls, the adult ADHD group showed deficits in N170 emotion modulation for facial stimuli. These N170 impairments were observed in the absence of any deficit in facial structural processing, suggesting a specific ADHD impairment in early facial emotion modulation. The cortical current density mapping of N170 yielded a main neural source of N170 at posterior section of fusiform gyrus (maximum at left hemisphere for words and right hemisphere for faces and simultaneous stimuli). Neural generators of N170 (fusiform gyrus) were reduced in ADHD. In those patients, N170 emotion processing was associated with performance on an emotional inference ToM task, and N170 from simultaneous stimuli was associated with EF, especially working memory. This is the first report to reveal an adult ADHD-specific impairment in the cortical modulation of emotion for faces and an association between N170 cortical measures and ToM and EF.

[1]  V. Stone,et al.  Social and emotional competence in traumatic brain injury: New and established assessment tools , 2011, Social neuroscience.

[2]  Daniel C. Krawczyk,et al.  Brain activation during a social attribution task in adolescents with moderate to severe traumatic brain injury , 2011, Social neuroscience.

[3]  A. Bechara,et al.  A somatic marker perspective of immoral and corrupt behavior , 2011, Social neuroscience.

[4]  H. Fukuyama,et al.  Transcultural differences in brain activation patterns during theory of mind (ToM) task performance in Japanese and Caucasian participants , 2011, Social neuroscience.

[5]  Michael F. Green,et al.  Theory of mind in schizophrenia: Exploring neural mechanisms of belief attribution , 2011, Social neuroscience.

[6]  Jean Decety,et al.  Subliminal presentation of other faces (but not own face) primes behavioral and evoked cortical processing of empathy for pain , 2011, Brain Research.

[7]  Carlos E. Thomaz,et al.  Please Scroll down for Article Social Neuroscience Identification of Psychopathic Individuals Using Pattern Classification of Mri Images Identification of Psychopathic Individuals Using Pattern Classification of Mri Images , 2022 .

[8]  S. Strejilevich,et al.  Neuropsychological functioning in adult bipolar disorder and ADHD patients: A comparative study , 2011, Psychiatry Research.

[9]  S. Baez,et al.  Facial and semantic emotional interference: A pilot study on the behavioral and cortical responses to the dual valence association task , 2011, Behavioral and Brain Functions.

[10]  Patrick Chauvel,et al.  From Perception to Recognition Memory: Time Course and Lateralization of Neural Substrates of Word and Abstract Picture Processing , 2011, Journal of Cognitive Neuroscience.

[11]  A. Lawrence,et al.  Apathy blunts neural response to money in Parkinson's disease , 2011, Social neuroscience.

[12]  F. Manes,et al.  When context is difficult to integrate: Cortical measures of congruency in schizophrenics and healthy relatives from multiplex families , 2011, Schizophrenia Research.

[13]  M. Herrmann,et al.  Neurobiological and psychophysiological correlates of emotional dysregulation in ADHD patients , 2010, Attention deficit and hyperactivity disorders.

[14]  V. Peralta,et al.  Risk factors, pre-morbid functioning and episode correlates of neurological soft signs in drug-naive patients with schizophrenia-spectrum disorders , 2010, Psychological Medicine.

[15]  L. Adler Monitoring adults with ADHD: a focus on executive and behavioral function. , 2010, The Journal of clinical psychiatry.

[16]  F. Manes,et al.  Applauding with Closed Hands: Neural Signature of Action-Sentence Compatibility Effects , 2010, PloS one.

[17]  R. Barkley,et al.  Differential diagnosis of adults with ADHD: the role of executive function and self-regulation. , 2010, The Journal of clinical psychiatry.

[18]  Agustín Ibáñez,et al.  Size and probability of rewards modulate the feedback error-related negativity associated with wins but not losses in a monetarily rewarded gambling task , 2010, NeuroImage.

[19]  P. Chokka,et al.  Adult ADHD and its comorbidities, with a focus on bipolar disorder. , 2010, Journal of affective disorders.

[20]  Alice Mado Proverbio,et al.  Face Coding Is Bilateral in the Female Brain , 2010, PloS one.

[21]  I. Daum,et al.  Social cognition in attention-deficit hyperactivity disorder (ADHD) , 2010, Neuroscience & Biobehavioral Reviews.

[22]  Werner Sommer,et al.  Individual Differences in Face Cognition: Brain–Behavior Relationships , 2010, Journal of Cognitive Neuroscience.

[23]  Natalia Trujillo,et al.  Gesture influences the processing of figurative language in non-native speakers: ERP evidence , 2010, Neuroscience Letters.

[24]  E. Elliott,et al.  Can we improve the clinical assessment of working memory? An evaluation of the Wechsler Adult Intelligence Scale–Third Edition using a working memory criterion construct , 2010, Journal of clinical and experimental neuropsychology.

[25]  S. Kochen,et al.  Approximate average head models for EEG source imaging , 2009, Journal of Neuroscience Methods.

[26]  M. Herrmann,et al.  Emotional deficits in adult ADHD patients: an ERP study. , 2009, Social cognitive and affective neuroscience.

[27]  F. Manes,et al.  INECO Frontal Screening (IFS): A brief, sensitive, and specific tool to assess executive functions in dementia – ERRATUM , 2009, Journal of the International Neuropsychological Society.

[28]  A. Ibanez,et al.  N400 deficits from semantic matching of pictures in probands and first-degree relatives from multiplex schizophrenia families , 2009, Brain and Cognition.

[29]  Vladimir López,et al.  ERPs studies of cognitive processing during sleep. , 2009, International journal of psychology : Journal international de psychologie.

[30]  Facundo Manes,et al.  Contextual blending of ingroup/outgroup face stimuli and word valence: LPP modulation and convergence of measures , 2009, BMC Neuroscience.

[31]  Roxane J. Itier,et al.  Neural bases of eye and gaze processing: The core of social cognition , 2009, Neuroscience & Biobehavioral Reviews.

[32]  P. Corkum,et al.  Social Information Processing in Elementary-School Aged Children with ADHD: Medication Effects and Comparisons with Typical Children , 2009, Journal of abnormal child psychology.

[33]  L. Pessoa How do emotion and motivation direct executive control? , 2009, Trends in Cognitive Sciences.

[34]  K. Lesch,et al.  Abnormal Affective Responsiveness in Attention-Deficit/Hyperactivity Disorder: Subtype Differences , 2009, Biological Psychiatry.

[35]  W. Sommer,et al.  Emotions in word and face processing: Early and late cortical responses , 2009, Brain and Cognition.

[36]  A. Ibanez,et al.  Multi-level analysis of cultural phenomena: The role of ERPs approach to prejudice , 2009 .

[37]  S. Bálint,et al.  Prevalence and correlates of adult attention-deficit hyperactivity disorder: meta-analysis , 2009, British Journal of Psychiatry.

[38]  N. M. Mukaddes,et al.  Co-morbidity of bipolar disorder in children and adolescents with attention deficit/hyperactivity disorder (ADHD) in an outpatient Turkish sample , 2009, The world journal of biological psychiatry : the official journal of the World Federation of Societies of Biological Psychiatry.

[39]  Abigail A. Marsh,et al.  Deficits in facial affect recognition among antisocial populations: A meta-analysis , 2008, Neuroscience & Biobehavioral Reviews.

[40]  Ann-Christine Ehlis,et al.  Diminished prefrontal oxygenation with normal and above-average verbal fluency performance in adult ADHD. , 2008, Journal of psychiatric research.

[41]  D. Yarnitsky,et al.  Neurophysiology of the cortical pain network: revisiting the role of S1 in subjective pain perception via standardized low-resolution brain electromagnetic tomography (sLORETA). , 2008, The journal of pain : official journal of the American Pain Society.

[42]  A. Ibanez,et al.  N400 deficits from semantic matching of pictures in probands and first degree relatives from multiplex schizophrenia families , 2008, Clinical Neurophysiology.

[43]  B. de Gelder,et al.  Rapid influence of emotional scenes on encoding of facial expressions: an ERP study. , 2008, Social cognitive and affective neuroscience.

[44]  T. Hendler,et al.  The validity of the face-selective ERP N170 component during simultaneous recording with functional MRI , 2008, NeuroImage.

[45]  Jonathan Williams,et al.  Working toward a neurobiological account of ADHD: commentary on Gail Tripp and Jeff Wickens, dopamine transfer deficit. , 2008, Journal of child psychology and psychiatry, and allied disciplines.

[46]  Hannah Keage,et al.  Misinterpreting Emotional Expressions in Attention-Deficit/Hyperactivity Disorder: Evidence for a Neural Marker and Stimulant Effects , 2008, Biological Psychiatry.

[47]  Jan K Buitelaar,et al.  Attention-deficit/hyperactivity disorder and social dysfunctioning. , 2008, Clinical psychology review.

[48]  Arthur W. Toga,et al.  Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template , 2008, NeuroImage.

[49]  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.

[50]  Bruno Rossion,et al.  Does physical interstimulus variance account for early electrophysiological face sensitive responses in the human brain? Ten lessons on the N170 , 2008, NeuroImage.

[51]  G. Pourtois,et al.  Distributed and interactive brain mechanisms during emotion face perception: Evidence from functional neuroimaging , 2007, Neuropsychologia.

[52]  Wolfram Boucsein,et al.  Modification of N170 by different emotional expression of schematic faces , 2007, Biological Psychology.

[53]  A. Bechara,et al.  Impulsive behavior in adults with attention deficit/ hyperactivity disorder: Characterization of attentional, motor and cognitive impulsiveness , 2007, Journal of the International Neuropsychological Society.

[54]  Gabriel Curio,et al.  MEG/EEG sources of the 170-ms response to faces are co-localized in the fusiform gyrus , 2007, NeuroImage.

[55]  Leanne M. Williams,et al.  ADHD and schizophrenia phenomenology: Visual scanpaths to emotional faces as a potential psychophysiological marker? , 2006, Neuroscience & Biobehavioral Reviews.

[56]  F. Rothhammer,et al.  Attention-deficit hyperactivity disorder involves differential cortical processing in a visual spatial attention paradigm , 2006, Clinical Neurophysiology.

[57]  N. Birbaumer,et al.  Evidence of cortical learning in vegetative state , 2006, Journal of Neurology.

[58]  Vladimir López,et al.  ERPs and contextual semantic discrimination: Degrees of congruence in wakefulness and sleep , 2006, Brain and Language.

[59]  Bernard Dan,et al.  Recognition of emotional facial expressions in attention-deficit hyperactivity disorder. , 2006, Pediatric neurology.

[60]  S. Safren Cognitive-behavioral approaches to ADHD treatment in adulthood. , 2006, The Journal of clinical psychiatry.

[61]  Hongtu Zhu,et al.  Hippocampus and amygdala morphology in attention-deficit/hyperactivity disorder. , 2006, Archives of general psychiatry.

[62]  Susan Sprich,et al.  Cognitive-behavioral therapy for ADHD in medication-treated adults with continued symptoms. , 2005, Behaviour research and therapy.

[63]  G. Bush,et al.  Functional Neuroimaging of Attention-Deficit/Hyperactivity Disorder: A Review and Suggested Future Directions , 2005, Biological Psychiatry.

[64]  Michela Balconi,et al.  Event-Related Potentials Related to Normal and Morphed Emotional Faces , 2005, The Journal of psychology.

[65]  E T Bullmore,et al.  Behavioural and neurocognitive responses to sad facial affect are attenuated in patients with mania , 2004, Psychological Medicine.

[66]  Lucy T. Zhang,et al.  Immersed finite element method , 2004 .

[67]  D. Morin,et al.  Depressive symptoms and associated factors in children with attention deficit hyperactivity disorder. , 2004, Journal of child and adolescent psychiatric nursing : official publication of the Association of Child and Adolescent Psychiatric Nurses, Inc.

[68]  H. Gray,et al.  P300 as an index of attention to self-relevant stimuli , 2004 .

[69]  B. Sodian,et al.  The self and action in theory of mind research , 2003, Consciousness and Cognition.

[70]  Bruno Rossion,et al.  Early lateralization and orientation tuning for face, word, and object processing in the visual cortex , 2003, NeuroImage.

[71]  E. Sonuga-Barke,et al.  The dual pathway model of AD/HD: an elaboration of neuro-developmental characteristics , 2003, Neuroscience & Biobehavioral Reviews.

[72]  J. Perner,et al.  Do Children with ADHD Not Need Their Frontal Lobes for Theory of Mind? A Review of Brain Imaging and Neuropsychological Studies , 2003 .

[73]  B. J. Casey,et al.  Differential patterns of striatal activation in young children with and without ADHD , 2003, Biological Psychiatry.

[74]  C. Neumann,et al.  Inhibitory capacity in adults with symptoms of Attention Deficit/Hyperactivity Disorder (ADHD). , 2003, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

[75]  L. Tebartz van Elst,et al.  Psychotherapy of attention deficit hyperactivity disorder in adults , 2002, European Archives of Psychiatry and Clinical Neuroscience.

[76]  M. Tarr,et al.  Expertise Training with Novel Objects Leads to Left-Lateralized Facelike Electrophysiological Responses , 2002, Psychological science.

[77]  A. Tzelepis,et al.  Executive Functioning in Adult Attention-Deficit Hyperactivity Disorder , 2001, The Clinical neuropsychologist.

[78]  J Mazziotta,et al.  A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[79]  W. Barr Schizophrenia and Attention Deficit Disorder , 2001 .

[80]  I. Shochet,et al.  Do autism spectrum disorders differ from each other and from non-spectrum disorders on emotion recognition tests? , 2001, European Child & Adolescent Psychiatry.

[81]  G. Baird,et al.  Commentary: The Modified Checklist for Autism in Toddlers , 2001, Journal of autism and developmental disorders.

[82]  R. Barkley The Executive Functions and Self-Regulation: An Evolutionary Neuropsychological Perspective , 2001, Neuropsychology Review.

[83]  S. Baron-Cohen,et al.  The "Reading the Mind in the Eyes" Test revised version: a study with normal adults, and adults with Asperger syndrome or high-functioning autism. , 2001, Journal of child psychology and psychiatry, and allied disciplines.

[84]  E. Braaten,et al.  Self-regulation of affect in attention deficit-hyperactivity disorder (ADHD) and non-ADHD boys: differences in empathic responding. , 2000, Journal of consulting and clinical psychology.

[85]  W. Pelham,et al.  Attention-deficit/hyperactivity disordered and control boys' responses to social success and failure. , 2000, Child development.

[86]  C. Carlson,et al.  Social Functioning and Emotional Regulation in the Attention Deficit Hyperactivity Disorder Subtypes , 2000, Journal of clinical child psychology.

[87]  H. Engeland,et al.  Deficient social problem-solving in boys with ODD/CD, with ADHD, and with both disorders. , 1999, Journal of the American Academy of Child and Adolescent Psychiatry.

[88]  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.

[89]  F. Castellanos,et al.  Attention deficit/hyperactivity disorders. , 1998, Pediatrics in review.

[90]  A. Beck,et al.  Comparison of Beck Depression Inventories -IA and -II in psychiatric outpatients. , 1996, Journal of personality assessment.

[91]  R. Barkley,et al.  Attention deficit hyperactivity disorder adults: comorbidities and adaptive impairments. , 1996, Comprehensive psychiatry.

[92]  C. Carlson,et al.  The Social Functioning Of Children With ADD With Hyperactivity And ADD Without Hyperactivity , 1994 .

[93]  S. Faraone,et al.  Patterns of psychiatric comorbidity, cognition, and psychosocial functioning in adults with attention deficit hyperactivity disorder. , 1993, The American journal of psychiatry.

[94]  L. Shapiro,et al.  Verb-Argument Structure Processing in Complex Sentences in Broca′s and Wernicke′s Aphasia , 1993, Brain and Language.

[95]  A. Dejong,et al.  Nationwide practices for screening and reporting prenatal cocaine abuse: a survey of teaching programs. , 1992, Child abuse & neglect.

[96]  P. Philippot,et al.  Age and social competence in preschoolers' decoding of facial expression. , 1990, The British journal of social psychology.

[97]  A. Young,et al.  Understanding face recognition. , 1986, British journal of psychology.

[98]  A. Manstead,et al.  The relationship between children's sociometric status and ability to recognize facial expressions of emotion , 1984 .

[99]  Muriel D. Lezak,et al.  The Problem of Assessing Executive Functions , 1982 .

[100]  R. C. Young,et al.  A Rating Scale for Mania: Reliability, Validity and Sensitivity , 1978, British Journal of Psychiatry.

[101]  T. Grossmann The development of emotion perception in face and voice during infancy. , 2010, Restorative neurology and neuroscience.

[102]  Daniel S Pine,et al.  Amygdala activation during emotion processing of neutral faces in children with severe mood dysregulation versus ADHD or bipolar disorder. , 2010, The American journal of psychiatry.

[103]  A. Ibanez,et al.  Methodological considerations related to sleep paradigm using event related potentials. , 2008, Biological Research.

[104]  Wei Li,et al.  Larger deficits in brain networks for response inhibition than for visual selective attention in attention deficit hyperactivity disorder (ADHD). , 2005, Journal of child psychology and psychiatry, and allied disciplines.

[105]  R D Pascual-Marqui,et al.  Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. , 2002, Methods and findings in experimental and clinical pharmacology.

[106]  S. Mineka,et al.  Fears, phobias, and preparedness: toward an evolved module of fear and fear learning. , 2001, Psychological review.

[107]  W. Barr Schizophrenia and attention deficit disorder. Two complex disorders of attention. , 2001, Annals of the New York Academy of Sciences.

[108]  Kevin R. Murphy,et al.  Attention-deficit hyperactivity disorder : a clinical workbook , 1991 .

[109]  Bernard Rimé,et al.  Fundamentals of nonverbal behavior , 1991 .

[110]  J. E. Partington Detailed instructions for administering Partington's Pathways Test. , 1949 .