Erin Burke Quinlan1, Anna Cattrell1, Tianye Jia1, Eric Artiges1, Tobias Banaschewski1, Gareth Barker1, Arun L W Bokde1, Uli Bromberg1, Christian Büchel1, Rüdiger Brühl1, Patricia J Conrod1, Sylvane Desrivieres1, Herta Flor1, Vincent Frouin1, Jürgen Gallinat1, Hugh Garavan1, Penny Gowland1, Andreas Heinz1, Jean-Luc Martinot1, Marie-Laure Paillère Martinot1, Frauke Nees1, Dimitri Papadopoulos-Orfanos1, Tomáš Paus1, Luise Poustka1, Michael N Smolka1, Nora C Vetter1, Henrik Walter1, Robert Whelan1, Jeffrey C Glennon1, Jan K Buitelaar1, Francesca Happé1, Eva Loth1, Edward D Barker1, Gunter Schumann1. 1. From the Medical Research Council Social, Genetic, and Developmental Psychiatry Centre, the Department of Psychology, the Department of Forensic and Neurodevelopmental Sciences, the Addictions Department, and the Centre for Neuroimaging Sciences, Institute of Psychiatry, Psychology, and Neuroscience, King's College London; INSERM, UMR 1000, Neuroimaging and Psychiatry Research Unit, University Paris-Sud, University Paris Descartes, Sorbonne Paris Cité, Paris; Maison de Solenn, Paris; the Department of Psychiatry, Orsay Hospital, Orsay, France; the Department of Child and Adolescent Psychiatry and Psychotherapy and the Department of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany; Discipline of Psychiatry, School of Medicine and Trinity College Institute of Neurosciences, Trinity College Dublin; the Department of Psychiatry and Psychotherapy, University Medical Center Hamburg-Eppendorf, Hamburg, Germany; Physikalisch-Technische Bundesanstalt, Braunschweig and Berlin, Germany; the Department of Psychiatry, University of Montreal, CHU Ste. Justine Hospital, Montreal; the Department of Psychology, School of Social Sciences, University of Mannheim, Mannheim, Germany; NeuroSpin, CEA (Alternative Energies and Atomic Energy Commission), University Paris-Saclay, Gif-sur-Yvette, France; the Departments of Psychiatry and Psychology, University of Vermont, Burlington; Sir Peter Mansfield Magnetic Resonance Center, School of Physics and Astronomy, University of Nottingham, University Park, Nottingham, U.K.; the Department of Psychiatry and Psychotherapy, Campus Charité Mitte, Charité, Universitätsmedizin Berlin, Berlin; AP-HP, Department of Adolescent Psychopathology and Medicine, Maison de Solenn, Cochin Hospital, Paris; Rotman Research Institute, Baycrest, and the Departments of Psychology and Psychiatry, University of Toronto, Toronto; the Department of Child and Adolescent Psychiatry and Psychotherapy, University Medical Centre Göttingen, von-Siebold-Str., Göttingen, Germany; Clinic for Child and Adolescent Psychiatry, Medical University of Vienna, Währinger Gürtel, Vienna; the Department of Psychiatry and the Neuroimaging Center, Technische Universität Dresden, Dresden, Germany; School of Psychology and Global Brain Health Institute, Trinity College Dublin; and the Department of Cognitive Neuroscience, Donders Institute for Brain, Cognition, and Behavior, Radboud University Medical Center, and Karakter Child and Adolescent Psychiatry, Nijmegen, the Netherlands.
Abstract
OBJECTIVE: The authors sought to explore how conduct, hyperactivity/inattention, and emotional symptoms are associated with neural reactivity to social-emotional stimuli, and the extent to which psychosocial stress modulates these relationships. METHOD: Participants were community adolescents recruited as part of the European IMAGEN study. Bilateral amygdala regions of interest were used to assess the relationship between the three symptom domains and functional MRI neural reactivity during passive viewing of dynamic angry and neutral facial expressions. Exploratory functional connectivity and whole brain multiple regression approaches were used to analyze how the symptoms and psychosocial stress relate to other brain regions. RESULTS: In response to the social-emotional stimuli, adolescents with high levels of conduct or hyperactivity/inattention symptoms who had also experienced a greater number of stressful life events showed hyperactivity of the amygdala and several regions across the brain. This effect was not observed with emotional symptoms. A cluster in the midcingulate was found to be common to both conduct problems and hyperactivity symptoms. Exploratory functional connectivity analyses suggested that amygdala-precuneus connectivity is associated with hyperactivity/inattention symptoms. CONCLUSIONS: The results link hyperactive amygdala responses and regions critical for top-down emotional processing with high levels of psychosocial stress in individuals with greater conduct and hyperactivity/inattention symptoms. This work highlights the importance of studying how psychosocial stress affects functional brain responses to social-emotional stimuli, particularly in adolescents with externalizing symptoms.
OBJECTIVE: The authors sought to explore how conduct, hyperactivity/inattention, and emotional symptoms are associated with neural reactivity to social-emotional stimuli, and the extent to which psychosocial stress modulates these relationships. METHOD: Participants were community adolescents recruited as part of the European IMAGEN study. Bilateral amygdala regions of interest were used to assess the relationship between the three symptom domains and functional MRI neural reactivity during passive viewing of dynamic angry and neutral facial expressions. Exploratory functional connectivity and whole brain multiple regression approaches were used to analyze how the symptoms and psychosocial stress relate to other brain regions. RESULTS: In response to the social-emotional stimuli, adolescents with high levels of conduct or hyperactivity/inattention symptoms who had also experienced a greater number of stressful life events showed hyperactivity of the amygdala and several regions across the brain. This effect was not observed with emotional symptoms. A cluster in the midcingulate was found to be common to both conduct problems and hyperactivity symptoms. Exploratory functional connectivity analyses suggested that amygdala-precuneus connectivity is associated with hyperactivity/inattention symptoms. CONCLUSIONS: The results link hyperactive amygdala responses and regions critical for top-down emotional processing with high levels of psychosocial stress in individuals with greater conduct and hyperactivity/inattention symptoms. This work highlights the importance of studying how psychosocial stress affects functional brain responses to social-emotional stimuli, particularly in adolescents with externalizing symptoms.
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