Brain Regions Related to Impulsivity Mediate the Effects of Early Adversity on Antisocial Behavior

Scott Mackey; Bader Chaarani; Kees-Jan Kan; Philip A Spechler; Catherine Orr; Tobias Banaschewski; Gareth Barker; Arun L W Bokde; Uli Bromberg; Christian Büchel; Anna Cattrell; Patricia J Conrod; Sylvane Desrivières; Herta Flor; Vincent Frouin; Jürgen Gallinat; Penny Gowland; Andreas Heinz; Bernd Ittermann; Marie-Laure Paillère Martinot; Eric Artiges; Frauke Nees; Dimitri Papadopoulos-Orfanos; Luise Poustka; Michael N Smolka; Sarah Jurk; Henrik Walter; Robert Whelan; Gunter Schumann; Robert R Althoff; Hugh Garavan; IMAGEN Consortium

doi:10.1016/j.biopsych.2015.12.027

Brain Regions Related to Impulsivity Mediate the Effects of Early Adversity on Antisocial Behavior

Biol Psychiatry. 2017 Aug 15;82(4):275-282. doi: 10.1016/j.biopsych.2015.12.027. Epub 2016 Jan 18.

Authors

Scott Mackey¹, Bader Chaarani², Kees-Jan Kan³, Philip A Spechler², Catherine Orr², Tobias Banaschewski⁴, Gareth Barker⁵, Arun L W Bokde⁶, Uli Bromberg⁷, Christian Büchel⁸, Anna Cattrell⁹, Patricia J Conrod¹⁰, Sylvane Desrivières⁸, Herta Flor¹¹, Vincent Frouin¹², Jürgen Gallinat¹³, Penny Gowland¹⁴, Andreas Heinz¹⁵, Bernd Ittermann¹⁶, Marie-Laure Paillère Martinot¹⁷, Eric Artiges¹⁸, Frauke Nees¹¹, Dimitri Papadopoulos-Orfanos¹², Luise Poustka¹⁹, Michael N Smolka²⁰, Sarah Jurk²⁰, Henrik Walter¹⁵, Robert Whelan²¹, Gunter Schumann⁸, Robert R Althoff², Hugh Garavan²; IMAGEN Consortium

Affiliations

¹ Department of Psychiatry, University of Vermont, Burlington, Vermont. Electronic address: msmackey@uvm.edu.
² Department of Psychiatry, University of Vermont, Burlington, Vermont.
³ Department of Psychiatry, University of Vermont, Burlington, Vermont; Department of Psychology, University College Dublin, Dublin, Ireland; Department of Biological Psychology, VU University, Amsterdam, Netherlands.
⁴ Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.
⁵ Centre for Neuroimaging Sciences, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, United Kingdom.
⁶ Discipline of Psychiatry, School of Medicine and Trinity College Institute of Neurosciences, Trinity College Dublin, Dublin, Ireland.
⁷ University Medical Centre Hamburg-Eppendorf, Hamburg, Germany.
⁸ Medical Research Council Social, Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, United Kingdom.
⁹ Department of Psychiatry, Universite de Montreal, CHU Ste Justine Hospital, Montreal, Canada.
¹⁰ Department of Psychiatry, Universite de Montreal, CHU Ste Justine Hospital, Montreal, Canada; Department of Psychological Medicine and Psychiatry, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, United Kingdom.
¹¹ Department of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.
¹² Department of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany; Neurospin, Commissariat à l'Energie Atomique, CEA-Saclay Center, Paris, France.
¹³ Department of Psychiatry and Psychotherapy, University Medical Centre Hamburg-Eppendorf, Hamburg, Germany.
¹⁴ Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham, University Park, Nottingham, United Kingdom.
¹⁵ Department of Psychiatry and Psychotherapy, Campus Charité Mitte, Charité, Universitätsmedizin Berlin, Berlin, Germany.
¹⁶ Physikalisch-Technische Bundesanstalt, Berlin, Germany.
¹⁷ Institut National de la Santé et de la Recherche Médicale, Unit 1000 Neuroimaging and Psychiatry, University Paris Sud, University Paris Descartes-Sorbonne Paris Cité, Paris; AP-HP, Department of Adolescent Psychopathology and Medicine, Maison de Solenn, Cochin Hospital, Paris.
¹⁸ Institut National de la Santé et de la Recherche Médicale, Unit 1000 Neuroimaging and Psychiatry, University Paris Sud, University Paris Descartes-Sorbonne Paris Cité, Orsay, France; Psychiatry Department, Orsay Hospital, Orsay, France.
¹⁹ Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany; Department of Child and Adolescent Psychiatry and Psychotherapy, Medical University of Vienna, Vienna, Austria.
²⁰ Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, Dresden, Germany.
²¹ Department of Psychology, University College Dublin, Dublin, Ireland.

PMID: 26971049
DOI: 10.1016/j.biopsych.2015.12.027

Abstract

Background: Individual differences in impulsivity and early adversity are known to be strong predictors of adolescent antisocial behavior. However, the neurobiological bases of impulsivity and their relation to antisocial behavior and adversity are poorly understood.

Methods: Impulsivity was estimated with a temporal discounting task. Voxel-based morphometry was used to determine the brain structural correlates of temporal discounting in a large cohort (n = 1830) of 14- to 15-year-old children. Mediation analysis was then used to determine whether the volumes of brain regions associated with temporal discounting mediate the relation between adverse life events (e.g., family conflict, serious accidents) and antisocial behaviors (e.g., precocious sexual activity, bullying, illicit substance use).

Results: Greater temporal discounting (more impulsivity) was associated with 1) lower volume in frontomedial cortex and bilateral insula and 2) greater volume in a subcortical region encompassing the ventral striatum, hypothalamus and anterior thalamus. The volume ratio between these cortical and subcortical regions was found to partially mediate the relation between adverse life events and antisocial behavior.

Conclusions: Temporal discounting is related to regions of the brain involved in reward processing and interoception. The results support a developmental imbalance model of impulsivity and are consistent with the idea that negative environmental factors can alter the developing brain in ways that promote antisocial behavior.

Keywords: Adversity; Antisocial behavior; Development; Impulsivity; Temporal discounting; Voxel-based morphometry.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Adolescent
Analysis of Variance
Antisocial Personality Disorder / diagnostic imaging
Antisocial Personality Disorder / pathology*
Antisocial Personality Disorder / physiopathology*
Brain / diagnostic imaging
Brain / pathology*
Brain Mapping*
Europe
Female
Humans
Impulsive Behavior / physiology*
Magnetic Resonance Imaging
Male
Neuropsychological Tests
Psychiatric Status Rating Scales
Reaction Time / physiology
Surveys and Questionnaires

Abstract

Publication types

MeSH terms

Grants and funding