Common structural correlates of trait impulsiveness and perceptual reasoning in adolescence

Background: Trait impulsiveness is a potential factor that predicts both substance use and certain psychiatric disorders. This study investigates whether there are common structural cerebral correlates of trait impulsiveness and cognitive functioning in a large sample of healthy adolescents from the IMAGEN project. Methods: Clusters of gray matter (GM) volume associated with trait impulsiveness, Cloningers' revised temperament, and character inventory impulsiveness (TCI‐R‐I) were identified in a whole brain analysis using optimized voxel‐based morphometry in 115 healthy 14‐year‐olds. The clusters were tested for correlations with performance on the nonverbal tests (Block Design, BD; Matrix Reasoning, MT) of the Wechsler Scale of Intelligence for Children IV reflecting perceptual reasoning. Results: Cloningers' impulsiveness (TCI‐R‐I) score was significantly inversely associated with GM volume in left orbitofrontal cortex (OFC). Frontal clusters found were positively correlated with performance in perceptual reasoning tasks (Bonferroni corrected). No significant correlations between TCI‐R‐I and perceptual reasoning were observed. Conclusions: The neural correlate of trait impulsiveness in the OFC matches an area where brain function has previously been related to inhibitory control. Additionally, orbitofrontal GM volume was associated with scores for perceptual reasoning. The data show for the first time structural correlates of both cognitive functioning and impulsiveness in healthy adolescent subjects. Hum Brain Mapp, 2013. © 2011 Wiley Periodicals, Inc.

[1]  E. Rolls,et al.  Borderline personality disorder, impulsivity, and the orbitofrontal cortex. , 2005, The American journal of psychiatry.

[2]  Karl J. Friston,et al.  Voxel-based morphometry of the human brain: Methods and applications , 2005 .

[3]  H. Meltzer,et al.  The Development and Well-Being Assessment: description and initial validation of an integrated assessment of child and adolescent psychopathology. , 2000, Journal of child psychology and psychiatry, and allied disciplines.

[4]  John P Hatch,et al.  A voxel‐based morphometry study of frontal gray matter correlates of impulsivity , 2009, Human brain mapping.

[5]  S. Lilienfeld,et al.  Psychopathy Factors and Risk for Aggressive Behavior: A Test of the “Threatened Egotism” Hypothesis , 2006, Law and human behavior.

[6]  R. Elliott,et al.  Response inhibition and impulsivity: an fMRI study , 2003, Neuropsychologia.

[7]  Carsten Nicolas Boehler,et al.  Pinning down response inhibition in the brain — Conjunction analyses of the Stop-signal task , 2010, NeuroImage.

[8]  G. Zimmermann.  Risk perception, emotion regulation and impulsivity as predictors of risk behaviours among adolescents in Switzerland , 2010 .

[9]  T. Robbins,et al.  Inhibition and the right inferior frontal cortex , 2004, Trends in Cognitive Sciences.

[10]  M. Sabbagh,et al.  Understanding orbitofrontal contributions to theory-of-mind reasoning: Implications for autism , 2004, Brain and Cognition.

[11]  M. Brass,et al.  Intentional inhibition: How the “veto‐area” exerts control , 2009, Human brain mapping.

[12]  C. R. Cloninger,et al.  A psychobiological model of temperament and character. , 1993, Archives of general psychiatry.

[13]  C. R. Cloninger,et al.  A unified biosocial theory of personality and its role in the development of anxiety states. , 1986, Psychiatric developments.

[14]  Daniel L. Schwartz,et al.  Global and local morphometric differences in recently abstinent methamphetamine-dependent individuals , 2010, NeuroImage.

[15]  P. Corr,et al.  Impulsivity, Time of Day, and Stress: Effects on Intelligence Test Performance , 1998 .

[16]  T. Canli,et al.  A neurogenetic approach to impulsivity. , 2008, Journal of personality.

[17]  S. Patz,et al.  Orbitofrontal correlates of aggression and impulsivity in psychiatric patients , 2006, Psychiatry Research: Neuroimaging.

[18]  C. R. Cloninger,et al.  The psychobiological theory of temperament and character: comment on Farmer and Goldberg (2008). , 2008, Psychological assessment.

[19]  L. Westlye,et al.  Associations between regional cortical thickness and attentional networks as measured by the attention network test. , 2011, Cerebral cortex.

[20]  Maneesh C. Patel,et al.  Distinct frontal systems for response inhibition, attentional capture, and error processing , 2010, Proceedings of the National Academy of Sciences.

[21]  V. Kumari,et al.  Dysfunctional, but not functional, impulsivity is associated with a history of seriously violent behaviour and reduced orbitofrontal and hippocampal volumes in schizophrenia , 2009, Psychiatry Research: Neuroimaging.

[22]  Simone Kühn,et al.  Reduced Thickness of Medial Orbitofrontal Cortex in Smokers , 2010, Biological Psychiatry.

[23]  Felice A. Kaufmann,et al.  Is attention deficit hyperactivity disorder a valid diagnosis in the presence of high IQ? Results from the MGH Longitudinal Family Studies of ADHD. , 2007, Journal of child psychology and psychiatry, and allied disciplines.

[24]  D. Dougherty,et al.  Suicidal behaviors and drug abuse: impulsivity and its assessment. , 2004, Drug and alcohol dependence.

[25]  C. Ávila,et al.  Measuring Impulsivity in School-Aged Boys and Examining Its Relationship with ADHD and ODD Ratings , 2004, Journal of abnormal child psychology.

[26]  I. Deary,et al.  Relationships between ability and personality:does intelligence contribute positively to personal and social adjustment? , 2002 .

[27]  E. Barratt.  Impulsiveness and aggression. , 1994 .

[28]  S. Dickman,et al.  Impulsivity, arousal and attention , 2000 .

[29]  E. Coccaro,et al.  Etiology of the impulsivity/aggression relationship: Genes or environment? , 1999, Psychiatry Research.

[30]  Christian Büchel,et al.  Changes in Gray Matter Induced by Learning—Revisited , 2008, PloS one.

[31]  D. Gitelman,et al.  The spatial attention network interacts with limbic and monoaminergic systems to modulate motivation-induced attention shifts. , 2008, Cerebral cortex.

[32]  Daniel Romer,et al.  Executive cognitive functions and impulsivity as correlates of risk taking and problem behavior in preadolescents , 2009, Neuropsychologia.

[33]  Steven C. R. Williams,et al.  Mapping IQ and gray matter density in healthy young people , 2004, NeuroImage.

[34]  Danielle C. Turner,et al.  Association Between Response Inhibition and Working Memory in Adult ADHD: A Link to Right Frontal Cortex Pathology? , 2007, Biological Psychiatry.

[35]  Andrea Fossati,et al.  Predicting borderline and antisocial personality disorder features in nonclinical subjects using measures of impulsivity and aggressiveness , 2004, Psychiatry Research.

[36]  Cloninger Cr.  Discussions arising from: Cloninger, CR. A. unified biosocial theory of personality and its role in the development of anxiety states. , 1987, Psychiatric developments.

[37]  E. Barratt.  Perceptual-Motor Performance Related to Impulsiveness and Anxiety , 1967, Perceptual and motor skills.

[38]  Marcus R. Munafò,et al.  Association of the Dopamine D4 Receptor (DRD4) Gene and Approach-Related Personality Traits: Meta-Analysis and New Data , 2008, Biological Psychiatry.

[39]  J. Soliva,et al.  Global and regional gray matter reductions in ADHD: A voxel-based morphometric study , 2005, Neuroscience Letters.

[40]  Richard S. J. Frackowiak,et al.  Navigation-related structural change in the hippocampi of taxi drivers. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[41]  C. R. Cloninger,et al.  The Junior Temperament and Character Inventory: Preliminary Validation of a Child Self-Report Measure , 1999, Psychological reports.

[42]  Robert J. Sternberg,et al.  Handbook of human intelligence , 1984 .

[43]  M. Pérez-García,et al.  Bright and dark sides of impulsivity: Performance of women with high and low trait impulsivity on neuropsychological tasks , 2009, Journal of Clinical and Experimental Neuropsychology.

[44]  J. Kenemans,et al.  A meta-analytic review of stopping performance in attention-deficit/hyperactivity disorder: deficient inhibitory motor control? , 2005, Journal of abnormal psychology.

[45]  J. Wallis.  Orbitofrontal cortex and its contribution to decision-making. , 2007, Annual review of neuroscience.

[46]  Daniel Tranel,et al.  Right ventromedial prefrontal cortex: a neuroanatomical correlate of impulse control in boys. , 2009, Social cognitive and affective neuroscience.

[47]  K. Sher,et al.  Personality and substance use disorders: a prospective study. , 2000, Journal of consulting and clinical psychology.

[48]  Frank Seifert,et al.  Smoking and structural brain deficits: a volumetric MR investigation , 2006, The European journal of neuroscience.

[49]  Kibeom Lee,et al.  Fluid Intelligence, Crystallized Intelligence, and the Openness/Intellect Factor , 2000 .

[50]  C. Robert Cloninger,et al.  Childhood personality predicts alcohol abuse in young adults. , 1988, Alcoholism, clinical and experimental research.

[51]  P. Conrod,et al.  Validation of a system of classifying female substance abusers on the basis of personality and motivational risk factors for substance abuse. , 2000, Psychology of addictive behaviors : journal of the Society of Psychologists in Addictive Behaviors.

[52]  T. Trull,et al.  Borderline personality disorder features predict negative outcomes 2 years later. , 2004, Journal of abnormal psychology.

[53]  Karl J. Friston,et al.  A Voxel-Based Morphometric Study of Ageing in 465 Normal Adult Human Brains , 2001, NeuroImage.

[54]  Paul Whitney,et al.  Impulsiveness and executive control of working memory , 2004 .

[55]  T. Bouchard,et al.  The Genetic Correlation Between Impulsivity and Sensation Seeking Traits , 1997, Behavior genetics.

[56]  J. Mink.  THE BASAL GANGLIA: FOCUSED SELECTION AND INHIBITION OF COMPETING MOTOR PROGRAMS , 1996, Progress in Neurobiology.

[57]  Vincenzo Varriale,et al.  Impulsivity, intelligence and P300 wave: an empirical study. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[58]  E. Khusnutdinova,et al.  Role of dopamine transporter gene (DAT1) polymorphisms in personality traits variation , 2009, Russian Journal of Genetics.

[59]  Karl J. Friston,et al.  Voxel-Based Morphometry—The Methods , 2000, NeuroImage.

[60]  C. R. Cloninger,et al.  Individual differences in personality traits reflect structural variance in specific brain regions , 2009, Brain Research Bulletin.

[61]  W. Reith,et al.  Impairment of fronto-striatal and parietal cerebral networks correlates with attention deficit hyperactivity disorder (ADHD) psychopathology in adults — A functional magnetic resonance imaging (fMRI) study , 2010, Psychiatry Research: Neuroimaging.

[62]  A. Spirito,et al.  Affective, behavioral, and cognitive functioning in adolescents with multiple suicide attempts. , 2003, Suicide & life-threatening behavior.

[63]  B. Krauss,et al.  A Comparative fMRI Study of Cortical Representations for Thermal Painful, Vibrotactile, and Motor Performance Tasks , 1999, NeuroImage.

[64]  Russell A. Poldrack,et al.  The Cognitive Neuroscience of Response Inhibition: Relevance for Genetic Research in Attention-Deficit/Hyperactivity Disorder , 2005, Biological Psychiatry.

[65]  Robert J. Sternberg,et al.  Personality and intelligence , 1994 .

[66]  Derek G. V. Mitchell,et al.  Parsing decision making processes in prefrontal cortex: Response inhibition, overcoming learned avoidance, and reversal learning , 2011, NeuroImage.

[67]  K Ugurbil,et al.  Activation of visuomotor systems during visually guided movements: a functional MRI study. , 1998, Journal of magnetic resonance.

[68]  Jérôme Prado,et al.  Overcoming Perceptual Features in Logical Reasoning: A Parametric Functional Magnetic Resonance Imaging Study , 2007, Journal of Cognitive Neuroscience.

[69]  M. McCloskey,et al.  IQ and nonplanning impulsivity are independently associated with delay discounting in middle-aged adults , 2007 .

[70]  K. Schweizer.  Does impulsivity influence performance in reasoning , 2002 .

[71]  E. Mori,et al.  Small gray matter volume in orbitofrontal cortex in Prader‐Willi syndrome: A voxel‐based MRI study , 2011, Human brain mapping.

[72]  T. Thiel,et al.  Frontoorbital volume reductions in adult patients with attention deficit hyperactivity disorder , 2002, Neuroscience Letters.

[73]  J. Bizot,et al.  Impulsivity as a confounding factor in certain animal tests of cognitive function. , 1996, Brain research. Cognitive brain research.

[74]  J P Hatch,et al.  Fronto-limbic brain structures in suicidal and non-suicidal female patients with major depressive disorder , 2007, Molecular Psychiatry.

[75]  A. Nambu,et al.  Functional significance of the cortico–subthalamo–pallidal ‘hyperdirect’ pathway , 2002, Neuroscience Research.

[76]  J. Patton,et al.  Factor structure of the Barratt impulsiveness scale. , 1995, Journal of clinical psychology.

[77]  B. Molina,et al.  Childhood ADHD Predicts Risky Sexual Behavior in Young Adulthood , 2006, Journal of clinical child and adolescent psychology : the official journal for the Society of Clinical Child and Adolescent Psychology, American Psychological Association, Division 53.

[78]  M. Mesulam.  A cortical network for directed attention and unilateral neglect , 1981, Annals of neurology.

[79]  S. Dickman,et al.  Impulsivity and information processing. , 1993 .

[80]  E. Harmon-Jones,et al.  Impulsiveness, aggression, reading, and the P300 of the event-related potential , 1997 .

[81]  S. Puttonen,et al.  Temperament and depressive symptoms: a population-based longitudinal study on Cloninger's psychobiological temperament model. , 2004, Journal of affective disorders.

[82]  Neuroticism, extraversion, and related traits in adult twins reared apart and reared together. , 1988, Journal of personality and social psychology.

[83]  Stephen Joseph,et al.  Assessing the component structure of four self-report measures of impulsivity , 2004 .

[84]  M. Roesch,et al.  Orbitofrontal cortex, decision-making and drug addiction , 2006, Trends in Neurosciences.

[85]  Vinod Goel,et al.  Anatomy of deductive reasoning , 2007, Trends in Cognitive Sciences.

[86]  Jin Fan,et al.  Event‐Related fMRI of Inhibitory Control in the Predominantly Inattentive and Combined Subtypes of ADHD , 2009, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[87]  C. Gerfen.  Molecular effects of dopamine on striatal-projection pathways , 2000, Trends in Neurosciences.

[88]  J. Gádoros,et al.  [Neurocognitive symptoms of childhood attention deficit hyperactivity disorder]. , 2005, Psychiatria Hungarica : A Magyar Pszichiatriai Tarsasag tudomanyos folyoirata.

[89]  L. Kubička,et al.  IQ and personality traits assessed in childhood as predictors of drinking and smoking behaviour in middle-aged adults: a 24-year follow-up study. , 2001, Addiction.

[90]  Martin Ystad,et al.  Correlations between measures of executive attention and cortical thickness of left posterior middle frontal gyrus - a dichotic listening study , 2009, Behavioral and Brain Functions.

[91]  Franz Petermann,et al.  Hamburg-Wechsler-Intelligenztest für Kinder - IV , 2007 .

[92]  D. Dougherty,et al.  Increased impulsivity associated with severity of suicide attempt history in patients with bipolar disorder. , 2005, The American journal of psychiatry.

[93]  Robert J Zatorre,et al.  Anatomical Correlates of Learning Novel Speech Sounds , 2002, Neuron.

[94]  P. Links,et al.  Impulsivity: core aspect of borderline personality disorder. , 1999, Journal of personality disorders.

[95]  T. Paus,et al.  Orbitofrontal Cortex and Drug Use during Adolescence: Role of Prenatal Exposure to Maternal Smoking and BDNF Genotype. , 2009, NeuroImage.

[96]  John Monahan,et al.  Violence and mental disorder: Developments in risk assessment. , 1994 .

[97]  Steven W Anderson,et al.  Is the Prefrontal Cortex Important For Fluid Intelligence? A Neuropsychological Study Using Matrix Reasoning , 2008, The Clinical neuropsychologist.

[98]  Charles W. Mathias,et al.  Comparisons of women with high and low trait impulsivity using behavioral models of response-disinhibition and reward-choice , 2002 .

[99]  J. Brebner,et al.  Theoretical and Empirical Relationships between Personality and Intelligence , 1995 .

[100]  T. McGlashan,et al.  Borderline personality disorder criteria associated with prospectively observed suicidal behavior. , 2004, The American journal of psychiatry.