Positive Emotionality is Associated with Baseline Metabolism in Orbitofrontal Cortex and in Regions of the Default Network

Positive emotionality (PEM) (personality construct of well-being, achievement/motivation, social and closeness) has been associated with striatal dopamine D2 receptor availability in healthy controls. As striatal D2 receptors modulate activity in orbitofrontal cortex (OFC) and cingulate (brain regions that process natural and drug rewards), we hypothesized that these regions underlie PEM. To test this, we assessed the correlation between baseline brain glucose metabolism (measured with positron emission tomography and [18F]fluoro-deoxyglucose) and scores on PEM (obtained from the multidimensional personality questionnaire or MPQ) in healthy controls (n=47). Statistical parametric mapping (SPM) analyses revealed that PEM was positively correlated (Pc<0.05, voxel corrected) with metabolism in various cortical regions that included orbitofrontal (Brodman area, BA 11, 47) and cingulate (BA 23, 32) and other frontal (BA 10, 9), parietal (precuneus, BA 40) and temporal (BA 20, 21) regions that overlap with the brain's default mode network (DMN). Correlations with the other two main MPQ personality dimensions (negative emotionality and constraint) were not significant (SPM Pc<0.05). Our results corroborate an involvement of orbitofrontal and cingulate regions in PEM, which is considered a trait that protects against substance use disorders. As dysfunction of OFC and cingulate is a hallmark of addiction, these findings support a common neural basis underlying protective personality factors and brain dysfunction underlying substance use disorders. In addition, we also uncovered an association between PEM and baseline metabolism in regions from the DMN, which suggests that PEM may relate to global cortical processes that are active during resting conditions (introspection, mind wandering).

[1]  M. Yücel,et al.  The neurobiological basis of temperament: Towards a better understanding of psychopathology , 2006, Neuroscience & Biobehavioral Reviews.

[2]  T. Wills,et al.  Family risk factors and adolescent substance use: moderation effects for temperament dimensions. , 2001, Developmental psychology.

[3]  J. Swanson,et al.  Dopamine in drug abuse and addiction: results from imaging studies and treatment implications , 2004, Molecular Psychiatry.

[4]  E. Hoffman,et al.  TOMOGRAPHIC MEASUREMENT OF LOCAL CEREBRAL GLUCOSE METABOLIC RATE IN HUMANS WITH (F‐18)2‐FLUORO-2‐DEOXY-D‐GLUCOSE: VALIDATION OF METHOD , 1980, Annals of neurology.

[5]  Thilo Deckersbach,et al.  Regional cerebral brain metabolism correlates of neuroticism and extraversion , 2006, Depression and anxiety.

[6]  Frank Telang,et al.  High levels of dopamine D2 receptors in unaffected members of alcoholic families: possible protective factors. , 2006, Archives of general psychiatry.

[7]  N. Volkow,et al.  Subjective sensitivity to monetary gradients is associated with frontolimbic activation to reward in cocaine abusers. , 2007, Drug and alcohol dependence.

[8]  M. Kringelbach The human orbitofrontal cortex: linking reward to hedonic experience , 2005, Nature Reviews Neuroscience.

[9]  Peter Kirsch,et al.  Motivational orientation modulates the neural response to reward , 2010, NeuroImage.

[10]  S. Hyman,et al.  Acute Effects of Cocaine on Human Brain Activity and Emotion , 1997, Neuron.

[11]  Christopher J Patrick,et al.  Development and validation of a brief form of the Multidimensional Personality Questionnaire. , 2002, Psychological assessment.

[12]  E. Rolls,et al.  Emotion-related learning in patients with social and emotional changes associated with frontal lobe damage. , 1994, Journal of neurology, neurosurgery, and psychiatry.

[13]  Timothy Edward John Behrens,et al.  Contrasting roles for cingulate and orbitofrontal cortex in decisions and social behaviour , 2007, Trends in Cognitive Sciences.

[14]  G. Shulman,et al.  Persistence and brain circuitry , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[15]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[16]  Rita Z. Goldstein,et al.  Anterior cingulate cortex hypoactivations to an emotionally salient task in cocaine addiction , 2009, Proceedings of the National Academy of Sciences.

[17]  R. Risinger,et al.  Expectation Modulates Human Brain Responses to Acute Cocaine: A Functional Magnetic Resonance Imaging Study , 2008, Biological Psychiatry.

[18]  Jean Logan,et al.  Brain DA D2 receptors predict reinforcing effects of stimulants in humans: Replication study , 2002, Synapse.

[19]  J S Fowler,et al.  Prediction of reinforcing responses to psychostimulants in humans by brain dopamine D2 receptor levels. , 1999, The American journal of psychiatry.

[20]  J S Fowler,et al.  Addiction, a disease of compulsion and drive: involvement of the orbitofrontal cortex. , 2000, Cerebral cortex.

[21]  N. Volkow,et al.  D2R DNA transfer into the nucleus accumbens attenuates cocaine self‐administration in rats , 2008, Synapse.

[22]  E. Rolls,et al.  From affective value to decision‐making in the prefrontal cortex , 2008, The European journal of neuroscience.

[23]  Nora D. Volkow,et al.  Methylphenidate Decreased the Amount of Glucose Needed by the Brain to Perform a Cognitive Task , 2008, PloS one.

[24]  N. Volkow,et al.  Functional importance of ventricular enlargement and cortical atrophy in healthy subjects and alcoholics as assessed with PET, MR imaging, and neuropsychologic testing. , 1993, Radiology.

[25]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[26]  A. Roberts,et al.  Uncoupling of behavioral and autonomic responses after lesions of the primate orbitofrontal cortex , 2008, Proceedings of the National Academy of Sciences.

[27]  J S Fowler,et al.  Association of methylphenidate-induced craving with changes in right striato-orbitofrontal metabolism in cocaine abusers: implications in addiction. , 1999, The American journal of psychiatry.

[28]  R. Depue,et al.  Neurobiology of the structure of personality: Dopamine, facilitation of incentive motivation, and extraversion , 1999, Behavioral and Brain Sciences.

[29]  N. Volkow,et al.  Imaging dopamine's role in drug abuse and addiction , 2009, Neuropharmacology.

[30]  M. Yücel,et al.  Neuroanatomical correlates of temperament in early adolescents. , 2008, Journal of the American Academy of Child and Adolescent Psychiatry.

[31]  A. Dale,et al.  Dorsal anterior cingulate cortex: A role in reward-based decision making , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[32]  I. Toni,et al.  On the neural control of social emotional behavior. , 2009, Social cognitive and affective neuroscience.

[33]  T. Robbins,et al.  Neural mechanisms underlying the vulnerability to develop compulsive drug-seeking habits and addiction , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[34]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[35]  K. Berridge,et al.  Affective neuroscience of pleasure: reward in humans and animals , 2008, Psychopharmacology.

[36]  C. Robert Cloninger,et al.  Measurement of Impulsivity in a Hierarchical Model of Personality Traits: Implications for Substance Use , 2003, Substance use & misuse.

[37]  Dong Soo Lee,et al.  Relationship between personality trait and regional cerebral glucose metabolism assessed with positron emission tomography , 2002, Biological Psychology.

[38]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[39]  J. Allman,et al.  The Anterior Cingulate Cortex , 2001, Annals of the New York Academy of Sciences.

[40]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

[41]  Rita Z. Goldstein,et al.  Drug addiction and its underlying neurobiological basis: neuroimaging evidence for the involvement of the frontal cortex. , 2002, The American journal of psychiatry.

[42]  Mikio Iwase,et al.  Regional brain cerebral glucose metabolism and temperament: A positron emission tomography study , 2006, Neuroscience Letters.

[43]  M. Reivich,et al.  THE [14C]DEOXYGLUCOSE METHOD FOR THE MEASUREMENT OF LOCAL CEREBRAL GLUCOSE UTILIZATION: THEORY, PROCEDURE, AND NORMAL VALUES IN THE CONSCIOUS AND ANESTHETIZED ALBINO RAT 1 , 1977, Journal of neurochemistry.