Genetic variation in MAOA modulates ventromedial prefrontal circuitry mediating individual differences in human personality
Little is known about neural mechanisms underlying human personality and temperament, despite their considerable importance as highly heritable risk mediators for somatic and psychiatric disorders. To identify these circuits, we used a combined genetic and imaging approach focused on Monoamine Oxida...
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| Published in | Molecular psychiatry Vol. 13; no. 3; pp. 313 - 324 |
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| Main Authors | , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
01.03.2008
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Little is known about neural mechanisms underlying human personality and temperament, despite their considerable importance as highly heritable risk mediators for somatic and psychiatric disorders. To identify these circuits, we used a combined genetic and imaging approach focused on Monoamine Oxidase A (MAOA), encoding a key enzyme for monoamine metabolism previously associated with temperament and antisocial behavior. Male carriers of a low-expressing genetic variant exhibited dysregulated amygdala activation and increased functional coupling with ventromedial prefrontal cortex (vmPFC). Stronger coupling predicted increased harm avoidance and decreased reward dependence scores, suggesting that this circuitry mediates a part of the association of MAOA with these traits. We utilized path analysis to parse the effective connectivity within this system, and provide evidence that vmPFC regulates amygdala indirectly by influencing rostral cingulate cortex function. Our data implicate a neural circuit for variation in human personality under genetic control, provide an anatomically consistent mechanism for vmPFC–amygdala interactions underlying this variation, and suggest a role for vmPFC as a superordinate regulatory area for emotional arousal and social behavior. |
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| AbstractList | Little is known about neural mechanisms underlying human personality and temperament, despite their considerable importance as highly heritable risk mediators for somatic and psychiatric disorders. To identify these circuits, we used a combined genetic and imaging approach focused on Monoamine Oxidase A (MAOA), encoding a key enzyme for monoamine metabolism previously associated with temperament and antisocial behavior. Male carriers of a low-expressing genetic variant exhibited dysregulated amygdala activation and increased functional coupling with ventromedial prefrontal cortex (vmPFC). Stronger coupling predicted increased harm avoidance and decreased reward dependence scores, suggesting that this circuitry mediates a part of the association of MAOA with these traits. We utilized path analysis to parse the effective connectivity within this system, and provide evidence that vmPFC regulates amygdala indirectly by influencing rostral cingulate cortex function. Our data implicate a neural circuit for variation in human personality under genetic control, provide an anatomically consistent mechanism for vmPFC–amygdala interactions underlying this variation, and suggest a role for vmPFC as a superordinate regulatory area for emotional arousal and social behavior. Little is known about neural mechanisms underlying human personality and temperament, despite their considerable importance as highly heritable risk mediators for somatic and psychiatric disorders. To identify these circuits, we used a combined genetic and imaging approach focused on Monoamine Oxidase A (MAOA), encoding a key enzyme for monoamine metabolism previously associated with temperament and antisocial behavior. Male carriers of a low-expressing genetic variant exhibited dysregulated amygdala activation and increased functional coupling with ventromedial prefrontal cortex (vmPFC). Stronger coupling predicted increased harm avoidance and decreased reward dependence scores, suggesting that this circuitry mediates a part of the association of MAOA with these traits. We utilized path analysis to parse the effective connectivity within this system, and provide evidence that vmPFC regulates amygdala indirectly by influencing rostral cingulate cortex function. Our data implicate a neural circuit for variation in human personality under genetic control, provide an anatomically consistent mechanism for vmPFC-amygdala interactions underlying this variation, and suggest a role for vmPFC as a superordinate regulatory area for emotional arousal and social behavior.Molecular Psychiatry (2008) 13, 313-324; doi:10.1038/sj.mp.4002020; published online 22 May 2007 Little is known about neural mechanisms underlying human personality and temperament, despite their considerable importance as highly heritable risk mediators for somatic and psychiatric disorders. To identify these circuits, we used a combined genetic and imaging approach focused on Monoamine Oxidase A (MAOA), encoding a key enzyme for monoamine metabolism previously associated with temperament and antisocial behavior. Male carriers of a low-expressing genetic variant exhibited dysregulated amygdala activation and increased functional coupling with ventromedial prefrontal cortex (vmPFC). Stronger coupling predicted increased harm avoidance and decreased reward dependence scores, suggesting that this circuitry mediates a part of the association of MAOA with these traits. We utilized path analysis to parse the effective connectivity within this system, and provide evidence that vmPFC regulates amygdala indirectly by influencing rostral cingulate cortex function. Our data implicate a neural circuit for variation in human personality under genetic control, provide an anatomically consistent mechanism for vmPFC-amygdala interactions underlying this variation, and suggest a role for vmPFC as a superordinate regulatory area for emotional arousal and social behavior.Little is known about neural mechanisms underlying human personality and temperament, despite their considerable importance as highly heritable risk mediators for somatic and psychiatric disorders. To identify these circuits, we used a combined genetic and imaging approach focused on Monoamine Oxidase A (MAOA), encoding a key enzyme for monoamine metabolism previously associated with temperament and antisocial behavior. Male carriers of a low-expressing genetic variant exhibited dysregulated amygdala activation and increased functional coupling with ventromedial prefrontal cortex (vmPFC). Stronger coupling predicted increased harm avoidance and decreased reward dependence scores, suggesting that this circuitry mediates a part of the association of MAOA with these traits. We utilized path analysis to parse the effective connectivity within this system, and provide evidence that vmPFC regulates amygdala indirectly by influencing rostral cingulate cortex function. Our data implicate a neural circuit for variation in human personality under genetic control, provide an anatomically consistent mechanism for vmPFC-amygdala interactions underlying this variation, and suggest a role for vmPFC as a superordinate regulatory area for emotional arousal and social behavior. Little is known about neural mechanisms underlying human personality and temperament, despite their considerable importance as highly heritable risk mediators for somatic and psychiatric disorders. To identify these circuits, we used a combined genetic and imaging approach focused on Monoamine Oxidase A (MAOA), encoding a key enzyme for monoamine metabolism previously associated with temperament and antisocial behavior. Male carriers of a low-expressing genetic variant exhibited dysregulated amygdala activation and increased functional coupling with ventromedial prefrontal cortex (vmPFC). Stronger coupling predicted increased harm avoidance and decreased reward dependence scores, suggesting that this circuitry mediates a part of the association of MAOA with these traits. We utilized path analysis to parse the effective connectivity within this system, and provide evidence that vmPFC regulates amygdala indirectly by influencing rostral cingulate cortex function. Our data implicate a neural circuit for variation in human personality under genetic control, provide an anatomically consistent mechanism for vmPFC-amygdaia interactions underlying this variation, and suggest a role for vmPFC as a superordinate regulatory area for emotional arousal and social behavior. |
| Audience | Academic |
| Author | Callicott, J H Hariri, A R Mattay, V S Kolachana, B Buckholtz, J W Egan, M F Goldberg, T E Genderson, M Meyer-Lindenberg, A Weinberger, D R |
| Author_xml | – sequence: 1 givenname: J W surname: Buckholtz fullname: Buckholtz, J W organization: Neuroimaging Core Facility, National Institute for Mental Health, NIH, DHHS, Clinical Brain Disorders Branch, Genes, Cognition and Psychosis Program, National Institute for Mental Health, NIH, DHHS – sequence: 2 givenname: J H surname: Callicott fullname: Callicott, J H organization: Neuroimaging Core Facility, National Institute for Mental Health, NIH, DHHS, Clinical Brain Disorders Branch, Genes, Cognition and Psychosis Program, National Institute for Mental Health, NIH, DHHS – sequence: 3 givenname: B surname: Kolachana fullname: Kolachana, B organization: Clinical Brain Disorders Branch, Genes, Cognition and Psychosis Program, National Institute for Mental Health, NIH, DHHS – sequence: 4 givenname: A R surname: Hariri fullname: Hariri, A R organization: Clinical Brain Disorders Branch, Genes, Cognition and Psychosis Program, National Institute for Mental Health, NIH, DHHS, 4Current address: Department of Psychiatry, University of Pittsburgh School of Medicine, Western Psychiatric Institute and Clinic, 3811 O'Hara Street, E-729, Pittsburgh, PA 15213, USA – sequence: 5 givenname: T E surname: Goldberg fullname: Goldberg, T E organization: Clinical Brain Disorders Branch, Genes, Cognition and Psychosis Program, National Institute for Mental Health, NIH, DHHS, 5Current address: Division of Psychiatry Research, The Zucker Hillside Hospital, 75-59 263rd Street, Glen Oaks, NY 11004, USA – sequence: 6 givenname: M surname: Genderson fullname: Genderson, M organization: Clinical Brain Disorders Branch, Genes, Cognition and Psychosis Program, National Institute for Mental Health, NIH, DHHS – sequence: 7 givenname: M F surname: Egan fullname: Egan, M F organization: Clinical Brain Disorders Branch, Genes, Cognition and Psychosis Program, National Institute for Mental Health, NIH, DHHS, 6Current address: Merck & Co Inc., BL2-6, PO Box 4, West Point, PA 19486, USA – sequence: 8 givenname: V S surname: Mattay fullname: Mattay, V S organization: Neuroimaging Core Facility, National Institute for Mental Health, NIH, DHHS, Clinical Brain Disorders Branch, Genes, Cognition and Psychosis Program, National Institute for Mental Health, NIH, DHHS – sequence: 9 givenname: D R surname: Weinberger fullname: Weinberger, D R organization: Clinical Brain Disorders Branch, Genes, Cognition and Psychosis Program, National Institute for Mental Health, NIH, DHHS – sequence: 10 givenname: A surname: Meyer-Lindenberg fullname: Meyer-Lindenberg, A email: andreasml@nih.gov organization: Neuroimaging Core Facility, National Institute for Mental Health, NIH, DHHS, Clinical Brain Disorders Branch, Genes, Cognition and Psychosis Program, National Institute for Mental Health, NIH, DHHS, Unit for Systems Neuroscience in Psychiatry, National Institute for Mental Health, NIH, DHHS |
| BackLink | http://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=20119587$$DView record in Pascal Francis https://www.ncbi.nlm.nih.gov/pubmed/17519928$$D View this record in MEDLINE/PubMed |
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| Copyright | Springer Nature Limited 2008 2008 INIST-CNRS COPYRIGHT 2008 Nature Publishing Group Copyright Nature Publishing Group Mar 2008 Nature Publishing Group 2008. |
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| Issue | 3 |
| Keywords | fMRI emotion regulation amygdala functional connectivity antisocial effective connectivity cingulate Affect affectivity Genetic variability Amygdala Central nervous system Genetic determinism Encephalon Cingulate cortex Genetics Amygdaloid nucleus Human Antisocial behavior Basal ganglion Emotion emotionality Personality Prefrontal cortex Nuclear magnetic resonance imaging Interindividual comparison Medical imagery Self regulation Social behavior disorder Functional imaging |
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| PublicationTitle | Molecular psychiatry |
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| PublicationYear | 2008 |
| Publisher | Nature Publishing Group UK Nature Publishing Group |
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| SubjectTerms | Adult Amine oxidase (flavin-containing) Amygdala Amygdala (Brain) Antisocial personality disorder Arousal Behavioral Sciences Biological and medical sciences Biological Psychology Brain Mapping Brain research Cortex (cingulate) Emotion regulation Emotional behavior Evaluation Facial Expression Female Genes Genetic aspects Genetic control Genetic diversity Genetic Variation Health aspects Humans Image Processing, Computer-Assisted Individuality Influence Magnetic Resonance Imaging Male Medical sciences Medicine Medicine & Public Health Mental disorders Mental health Models, Biological Monoamine oxidase Monoamine Oxidase - genetics Neural circuitry Neural Pathways - blood supply Neural Pathways - physiology Neuroimaging Neuropsychological Tests Neurosciences original-article Oxygen - blood Personality Personality - genetics Personality tests Personality traits Pharmacotherapy Photic Stimulation - methods Physiological aspects Prefrontal cortex Prefrontal Cortex - blood supply Prefrontal Cortex - physiology Properties Psychiatry Psychology. Psychoanalysis. Psychiatry Psychopathology. Psychiatry Psychosis Reinforcement Serotonin Social behavior |
| Title | Genetic variation in MAOA modulates ventromedial prefrontal circuitry mediating individual differences in human personality |
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