Prefrontal regional correlates of self-control in male psychiatric patients: Impulsivity facets and aggression

Investigating the organization of trait aggression and impulsivity in the prefrontal cortex (PFC) advances our understanding of the neuropsychobiology of self-control. While the orbital aspect of the PFC (OFC) has received attention, there is reason to believe the lateral aspect is also relevant. In the current study using magnetic resonance imaging, gray matter volumes in lateral PFC (LPFC) were derived in a heterogeneous male psychiatric sample (N=36) in which OFC volumes had previously been reported. In an analysis using self-report measures of trait impulsivity and aggression, the left LPFC accounted for significant variance in attentional aspects of impulsivity (13%) and aggression (10%) but not motor aspects of impulsivity, as hypothesized. The OFC was associated with motor impulsivity (left-20%; right-14%) and was also more robustly associated with aggression (left-36%; right-16%). A social/emotional information processing model was explored, based upon whether the LPFC or the OFC depended upon one another for their association to trait aggression and impulsivity. It was demonstrated that association of the LPFC to both aggression and attentional impulsivity depended upon the OFC, while the converse was not supported. The LPFC appears relevant to the higher-order aspects of a cortical self-control network, and that relevance is dependent upon the robust contribution of the OFC.

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

[2]  L. Passamonti,et al.  Monoamine Oxidase-A Genetic Variations Influence Brain Activity Associated with Inhibitory Control: New Insight into the Neural Correlates of Impulsivity , 2006, Biological Psychiatry.

[3]  H. Barbas,et al.  Sequential and parallel circuits for emotional processing in primate orbitofrontal cortex , 2006 .

[4]  E. Murray,et al.  The amygdala and reward , 2002, Nature Reviews Neuroscience.

[5]  Hoi-Chung Leung,et al.  Functional architecture of the dorsolateral prefrontal cortex in monkeys and humans , 2002 .

[6]  A. Hariri,et al.  Preference for Immediate over Delayed Rewards Is Associated with Magnitude of Ventral Striatal Activity , 2006, The Journal of Neuroscience.

[7]  A. Damasio,et al.  Emotion, decision making and the orbitofrontal cortex. , 2000, Cerebral cortex.

[8]  Matcheri S. Keshavan,et al.  Disruption of Orbitofrontal Cortex Laterality in Offspring from Multiplex Alcohol Dependence Families , 2009, Biological Psychiatry.

[9]  J. Fuster Prefrontal Cortex , 2018 .

[10]  E T Rolls,et al.  Impulsivity, time perception, emotion and reinforcement sensitivity in patients with orbitofrontal cortex lesions. , 2004, Brain : a journal of neurology.

[11]  A. Zeichner,et al.  Neuropsychological performance on tests of frontal-lobe functioning and aggressive behavior in men. , 1994, Journal of abnormal psychology.

[12]  Joseph E LeDoux Synaptic Self: How Our Brains Become Who We Are , 2002 .

[13]  J. Monahan,et al.  Developing a clinically useful actuarial tool for assessing violence risk , 2000, British Journal of Psychiatry.

[14]  Niels Birbaumer,et al.  Evidence for a different role of the ventral and dorsal medial prefrontal cortex for social reactive aggression: An interactive fMRI study , 2007, NeuroImage.

[15]  P. Nopoulos,et al.  Right anterior cingulate: a neuroanatomical correlate of aggression and defiance in boys. , 2008, Behavioral neuroscience.

[16]  Robert T. Knight,et al.  Prefrontal cortex: the present and the future , 2002 .

[17]  D D Blatter,et al.  Quantitative volumetric analysis of brain MR: normative database spanning 5 decades of life. , 1995, AJNR. American journal of neuroradiology.

[18]  B. Thompson,et al.  MR imaging of head trauma: review of the distribution and radiopathologic features of traumatic lesions. , 1988, AJR. American journal of roentgenology.

[19]  Acioly L. T Lacerda,et al.  Measurement of the orbitofrontal cortex: a validation study of a new method , 2003, NeuroImage.

[20]  G. Schwartz,et al.  Consciousness and Self-Regulation , 1976 .

[21]  J. Lucas,et al.  Decision making in alcohol dependence: insensitivity to future consequences and comorbid disinhibitory psychopathology. , 2008, Alcoholism, clinical and experimental research.

[22]  Deborah A Yurgelun-Todd,et al.  Sex differences in the relationship between white matter microstructure and impulsivity in adolescents. , 2006, Magnetic resonance imaging.

[23]  A. Toga,et al.  Localization of deformations within the amygdala in individuals with psychopathy. , 2009, Archives of general psychiatry.

[24]  R. Robinson,et al.  Clinical correlates of aggressive behavior after traumatic brain injury. , 2003, The Journal of neuropsychiatry and clinical neurosciences.

[25]  E. Barratt,et al.  Defining, measuring, and predicting impulsive aggression: a heuristic model. , 1998, Behavioral sciences & the law.

[26]  David M. Amodio,et al.  Implicit regulatory focus associated with asymmetrical frontal cortical activity. , 2004 .

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

[28]  R. Davidson,et al.  Dysfunction in the neural circuitry of emotion regulation--a possible prelude to violence. , 2000, Science.

[29]  Richard E. Tremblay,et al.  Eysenck’s personality dimensions as predictors of male adolescent trajectories of physical aggression, theft and vandalism , 2006 .

[30]  Jin Fan,et al.  Neural Correlates of the Use of Psychological Distancing to Regulate Responses to Negative Social Cues: A Study of Patients with Borderline Personality Disorder , 2009, Biological Psychiatry.

[31]  M. Jerram,et al.  A multivariate approach to aggression and the orbital frontal cortex in psychiatric patients , 2009, Psychiatry Research: Neuroimaging.

[32]  M. Stanford,et al.  Characterizing Aggressive Behavior , 2003, Assessment.

[33]  Stephan Hamann,et al.  Neuroticism and psychopathy predict brain activation during moral and nonmoral emotion regulation , 2009, Cognitive, affective & behavioral neuroscience.

[34]  Samuel M. McClure,et al.  Separate Neural Systems Value Immediate and Delayed Monetary Rewards , 2004, Science.

[35]  A. Raine,et al.  Reduced prefrontal gray matter volume and reduced autonomic activity in antisocial personality disorder. , 2000, Archives of general psychiatry.

[36]  B. Price,et al.  Neuropsychiatry of frontal lobe dysfunction in violent and criminal behaviour: a critical review , 2001, Journal of neurology, neurosurgery, and psychiatry.

[37]  E. Barratt,et al.  Impulsivity and BOLD fMRI activation in MDMA users and healthy control subjects , 2006, Psychiatry Research: Neuroimaging.

[38]  Jens C. Pruessner,et al.  Regional Frontal Cortical Volumes Decrease Differentially in Aging: An MRI Study to Compare Volumetric Approaches and Voxel-Based Morphometry , 2002, NeuroImage.

[39]  T. Sharma,et al.  Volumetric structural brain abnormalities in men with schizophrenia or antisocial personality disorder , 2006, Behavioural Brain Research.

[40]  Edmund T. Rolls,et al.  The functions of the orbitofrontal cortex , 1999 .

[41]  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.

[42]  E. Coccaro,et al.  Assessment of life history of aggression: development and psychometric characteristics , 1997, Psychiatry Research.

[43]  Daniel S. O'Leary,et al.  Human Frontal Cortex: An MRI-Based Parcellation Method , 1999, NeuroImage.

[44]  J. Grafman,et al.  Frontal lobe injuries, violence, and aggression , 1996, Neurology.

[45]  R. Blair The amygdala and ventromedial prefrontal cortex in morality and psychopathy , 2007, Trends in Cognitive Sciences.

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

[47]  R. Elliott,et al.  Serotonergic modulation of neuronal responses to behavioural inhibition and reinforcing stimuli: an fMRI study in healthy volunteers , 2006, The European journal of neuroscience.

[48]  D. Stuss,et al.  Principles of frontal lobe function , 2002 .

[49]  E. Rolls,et al.  The Orbitofrontal Cortex , 2019 .

[50]  A. Bechara Decision making, impulse control and loss of willpower to resist drugs: a neurocognitive perspective , 2005, Nature Neuroscience.

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

[52]  Hu Cheng,et al.  Neural correlates of emotion processing in borderline personality disorder , 2009, Psychiatry Research: Neuroimaging.

[53]  M. Preul The Human Brain: Surface, Blood Supply, and Three-Dimensional Sectional Anatomy , 2001 .

[54]  L. Siever Neurobiology of aggression and violence. , 2008, The American journal of psychiatry.

[55]  Y. Okamoto,et al.  Negative correlation between right prefrontal activity during response inhibition and impulsiveness: A fMRI study , 2004, European Archives of Psychiatry and Clinical Neuroscience.

[56]  M. Trimble,et al.  Dual brain pathology in patients with affective aggressive episodes. , 2001, Archives of general psychiatry.