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Fear conditioning, persistence of disruptive behavior and psychopathic traits: an fMRI study.

Cohn MD, Popma A, van den Brink W, Pape LE, Kindt M, van Domburgh L, Doreleijers TA, Veltman DJ - Transl Psychiatry (2013)

Bottom Line: Both persistent and desistent DBD subgroups were found to show higher activation in fear processing-related brain areas during fear conditioning compared with healthy controls.In addition, regression analyses revealed that impulsive-irresponsible and grandiose-manipulative psychopathic traits were associated with higher activation, whereas callous-unemotional psychopathic traits were related to lower activation in fear-related areas.Finally, the association between neural activation and DBD subgroup membership was mediated by impulsive-irresponsible psychopathic traits.

View Article: PubMed Central - PubMed

Affiliation: Department of Child and Adolescent Psychiatry, VU University Medical Center, Amsterdam, The Netherlands.

ABSTRACT
Children diagnosed with Disruptive Behavior Disorders (DBD), especially those with psychopathic traits, are at risk of developing persistent and severe antisocial behavior. Deficient fear conditioning may be a key mechanism underlying persistence, and has been associated with altered regional brain function in adult antisocial populations. In this study, we investigated the associations between the neural correlates of fear conditioning, persistence of childhood-onset DBD during adolescence and psychopathic traits. From a cohort of children arrested before the age of 12 years, participants who were diagnosed with Oppositional Defiant Disorder or Conduct Disorder in previous waves (mean age of onset 6.5 years, s.d. 3.2) were reassessed at mean age 17.6 years (s.d. 1.4) and categorized as persistent (n=25) or desistent (n=25) DBD. Using the Youth Psychopathic Traits Inventory and functional magnetic resonance imaging during a fear conditioning task, these subgroups were compared with 26 matched healthy controls from the same cohort. Both persistent and desistent DBD subgroups were found to show higher activation in fear processing-related brain areas during fear conditioning compared with healthy controls. In addition, regression analyses revealed that impulsive-irresponsible and grandiose-manipulative psychopathic traits were associated with higher activation, whereas callous-unemotional psychopathic traits were related to lower activation in fear-related areas. Finally, the association between neural activation and DBD subgroup membership was mediated by impulsive-irresponsible psychopathic traits. These results provide evidence for heterogeneity in the neurobiological mechanisms underlying psychopathic traits and antisocial behavior and, as such, underscore the need to develop personalized interventions.

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Association between differential neural fear conditioning responses (CS+>CS− contrast) and Youth Psychopathic traits Inventory (YPI) impulsive-irresponsible traits (left; positive association), and callous-unemotional traits (right; negative association). Single dimension regression analysis effects (red), unique effects (green; i.e. corrected for the other psychopathy dimensions in a multiple regression analysis) and their overlap (yellow) are displayed at P<0.001, k⩾10 uncorrected for display purposes, and are overlaid on an anatomical template. CS, conditioned stimuli.
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fig1: Association between differential neural fear conditioning responses (CS+>CS− contrast) and Youth Psychopathic traits Inventory (YPI) impulsive-irresponsible traits (left; positive association), and callous-unemotional traits (right; negative association). Single dimension regression analysis effects (red), unique effects (green; i.e. corrected for the other psychopathy dimensions in a multiple regression analysis) and their overlap (yellow) are displayed at P<0.001, k⩾10 uncorrected for display purposes, and are overlaid on an anatomical template. CS, conditioned stimuli.

Mentions: Regression analyses showed that higher levels of II traits were associated with higher activation in the right insula as well as in the left and right ACC. When all dimensions were entered into a multiple regression model, both GM and II traits were associated with higher activation. In contrast, CU traits were associated with lower levels of activation. This effect was significant at P<0.05 (whole-brain FWE-corrected) in the ACC, and was present at a lower statistical threshold throughout the fear conditioning network (see Table 3 and Figures 1 and 2). Post hoc exclusion of an outlier with respect to differential activation in the ACC (visible in Figure 2) slightly reduced the effect size of the latter CU traits result (from peak voxel partial r=0.57 to partial r=0.50, uncorrected P<0.001, PFWE=0.095) and increased the effect of the II trait result (from peak voxel partial r=0.33 to partial r=0.38, uncorrected P<0.001, PFWE=0.005). All between-group effects remained significant after exclusion of this outlier. Psychopathic traits' dimensions were unrelated to neural activation to the US.


Fear conditioning, persistence of disruptive behavior and psychopathic traits: an fMRI study.

Cohn MD, Popma A, van den Brink W, Pape LE, Kindt M, van Domburgh L, Doreleijers TA, Veltman DJ - Transl Psychiatry (2013)

Association between differential neural fear conditioning responses (CS+>CS− contrast) and Youth Psychopathic traits Inventory (YPI) impulsive-irresponsible traits (left; positive association), and callous-unemotional traits (right; negative association). Single dimension regression analysis effects (red), unique effects (green; i.e. corrected for the other psychopathy dimensions in a multiple regression analysis) and their overlap (yellow) are displayed at P<0.001, k⩾10 uncorrected for display purposes, and are overlaid on an anatomical template. CS, conditioned stimuli.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3818535&req=5

fig1: Association between differential neural fear conditioning responses (CS+>CS− contrast) and Youth Psychopathic traits Inventory (YPI) impulsive-irresponsible traits (left; positive association), and callous-unemotional traits (right; negative association). Single dimension regression analysis effects (red), unique effects (green; i.e. corrected for the other psychopathy dimensions in a multiple regression analysis) and their overlap (yellow) are displayed at P<0.001, k⩾10 uncorrected for display purposes, and are overlaid on an anatomical template. CS, conditioned stimuli.
Mentions: Regression analyses showed that higher levels of II traits were associated with higher activation in the right insula as well as in the left and right ACC. When all dimensions were entered into a multiple regression model, both GM and II traits were associated with higher activation. In contrast, CU traits were associated with lower levels of activation. This effect was significant at P<0.05 (whole-brain FWE-corrected) in the ACC, and was present at a lower statistical threshold throughout the fear conditioning network (see Table 3 and Figures 1 and 2). Post hoc exclusion of an outlier with respect to differential activation in the ACC (visible in Figure 2) slightly reduced the effect size of the latter CU traits result (from peak voxel partial r=0.57 to partial r=0.50, uncorrected P<0.001, PFWE=0.095) and increased the effect of the II trait result (from peak voxel partial r=0.33 to partial r=0.38, uncorrected P<0.001, PFWE=0.005). All between-group effects remained significant after exclusion of this outlier. Psychopathic traits' dimensions were unrelated to neural activation to the US.

Bottom Line: Both persistent and desistent DBD subgroups were found to show higher activation in fear processing-related brain areas during fear conditioning compared with healthy controls.In addition, regression analyses revealed that impulsive-irresponsible and grandiose-manipulative psychopathic traits were associated with higher activation, whereas callous-unemotional psychopathic traits were related to lower activation in fear-related areas.Finally, the association between neural activation and DBD subgroup membership was mediated by impulsive-irresponsible psychopathic traits.

View Article: PubMed Central - PubMed

Affiliation: Department of Child and Adolescent Psychiatry, VU University Medical Center, Amsterdam, The Netherlands.

ABSTRACT
Children diagnosed with Disruptive Behavior Disorders (DBD), especially those with psychopathic traits, are at risk of developing persistent and severe antisocial behavior. Deficient fear conditioning may be a key mechanism underlying persistence, and has been associated with altered regional brain function in adult antisocial populations. In this study, we investigated the associations between the neural correlates of fear conditioning, persistence of childhood-onset DBD during adolescence and psychopathic traits. From a cohort of children arrested before the age of 12 years, participants who were diagnosed with Oppositional Defiant Disorder or Conduct Disorder in previous waves (mean age of onset 6.5 years, s.d. 3.2) were reassessed at mean age 17.6 years (s.d. 1.4) and categorized as persistent (n=25) or desistent (n=25) DBD. Using the Youth Psychopathic Traits Inventory and functional magnetic resonance imaging during a fear conditioning task, these subgroups were compared with 26 matched healthy controls from the same cohort. Both persistent and desistent DBD subgroups were found to show higher activation in fear processing-related brain areas during fear conditioning compared with healthy controls. In addition, regression analyses revealed that impulsive-irresponsible and grandiose-manipulative psychopathic traits were associated with higher activation, whereas callous-unemotional psychopathic traits were related to lower activation in fear-related areas. Finally, the association between neural activation and DBD subgroup membership was mediated by impulsive-irresponsible psychopathic traits. These results provide evidence for heterogeneity in the neurobiological mechanisms underlying psychopathic traits and antisocial behavior and, as such, underscore the need to develop personalized interventions.

Show MeSH
Related in: MedlinePlus