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Research ArticleNew Research, Cognition and Behavior

Testosterone Modulates Altered Prefrontal Control of Emotional Actions in Psychopathic Offenders

Inge Volman, Anna Katinka Louise von Borries, Berend Hendrik Bulten, Robbert Jan Verkes, Ivan Toni and Karin Roelofs
eNeuro 15 January 2016, 3 (1) ENEURO.0107-15.2016; DOI: https://doi.org/10.1523/ENEURO.0107-15.2016
Inge Volman
1Sobell Department of Motor Neuroscience and Movement Disorders, UCL Institute of Neurology, University College London, London WC1N 3BG, United Kingdom
2Behavioural Science Institute, Radboud University Nijmegen, 6525 HR, Nijmegen, The Netherlands
3Donders Institute for Brain, Cognition and Behavior, Radboud University Nijmegen, 6525 EN, Nijmegen, The Netherlands
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  • ORCID record for Inge Volman
Anna Katinka Louise von Borries
2Behavioural Science Institute, Radboud University Nijmegen, 6525 HR, Nijmegen, The Netherlands
3Donders Institute for Brain, Cognition and Behavior, Radboud University Nijmegen, 6525 EN, Nijmegen, The Netherlands
4Department of Psychiatry, UMC Sint Radboud, 6525 GA, Nijmegen, The Netherlands
5Pompestichting, 6532 CN, Nijmegen, The Netherlands
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Berend Hendrik Bulten
5Pompestichting, 6532 CN, Nijmegen, The Netherlands
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Robbert Jan Verkes
3Donders Institute for Brain, Cognition and Behavior, Radboud University Nijmegen, 6525 EN, Nijmegen, The Netherlands
4Department of Psychiatry, UMC Sint Radboud, 6525 GA, Nijmegen, The Netherlands
5Pompestichting, 6532 CN, Nijmegen, The Netherlands
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Ivan Toni
3Donders Institute for Brain, Cognition and Behavior, Radboud University Nijmegen, 6525 EN, Nijmegen, The Netherlands
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Karin Roelofs
2Behavioural Science Institute, Radboud University Nijmegen, 6525 HR, Nijmegen, The Netherlands
3Donders Institute for Brain, Cognition and Behavior, Radboud University Nijmegen, 6525 EN, Nijmegen, The Netherlands
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  • Figure 1.
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    Figure 1.

    The emotional control AA task. The AA task involved the presentation of happy and angry faces, and the performance of approach and avoidance responses. During the AA task, the participants had to select their response according to the perceived emotion of the face. At the beginning of each block of 12 trials, the participants received instructions on whether to pull the joystick toward themselves (approach) or push it away (avoid) when seeing a face with a particular emotion. When viewing happy or angry faces, automatic stimulus–response tendencies trigger corresponding approach or avoidance actions. These tendencies could be followed during the affect-congruent condition (approach–happy, avoid–angry). In contrast, when task instructions required participants to avoid happy faces or to approach angry faces, automatic tendencies needed to be controlled and overridden with the instructed response (affect-incongruent condition). Participants saw the faces and moved the joystick while lying in a MR scanner (top left corner of the table). Figure adapted from Volman et al. (2011a, 2013).

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    Figure 2.

    Behavioral results. Mean RTs (±SEM) for the affect-congruent and affect-incongruent conditions of the AA task for the healthy control subjects and psychopathic offenders. The groups were significantly slower to provide affect-incongruent responses (approach–angry; avoid–happy) than affect-congruent responses (approach–happy; avoid–angry), with no significant group differences.

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    Figure 3.

    Testosterone modulations of the cerebral congruency effect in psychopathic offenders and healthy control subjects. A, D, Brain image showing testosterone-modulated congruency effects (affect-incongruent−affect-congruent) in the psychopathic offenders in the bilateral aPFC (A) and right supramarginal gyrus (D). B, E, Bar graphs showing the mean activation (±SEM) of the active voxels within the yellow circles per group. *pFWE < 0.05. ns, Not significant. C, F, Scatterplots showing the correlation of the mean activation of active voxels within the yellow circles with testosterone (log-transformed and standardized) for the healthy control group and the psychopathy group. The ROI activations are presented at p < 0.05, uncorrected for visualization purposes. There are no outliers [Mahalanobis distances D 2i < 4.2 (cutoff at p < 0.05; D = 7.74); Barnett and Lewis, 1978; Stevens, 1996]. Healthy control subjects show an increased aPFC activity for the congruency effect and no modulation by testosterone, while in psychopathic offenders endogenous testosterone levels modulate the activity of the aPFC and right supramarginal gyrus.

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    Figure 4.

    Group difference on congruency-related aPFC–amygdala connectivity. A, Brain images illustrating the congruency-related modulation of connectivity between the right aPFC (yellow circle, axial slice) and the right amygdala (coronal slice) for the congruency contrast. The activations are presented at p < 0.05, uncorrected for visualization purposes. B, Bar graph visualizing the strength of the congruency-specific change (±SEM) in aPFC–amygdala connectivity for the healthy control subjects and psychopathic offenders. There is a significant negative aPFC–amygdala coupling in the healthy control subjects, which is not present in the psychopathic offenders.

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    Table 1:

    Demographical data

    Psychopathic offenders
    (n = 15)
    HCs
    (n = 19)
    p value
    Age37.8 (7.9)40.7 (10.3)0.368
    IQ101 (10)102 (9)0.761
    Handedness50.7 (81)59.2 (62)0.729
    PCL-R total30.4 (3.5)
    PCL-R F112.1 (2.6)
    PCL-R F214.1 (2.3)
    • Values are presented as the mean (SD), unless otherwise indicated. F1, factor 1; F2, factor 2.

    • View popup
    Table 2:

    RTs and error rates for each group and factor of the AA task

    Psychopathic offendersHCs
    ApproachAvoidApproachAvoid
    Errors (%)
    Happy3.2 (0.9)8.9 (1.8)2.4 (0.8)7.7 (1.1)
    Neutral6.1 (1.3)5.8 (1.1)7.1 (1.4)5.2 (1.0)
    Angry10.1 (2.2)13.1 (2.1)9.6 (1.8)11.6 (1.8)
    RT (ms)
    Happy554 (25)625 (35)553 (23)603 (25)
    Neutral666 (28)687 (31)639 (21)668 (24)
    Angry630 (25)665 (33)620 (24)630 (23)
    • Values are presented as the mean (SE).

    • View popup
    Table 3:

    Clusters showing significantly larger activity for the affect-incongruent vs the affect-congruent conditions (emotion-control effect)

    Anatomical regionPutative BASidexyzVoxels (n)p valuet value
    Whole-brain effects
    Congruency effect over groups
    Cuneus18R/L−16−9624634<0.0014.85
    SPL/Superior occipital gyrus7/19L−30−76342540.0044.37
    IFG45/47L−5222−102230.0074.37
    Cuneus18R18−98161900.0164.52
    Congruency effect for psychopathy group
    SPL/superior occipital gyrus7/19R/L8−8238925<0.0014.98
    Angular gyrus39/19L−30−72343370.0014.35
    Superior temporal gyrus42L−32−3262140.0094.51
    SPL7R28−74461580.0344.58
    CerebellumL−24−66−381460.0464.63
    Negative testosterone modulation of group (psychopathic offenders > healthy control subjects) × congruency interaction
    aPFC10R305812391<0.0015.10
    Supramarginal gyrus40R54−42543250.0014.66
    Caudate nucleusR101022730.0024.69
    Putamen/InsulaL−346−101760.0225.22
    CerebellumR18−76−381880.0165.09
    Negative testosterone modulation of Congruency effect in psychopathy
    Supramarginal gyrus40R52−4054657<0.0015.32
    Precentral/superior frontal gyrus6R/L62266471<0.0015.65
    Caudate nucleusR6642280.0064.28
    VOI on bilateral aPFC
    Congruency effect over groups10R305814310.0014.46
    10L−30581050.0363.43
    Congruency effect in healthy control subjects10R325814120.0014.58
    10L−3452420.0403.40
    Negative testosterone modulation of group (psychopathic offenders > healthy control subjects) × congruency interaction10R305812145<0.0015.10
    10L−24566150.0103.87
    Negative testosterone modulation of congruency effect in psychopathy10R325610770.0024.34
    10L−30588170.0153.74
    • Coordinates are defined in MNI (x, y, z) space. The p values represent the FWE cluster-level corrected values for the whole-brain analyses and FWE voxel-level corrected values for the VOI analyses. IFG, Inferior frontal gyrus; L, left; R, right; SPL, superior parietal lobule.

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Testosterone Modulates Altered Prefrontal Control of Emotional Actions in Psychopathic Offenders
Inge Volman, Anna Katinka Louise von Borries, Berend Hendrik Bulten, Robbert Jan Verkes, Ivan Toni, Karin Roelofs
eNeuro 15 January 2016, 3 (1) ENEURO.0107-15.2016; DOI: 10.1523/ENEURO.0107-15.2016

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Testosterone Modulates Altered Prefrontal Control of Emotional Actions in Psychopathic Offenders
Inge Volman, Anna Katinka Louise von Borries, Berend Hendrik Bulten, Robbert Jan Verkes, Ivan Toni, Karin Roelofs
eNeuro 15 January 2016, 3 (1) ENEURO.0107-15.2016; DOI: 10.1523/ENEURO.0107-15.2016
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Keywords

  • amygdala
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