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Articles, Behavioral/Cognitive

Testosterone during Puberty Shifts Emotional Control from Pulvinar to Anterior Prefrontal Cortex

Anna Tyborowska, Inge Volman, Sanny Smeekens, Ivan Toni and Karin Roelofs
Journal of Neuroscience 8 June 2016, 36 (23) 6156-6164; DOI: https://doi.org/10.1523/JNEUROSCI.3874-15.2016
Anna Tyborowska
1Behavioural Science Institute, Radboud University Nijmegen, 6525 HR Nijmegen, The Netherlands,
2Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, 6525 EN Nijmegen, The Netherlands, and
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Inge Volman
1Behavioural Science Institute, Radboud University Nijmegen, 6525 HR Nijmegen, The Netherlands,
2Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, 6525 EN Nijmegen, The Netherlands, and
3Sobell Department of Motor Neuroscience and Movement Disorders, UCL Institute of Neurology, University College London, London WC1E 6BT, United Kingdom
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Sanny Smeekens
1Behavioural Science Institute, Radboud University Nijmegen, 6525 HR Nijmegen, The Netherlands,
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Ivan Toni
2Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, 6525 EN Nijmegen, The Netherlands, and
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Karin Roelofs
1Behavioural Science Institute, Radboud University Nijmegen, 6525 HR Nijmegen, The Netherlands,
2Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, 6525 EN Nijmegen, The Netherlands, and
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  • Figure 1.
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    Figure 1.

    Approach-avoidance task (Volman et al., 2011a, 2013). The response action to an emotional face is associated with an approach (pull toward) or avoidance (pull away) movement and can be either congruent or incongruent with the automatic tendency elicited by the face. Affect-congruent conditions (approach–happy, avoid–angry) overlap with the automatic tendency to approach something positive and avoid something negative. However, during affect-incongruent conditions these emotional tendencies need to be controlled to perform the opposite action (avoid-happy, approach-angry).

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    Figure 2.

    Cerebral distribution of significant testosterone-modulated congruency effects (incongruent > congruent trials) across the sample of 47 participants. a–c, BOLD congruency effects decreased as testosterone levels increased in the thalamus (a; pFWE < 0.05) and in the amygdala (b; SVC pFWE < 0.05). BOLD congruency effects increased as testosterone levels increased in the aPFC (c; SVC pFWE < 0.05). d, Mean-adjusted BOLD congruency effects (incongruent > congruent) in the aPFC (green) and pulvinar (blue) as a function of testosterone level (as an indicator of pubertal status). Dots represent the effect size of the congruency effect of each participant.

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    Figure 3.

    a, b, Functional coupling between the amygdala and pulvinar (a) changed as a function of performance (b). Individuals with higher testosterone levels had stronger positive coupling between the amygdala and pulvinar, as a function of increasing error rate (incongruent vs congruent trials; SVC pFWE = 0.043). The scatterplot illustrates mean-adjusted congruency-related modulation of amygdala–pulvinar connectivity as a function of error rate, separately for high-testosterone (in green) and low-testosterone participants (in blue).

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    Table 1.

    Demographic information: testosterone levels, PDS, and age per gender

    Testosterone T1 (pg/ml)Testosterone T2 (pg/ml)PDS scoreAge (years)
    Boys39.4 (31.53)42.2 (24.77)2.4 (0.63)14.55 (0.10)
    Girls10.7 (6.28)11.66 (9.25)2.6 (1.02)14.61 (0.18)
    • Values represent the mean (SD). Testosterone T1 and T2 represent the first and second salivary measurement (respectively). Testosterone values between the first and second measurement did not differ significantly either for boys (t(19) = −0.99, p = 0.333) or girls (t(25) = −0.66, p = 0.514). Testosterone T1 levels were used for subsequent analyses.

    • View popup
    Table 2.

    Reaction times and error rates in the AA task for approach and avoidance movements in response to happy and angry faces

    ApproachAvoid
    RT (ms)
        Happy622 (16)679 (16)
        Angry673 (19)679 (17)
    ER (%)
        Happy6.4 (0.5)8.4 (0.9)
        Angry8.7 (1.2)6.7 (0.8)
    • Values indicate mean (SE) across participants.

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    Table 3.

    Significant clusters showing a larger effect during affect-incongruent than affect-congruent trials in the approach avoidance task modulated by testosterone

    Anatomical regionSideBAkMNI coordinatespt
    xyz
    Positive testosterone modulation of congruency effect
        aPFC/mid frontal orbitalR10/46334058−60.04a3.55
    Negative testosterone modulation of congruency effect
        Dorsomedial thalamus/pulvinarL626−8−2016<0.0015.39
        Anterior thalamus/caudate nucleusR
        HippocampusL37272−38−34−20.0136.56
        Precentral sulcus/SFSR619620−8500.0464.91
        AmygdalaR341426−2−140.026a3.87
    • BA, Brodmann Area; k, number of voxels in a cluster; p, FWE-corrected cluster-level value; t, t-statistic at the peak voxel; R, right; L, left; SFS, superior frontal sulcus.

    • ↵aSVC over anatomically defined ROI.

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The Journal of Neuroscience: 36 (23)
Journal of Neuroscience
Vol. 36, Issue 23
8 Jun 2016
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Testosterone during Puberty Shifts Emotional Control from Pulvinar to Anterior Prefrontal Cortex
Anna Tyborowska, Inge Volman, Sanny Smeekens, Ivan Toni, Karin Roelofs
Journal of Neuroscience 8 June 2016, 36 (23) 6156-6164; DOI: 10.1523/JNEUROSCI.3874-15.2016

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Testosterone during Puberty Shifts Emotional Control from Pulvinar to Anterior Prefrontal Cortex
Anna Tyborowska, Inge Volman, Sanny Smeekens, Ivan Toni, Karin Roelofs
Journal of Neuroscience 8 June 2016, 36 (23) 6156-6164; DOI: 10.1523/JNEUROSCI.3874-15.2016
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Keywords

  • adolescence
  • approach-avoidance task
  • fMRI
  • frontal pole
  • hormones
  • thalamus

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