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Research ArticleNew Research, Cognition and Behavior

Avoidant Responses to Interpersonal Provocation Are Associated with Increased Amygdala and Decreased Mentalizing Network Activity

Macià Buades-Rotger, Frederike Beyer and Ulrike M. Krämer
eNeuro 26 June 2017, 4 (3) ENEURO.0337-16.2017; DOI: https://doi.org/10.1523/ENEURO.0337-16.2017
Macià Buades-Rotger
1Department of Neurology, University of Lübeck, Lübeck 23562, Germany
2Institute of Psychology II, University of Lübeck, Lübeck 23562, Germany
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Frederike Beyer
3Institute of Cognitive Neuroscience, University College London, London WC1N 3AR, United Kingdom
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Ulrike M. Krämer
1Department of Neurology, University of Lübeck, Lübeck 23562, Germany
2Institute of Psychology II, University of Lübeck, Lübeck 23562, Germany
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    Figure 1.

    Example trials of the FOE paradigm. Participants confronted a HP and a LP opponent alternatingly. In the escape phase, they could choose whether to fight (upper row) or avoid the encounter (lower row). Fighting led to the punishment selection phase, followed by a reaction time task in which they had to press any button faster than their alleged opponent. In the outcome phase, participants were informed of whether they won or lost and, in the latter case, received the corresponding sound blast through the headphones. If they chose to avoid the trial, they had a short pause. Avoidance decisions were limited to 5 out of 20 trials per run (three runs in total). The fixation cross is only depicted for the avoidance trial, but appeared between all trials regardless of the participant’s decision. For details, see Materials and Methods.

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    Figure 2.

    A, Cumulative proportion of participants who used all avoidance options in each trial. B, Mean avoidance by run and provocation. C, Mean aggression by run and provocation. D, Reaction times in the escape phase by decision and provocation. E, HR results in the selection phase by provocation. All values in this figure are mean ± SE. *p < .05, **p < .01, ***p < .001.

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    Figure 3.

    A, Avoid > fight contrast. Avoid decisions were linked with activation in regions such as the medial frontal gyrus (mPFC), the TPJ, the PCC extending into the ventral precuneus, and the right IFG. B, Fight > avoid contrast. Fight decisions were associated with increased activation in bilateral somatomotor cortex, OFC, ventral thalamus, and dorsal precuneus. Statistical parametric maps are thresholded and presented at p < 0.001, pFWE < 0.05 cluster-level corrected; N = 27.

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    Figure 4.

    Avoid high > avoid low: fight low > fight high contrast. A, Amygdala (Amy), precuneus (Prec), cuneus, and posterior cerebellar clusters. Statistical parametric maps are thresholded and presented at p < 0.001, pFWE < 0.05 cluster-level corrected. B, Contrast values by decision and provocation in basolateral amygdala (above) and precuneus (below). Values are mean ± SE within a 7.5 mm sphere around the local peak; N = 27.

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    Figure 5.

    Avoid low > avoid high: fight high > fight low. A, Clusters in sgACC extending into the rostral mPFC, in TPJ, and in IFG. Statistical parametric maps are thresholded and presented at p < 0.001, pFWE < 0.05 cluster-level corrected. B, Contrast values by decision and provocation in mPFC (above), IFG (below left), and TPJ (below right). Values are mean ± SE within a 7.5 mm sphere around the local peak; N = 27.

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    Figure 6.

    A, High > low provocation contrast in the punishment selection phase. High provocation elicited activation in PAG extending to the ventral thalamus, precuneus, supplementary motor area (SMA), TPJ, and IFG among others. B, Contrast values by provocation in the PAG. Values are mean ± SE within a 7.5 mm sphere around the local peak. C, Won > lost contrast in the outcome phase. Winning was associated with activity in VS, middle frontal and inferior occipital areas among others. D, Lost > won contrast in the outcome phase. Losing was related to activity in AI, superior temporal gyrus, and lingual gyrus among other regions. Statistical parametric maps are thresholded and presented at p < 0.001, pFWE < 0.05 cluster-level corrected; N = 36.

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    Table 1.

    Brain activity in the escape phase

    Region/contrastkPeak Txyz
    a) Avoid > fight
    Superior temporal gyrus101829.6365.5−49.520
    9.4950.5−4220
    9.2358−5210
    IFG3226.43632312.5
    5.4255.525.55
    4.8450.540.512.5
    Middle frontal gyrus10676.2925.525.537.5
    Superior frontal gyrus5.88185340
    Medial frontal gyrus5.850.5587.5
    b) Fight > avoid
    Superior frontal gyrus985610.09−22−265
    9.6928−757.5
    Supplementary motor area9.60−710.545
    Anterior cerebellum1937.8130.5−52−32.5
    5.5520.5−54.5−22.5
    Precuneus2767.4318−6755
    Ventral thalamus1566.06−9.5−172.5
    4.220.5−29.52.5
    3.473−19.5−5
    Superior occipital gyrus1645.8818−9715
    5.1813−99.52.5
    c) Avoid high > avoid low: fight low > fight high
    Anterior cerebellum6487.3340.5−52−30
    Posterior cerebellum4.558−72−20
    4.2618−72−22.5
    Cuneus27476.67−17−5725
    Middle occipital gyrus6.66−32−74.525
    Cuneus6.1813−79.527.5
    Posterior cerebellum2875.53−27−69.5−27.5
    4.97−34.5−52−30
    Lingual gyrus3085.4513−472.5
    4.5823−64.5−5
    3.8223−49.57.5
    Amygdala1825.3430.53−22.5
    Temporal pole5.134310.5−17.5
    Inferior frontal cortex4.2530.515.5−22.5
    Supplementary motor area2594.782810.562.5
    4.5713−4.560
    4.3313−14.560
    d) Avoid low > avoid high: fight high > fight low
    Middle frontal gyrus48127.4828530
    Middle frontal gyrus6.99−24.540.525
    Postcentral gyrus6.30−32−2235
    Postcentral gyrus2386.7253−9.535
    5.3963−4.530
    4.3655.5−9.522.5
    Inferior parietal lobe2325.6655.5−5742.5
    5.0053−3740
    4.6855.5−64.530
    • n = 27, p < 0.001, pFWE < 0.05 cluster-level corrected.

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    Table 2.

    Brain activity in the selection and outcome phases

    RegionkPeak Txyz
    a) High > low selection phase
    IFG7906.5050.520.55
    5.484330.5−2.5
    5.0028−4.52.5
    4295.5343−5245
    4.2255.5−4737.5
    4.1138−6755
    PCC16915.4713−44.535
    Calcarine sulcus5.24−14.5−6217.5
    Precentral gyrus4.79−39.5−24.557.5
    PAG2185.3915.5−24.5−15
    5.163−24.5−5
    Putamen1294.9425.58−10
    3.68180.5−15
    Supplementary motor area2414.9010.5−267.5
    4.21810.562.5
    3.86−2−4.565
    OFC994.88−3218−17.5
    4.21−3233−10
    Middle occipital gyrus934.41−47−84.57.5
    Middle temporal gyrus4.34−59.5−69.55
    3.91−52−74.510
    Midcingulate cortex824.1985.540
    3.73−9.5840
    b) Won > lost outcome phase
    Inferior occipital gyrus8057.48−19.5−97−5
    5.60−27−94.512.5
    5.11−17−99.512.5
    Fusiform gyrus15686.8235.5−44.5−22.5
    Inferior occipital gyrus6.2328−92−5
    5.7320.5−970
    VS2466.491313−10
    SMG7246.06−47−6735
    4.96−54.5−49.550
    4.63−44.5−5742.5
    Superior temporal gyrus5295.6755.5−59.532.5
    5.0650.5−6245
    3.9555.5−4750
    IFG2595.2950.538−10
    4.4940.555.5−7.5
    Middle frontal gyrus17635.04−29.52345
    Medial prefrontal cortex4.68−4.560.515
    Middle frontal gyrus4.54−14.54342.5
    VS1924.90−123−15
    4.68−1213−12.5
    3.33−9.5182.5
    Middle frontal gyrus5374.673810.547.5
    4.57232357.5
    4.081335.552.5
    IFG4634.60−3750.5−7.5
    4.60−4743−10
    4.30−54.530.52.5
    c) Lost > won outcome phase
    Superior temporal gyrus305522.95−47−24.57.5
    18.72−54.5−3212.5
    17.28−39.5−3212.5
    Superior temporal gyrus333122.7150.5−19.57.5
    19.2165.5−2712.5
    AI6.583825.55
    Lingual gyrus2935.1920.5−59.55
    3.5515.5−7225
    • n = 36, p < 0.001, pFWE < 0.05 cluster-level corrected.

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Avoidant Responses to Interpersonal Provocation Are Associated with Increased Amygdala and Decreased Mentalizing Network Activity
Macià Buades-Rotger, Frederike Beyer, Ulrike M. Krämer
eNeuro 26 June 2017, 4 (3) ENEURO.0337-16.2017; DOI: 10.1523/ENEURO.0337-16.2017

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Avoidant Responses to Interpersonal Provocation Are Associated with Increased Amygdala and Decreased Mentalizing Network Activity
Macià Buades-Rotger, Frederike Beyer, Ulrike M. Krämer
eNeuro 26 June 2017, 4 (3) ENEURO.0337-16.2017; DOI: 10.1523/ENEURO.0337-16.2017
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