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. 2024 May 16;22(5):e3002195.
doi: 10.1371/journal.pbio.3002195. eCollection 2024 May.

Acute stress during witnessing injustice shifts third-party interventions from punishing the perpetrator to helping the victim

Huagen Wang  1   2   3 , Xiaoyan Wu  1   2   3 , Jiahua Xu  4 , Ruida Zhu  5 , Sihui Zhang  1   2   3 , Zhenhua Xu  1   2   3 , Xiaoqin Mai  6 , Shaozheng Qin  1   2   3   7 , Chao Liu  1   2   3
Affiliations

Acute stress during witnessing injustice shifts third-party interventions from punishing the perpetrator to helping the victim

Huagen Wang et al. PLoS Biol. .

Abstract

People tend to intervene in others' injustices by either punishing the transgressor or helping the victim. Injustice events often occur under stressful circumstances. However, how acute stress affects a third party's intervention in injustice events remains open. Here, we show a stress-induced shift in third parties' willingness to engage in help instead of punishment by acting on emotional salience and central-executive and theory-of-mind networks. Acute stress decreased the third party's willingness to punish the violator and the severity of the punishment and increased their willingness to help the victim. Computational modeling revealed a shift in preference of justice recovery from punishment the offender toward help the victim under stress. This finding is consistent with the increased dorsolateral prefrontal engagement observed with higher amygdala activity and greater connectivity with the ventromedial prefrontal cortex in the stress group. A brain connectivity theory-of-mind network predicted stress-induced justice recovery in punishment. Our findings suggest a neurocomputational mechanism of how acute stress reshapes third parties' decisions by reallocating neural resources in emotional, executive, and mentalizing networks to inhibit punishment bias and decrease punishment severity.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Experimental procedure, stress induction, and TPIG.
(A) Timeline depicting the experimental procedure. Four saliva samples with concurrent subjective affect ratings were collected throughout the task (S1–S4 and P1–P4). Heart rate was collected during stress induction (H1) and the TPIG (H2). (B–D) The curves depict salivary cortisol concentration, negative affect, and heart rate in the control and stress groups. The red and blue boxes represent the CPT and TPI time windows. (E) An illustration of the TPIG with a sample trial. In each trial, participants were asked to choose from 3 options within 4 s (i.e., subtract “A,” add “B,” or keep) in the decision window, and they were instructed to decide how many MUs to use to reduce the MUs of A or increase the MUs of B within 4 s in the transfer window. If the participants chose to keep the money for themselves, the transfer phase windows were shown to the participants, but they were asked to select the zero option (meaning no tokens were used to intervene in other-regarding events). A 1–5 s intertrial interval was set between each window to dissociate the neural signal from each phase. ***P < 0.001; **P < 0.01; error bars represent SEM. The source data of Fig 1B–1D can be found at https://osf.io/fkae9/. CPT, cold pressor test; MU, monetary unit; TPI, third-party intervention; TPIG, third-party intervention game.
Fig 2
Fig 2. Behavioral measures and computational modeling of the TPIG.
(A and C) Stress decreased the punishment rate but increased the help rate in the unfair condition (80:20 and 90:10). (B) In the unfair condition, stress decreased the severity of punishment. (D) Stress decreased the severity of punishment. The squares represent the predicted contributions of punishment and help under unfair conditions based on winning model. (E) An overview of model comparisons: Models 1 and 2 represent the baseline model and the inequality aversion model. Model 3 represents the other-regarding inequality aversion model with a shared parameter of relative severity preference. Model 4 represents the other-regarding inequality aversion model with 2 parameters of the severity of punishment and help separately. (F) The difference between the stress and control groups in the relative severity preference based on the computational model (α—β). (G) The actual choice rate differences between punishment and help (punishment bias) in all conditions as a function of the model-estimated relative severity. (H) The actual contribution differences between punishment and help (punishment bias) in all conditions as a function of the model-estimated relative severity. Each dot represents the data of a single participant. ***P < 0.001; **P < 0.01; *P < 0.05; †P < 0.01. Error bars represent the SEM. The source data of Fig 2A–2H can be found at https://osf.io/fkae9/. MU, monetary unit; TPIG, third-party intervention game.
Fig 3
Fig 3. Stress-induced changes in amygdala emotional salience and prefrontal executive networks in the decision phase.
(A and C) Stress-induced differences in brain representation of the degree of inequality and the functional connectivity between the amygdala and vmPFC. (A and B) PPI analysis based on the right amygdala as a seed showed that the stress group had increased functional connectivity of the right amygdala and the vmPFC during the decision stage in the punishment options. *P < 0.05; error bars represent the SEM. (C) The mediating effect of amygdala-vmPFC connectivity on the association between acute stress and the punishment rate (i.e., the frequency of selecting the punishment option in the decision phase). (D–G) Stress-induced neural activity in the decision phase. (D) Relative to the control group, the stress group demonstrated stronger DLPFC activation when selecting the punishment option than when selecting the help option (initial whole-brain threshold P < 0.001, cluster corrected P FWE < 0.05 for left DLPFC). (E–G) Relative to the control group, the stress group had stronger activation in the rDLPFC, rTPJ, and rPCC in trials in which participants selected the punishment option (initial threshold P < 0.001; cluster corrected P FWE < 0.05), and the effect was not significant in trials in which participants selected the help option. The source data of Fig 3B–3G can be found at https://osf.io/fkae9/. DLPFC, dorsolateral prefrontal cortex; PPI, psychophysiology interaction; vmPFC, ventromedial prefrontal cortex.
Fig 4
Fig 4. Stress-induced changes in brain-behavior associations with severity computations in the transfer stage.
(A) Brain-behavior relationships between the stress-induced shift of punishment bias (α-β) and activation in the rACC and PCC. Scatter plots depict the correlations between punishment bias (α-β) and activation in these regions. (B) Parametric modulation with trialwise Utility revealed a significant correlation with BOLD responses in the vmPFC and PCC for both the stress and control groups. (C) The moderated mediation models depict that the punishment bias (α-β) could account for the indirect associations of value computation in the activity of the rACC (left panel) and rPCC (right panel) with the punishment severity bias (punishment contribution minus help contribution). Acute stress moderated the correlation between value computation and punishment bias. All significant clusters were determined by a voxel level threshold P uncorrected < 0.001; cluster level threshold P FWE < 0.05, SVC. The source data of Fig 4A and 4C can be found at https://osf.io/fkae9/. BOLD, blood oxygen level-dependent; SVC, small-volume correction; vmPFC, ventromedial prefrontal cortex.
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Grants and funding

The research was supported by the Scientific and Technological Innovation (STl) 2030-Major Projects 2021ZD0200500 (https://en.most.gov.cn/) , the National Natural Science Foundation of China (https://www.nsfc.gov.cn/english/site_1/index.html, 32130045 to SQ and 32271092 to CL), the Major Project of National Social Science Foundation (http://www.nopss.gov.cn/GB/219469/431028/, 19ZDA363 to CL and 20&ZD153 to SQ), and Beijing Municipal Science and Technology Commission (https://kw.beijing.gov.cn/, Z151100003915122 to CL) , and the Fundamental Research Funds for the Central Universities to SQ. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.