Anger can generate action by individuals and groups. Therefore, it is important to understand the behavioral phenotypes of anger and its underlying neural substrates. Here, we introduce a construct we call anger agency, a negatively balanced internal state that motivates action to achieve risky goals.
Study 2 assessed the functional MRI response to risk in healthy volunteers given 20 mg d-amphetamine in a double-blind, placebo-controlled crossover study (N = 10 men), providing preliminary information on the ventral striatal response to risky rewards during catecholamine activation.
Results of Study 2: Trait SP and task-induced PA were strongly positively related to the catecholamine-facilitated BOLD response in the right nucleus accumbens, a brain region where the DA prediction error signal shapes action value and selection. Participants’ task-induced NA was strongly positively related to both trait SP and task-induced PA.
Social rewards and punishments motivate human learning and behavior, and alterations in brain circuits involved in processing these stimuli are associated with several neuropsychiatric disorders. However, questions remain about the exact neural substrates involved in the processing of social rewards and punishments. Here, we conducted four voxel-wise Signed Differential Mapping of Anisotropic Effect Size meta-analyses of fMRI studies investigating the neural correlates of anticipation and receipt of social rewards and punishments using the Social Incentive Delay task.
We found that anticipation of social rewards and avoidance of social punishment recruit a broad network of areas, including the basal ganglia, midbrain, dorsal anterior cingulate cortex, supplementary motor area, anterior insula, occipital gyrus, and other frontal, temporal, parietal, and cerebellar regions not captured in previous coordinate-based meta-analyses. We identified decreases in BOLD signal during anticipation of social reward and avoidance of punishment in regions of the default mode network missed in individual studies, likely due to lack of power. Receipt of social rewards engaged a robust network of brain regions, including ventromedial frontal and orbitofrontal cortices, anterior cingulate cortex, amygdala, hippocampus, occipital cortex, and brainstem, but not the basal ganglia.
Receiving social punishments increased BOLD signal in the orbitofrontal cortex, superior and inferior frontal gyri, lateral occipital cortex, and insula. In contrast to receiving social rewards, we identified a decrease in BOLD signal in the basal ganglia in response to receiving social punishments. These results provide a better understanding of the brain circuitry involved in the processing of social rewards and punishments. Furthermore, they may inform hypotheses about brain areas where disruption of activity may be associated with dysfunctional processing of social incentives and dysfunctions of agency (sense of responsibility).
Harm avoidance (HA) is a Cloninger personality trait that describes behavioral inhibition to avoid aversive stimuli. It serves as a predisposing factor contributing to the development of mental disorders such as anxiety and major depressive disorder. A multimodal meta-analysis of whole-brain structural and resting-state functional neuroimaging studies to identify the most stable neural substrate of HA. A total of 10 structural voxel-based morphometry studies (11 datasets) and 13 functional positron emission tomography or single-photon emission computed tomography studies (16 datasets) involving 3,053 healthy participants without any psychiatric or neurological disorders were included.
The meta-analysis revealed brain volumetric correlates of HA in the parietal and temporal cortices, and resting-state functional correlates in the prefrontal, temporal, and parietal gray matter. Volumetric and functional correlates co-occurred in the left superior frontal gyrus and left middle frontal gyrus, and were dissociated in the left gyrus rectus. A comprehensive meta-analysis of the structural and functional correlates of harm avoidance is a contribution that may help to bridge the serious gap between the neurobiology of harm avoidance and its pathogenesis, prevention, and treatment of mental disorders related to the sense of causing harm, which indirectly involves a healthy agency system. Neuroticism is one of the most robust higher-order personality traits associated with negative emotionality, dysfunction of the sense of agency, and risk for mental disorders.
The most common differences found in brain activation studies have been associated with neuroticism during fear learning, anticipation of aversive stimuli, and emotion processing and regulation. There is a within-brain association between social status and socioemotional neural responses that are localized to the frontal-parietal and visual cortices.
A meta-analysis of whole-brain resting-state functional neuroimaging studies was performed to identify the most stable neurofunctional substrates of neuroticism, and found significant and stable positive correlations between neuroticism and resting-state brain activity in the left middle temporal gyrus (MTG), left striatum, and right hippocampus. In contrast, resting-state brain activity in the left superior temporal gyrus (STG) and right supramarginal gyrus (SMG) was negatively associated with neuroticism. Furthermore, meta-regression analysis revealed brain regions in which sex and age moderated the link between spontaneous activity and neuroticism.
It is known that the absence of perception and sense of premonition regarding the health of others, and one’s own health (self-premonition) requires a healthy agency system, and when very dysfunctional, the temporal and parietal regions have low activity, observed in functional neuroimaging exams.
Discussion: Together, these findings inform the phenomenology and neurobiology of agentic anger, which recruits incentive motivational circuits and motivates personal action in response to goals that involve risk (defined as exposure to uncertainty, obstacles, potential harm, loss, and/or financial, emotional, bodily, or moral danger).
Conclusion
Neural mechanisms of agency, anger, risk-taking and harm avoidance are discussed, with implications for personal and group action, decision-making, social justice and behavior change, in addition to showing the importance of the cognitive domain of responsibility, through the neural bases of the neural system of agency, which functionally presents a distortion of responsibilities for harm to health.
Bibliographic References
Jinping Lin et al., Analysis of neural correlates of neuroticism: a coordinate-based meta-analysis of resting-state functional brain imaging studies Neurosci Biobehav Rev. 2023 March.
Guo Z, Xing Z, Liu L, Schwieter JW, Liu H. An fMRI study on how decisions are influenced by affective evaluations from different social hierarchical positions. Cogn Neurodyn. 2024 Oct;18(5):2161-2176. doi: 10.1007/s11571-024-10072-6. Epub 2024 Feb 23. PMID: 39555254; PMCID: PMC11564596.
Servaas MN, van der Velde J, Costafreda SG, Horton P, Ormel J, Riese H, Aleman A. Neuroticism and the brain: a quantitative meta-analysis of neuroimaging studies investigating emotion processing. Neurosci Biobehav Rev. 2013 Sep;37(8):1518-29. doi: 10.1016/j.neubiorev.2013.05.005. Epub 2013 May 15. PMID: 23685122.
Lin J, Li L, Pan N, Liu X, Zhang X, Suo X, Kemp GJ, Wang S, Gong Q. Neural correlates of neuroticism: A coordinate-based meta-analysis of resting-state functional brain imaging studies. Neurosci Biobehav Rev. 2023 Mar;146:105055. doi: 10.1016/j.neubiorev.2023.105055. Epub 2023 Jan 18. PMID: 36681370.
White TL, Gonsalves MA, Zimmerman C, Joyce H, Cohen RA, Clark US, Sweet LH, Lejuez CW, Nitenson AZ. Anger, agency, risk and action: a neurobehavioral model with proof-of-concept in healthy young adults. Front Psychol. 2023 May 30;14:1060877. doi: 10.3389/fpsyg.2023.1060877. PMID: 37325735; PMCID: PMC10261990.
Martins D, Rademacher L, Gabay AS, Taylor R, Richey JA, Smith DV, Goerlich KS, Nawijn L, Cremers HR, Wilson R, Bhattacharyya S, Paloyelis Y. Mapping social reward and punishment processing in the human brain: A voxel- based meta-analysis of neuroimaging findings using the social incentive delay task. Neurosci Biobehav Rev. 2021 Mar;122:1-17. doi: 10.1016/j.neubiorev.2020.12.034. Epub 2021 Jan 6. PMID: 33421544.
Zhong S, Lin J, Zhang L, Wang S, Kemp GJ, Li L, Gong Q. Neural correlates of harm avoidance: a multimodal meta-analysis of brain structural and resting-state functional neuroimaging studies. Transl Psychiatry. 2024 Sep 20;14(1):384. doi: 10.1038/s41398-024-03091-8. PMID: 39304648; PMCID: PMC11415487.
