Anger, agency, risk and action: a neurobehavioral model with proof-of-concept in healthy young adults

Tara L White; Meghan A Gonsalves; Chloe Zimmerman; Hannah Joyce; Ronald A Cohen; Uraina S Clark; Lawrence H Sweet; Carl W Lejuez; Adam Z Nitenson

doi:10.3389/fpsyg.2023.1060877

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. eCollection 2023.

Authors

Tara L White¹, Meghan A Gonsalves², Chloe Zimmerman², Hannah Joyce³, Ronald A Cohen⁴, Uraina S Clark⁵, Lawrence H Sweet⁶, Carl W Lejuez⁷, Adam Z Nitenson²

Affiliations

¹ Department of Behavioral and Social Sciences, Center for Alcohol and Addiction Studies, and Carney Institute for Brain Science, Brown University, Providence, RI, United States.
² Neuroscience Graduate Program, Brown University, Providence, RI, United States.
³ Undergraduate Program in Cognitive Neuroscience, Brown University, Providence, RI, United States.
⁴ Center for Cognitive Aging and Memory, McKnight Brain Foundation, University of Florida, Gainesville, FL, United States.
⁵ Department of Neurology, Icahn School of Medicine at Mount Sinai, New York, NY, United States.
⁶ Department of Psychology, University of Georgia, Athens, GA, United States.
⁷ Provost and Executive Vice President, Department of Psychology, Department of Psychiatry and Behavioral Health, Stony Brook University, Stony Brook, NY, United States.

Abstract

Introduction: Anger can engender action by individuals and groups. It is thus important to understand anger's behavioral phenotypes and their underlying neural substrates. Here, we introduce a construct we term agentic anger, a negatively valenced internal state that motivates action to achieve risky goals. We evaluate our neurobehavioral model via testable hypotheses in two proof-of-concept studies.

Study 1 methods: Study 1 used the Incentive Balloon Analogue Risk Task in a within-subjects, repeated measures design in 39 healthy volunteers to evaluate: (a) impact of blockade of reward on agentic anger, assessed by self-reports of negative activation (NA), (b) impact of achievement of reward on exuberance, assessed by self-reports of positive activation (PA), (c) the interrelationship of these valenced states, and (d) their relationship with personality.

Study 1 results: Task-induced NA was positively correlated with task-induced PA, risk-taking on the task and trait Social Potency (SP), a measure of trait agency and reward sensitivity on the Multidimensional Personality Questionnaire Brief-Form.

Study 2 methods: Study 2 assessed functional MRI response to stakes for risk-taking in healthy volunteers receiving 20 mg d-amphetamine in a double-blinded, placebo-controlled crossover design (N = 10 males), providing preliminary information on ventral striatal response to risky rewards during catecholamine activation.

Study 2 results: Trait SP and task-induced PA were strongly positively related to catecholamine-facilitated BOLD response in the right nucleus accumbens, a brain region where DA prediction error signal shapes action value and selection. Participants' task-induced NA was strongly positively related with trait SP and task-induced PA, replicating the findings of Study 1.

Discussion: Together these results inform the phenomenology and neurobiology of agentic anger, which recruits incentive motivational circuitry and motivates personal action in response to goals that entail risk (defined as exposure to uncertainty, obstacles, potential harm, loss and/or financial, emotional, bodily, or moral peril). Neural mechanisms of agency, anger, exuberance, and risk-taking are discussed, with implications for personal and group action, decision-making, social justice, and behavior change.

Keywords: agency; anger; catecholamines; emotion; incentive motivation; monoamines; reward.