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

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 risk...

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Autores principales: White, Tara L., Gonsalves, Meghan A., Zimmerman, Chloe, Joyce, Hannah, Cohen, Ronald A., Clark, Uraina S., Sweet, Lawrence H., Lejuez, Carl W., Nitenson, Adam Z.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10261990/
https://www.ncbi.nlm.nih.gov/pubmed/37325735
http://dx.doi.org/10.3389/fpsyg.2023.1060877
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author White, Tara L.
Gonsalves, Meghan A.
Zimmerman, Chloe
Joyce, Hannah
Cohen, Ronald A.
Clark, Uraina S.
Sweet, Lawrence H.
Lejuez, Carl W.
Nitenson, Adam Z.
author_facet White, Tara L.
Gonsalves, Meghan A.
Zimmerman, Chloe
Joyce, Hannah
Cohen, Ronald A.
Clark, Uraina S.
Sweet, Lawrence H.
Lejuez, Carl W.
Nitenson, Adam Z.
author_sort White, Tara L.
collection PubMed
description 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.
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spelling pubmed-102619902023-06-15 Anger, agency, risk and action: a neurobehavioral model with proof-of-concept in healthy young adults White, Tara L. Gonsalves, Meghan A. Zimmerman, Chloe Joyce, Hannah Cohen, Ronald A. Clark, Uraina S. Sweet, Lawrence H. Lejuez, Carl W. Nitenson, Adam Z. Front Psychol Psychology 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. Frontiers Media S.A. 2023-05-30 /pmc/articles/PMC10261990/ /pubmed/37325735 http://dx.doi.org/10.3389/fpsyg.2023.1060877 Text en Copyright © 2023 White, Gonsalves, Zimmerman, Joyce, Cohen, Clark, Sweet, Lejuez and Nitenson. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Psychology
White, Tara L.
Gonsalves, Meghan A.
Zimmerman, Chloe
Joyce, Hannah
Cohen, Ronald A.
Clark, Uraina S.
Sweet, Lawrence H.
Lejuez, Carl W.
Nitenson, Adam Z.
Anger, agency, risk and action: a neurobehavioral model with proof-of-concept in healthy young adults
title Anger, agency, risk and action: a neurobehavioral model with proof-of-concept in healthy young adults
title_full Anger, agency, risk and action: a neurobehavioral model with proof-of-concept in healthy young adults
title_fullStr Anger, agency, risk and action: a neurobehavioral model with proof-of-concept in healthy young adults
title_full_unstemmed Anger, agency, risk and action: a neurobehavioral model with proof-of-concept in healthy young adults
title_short Anger, agency, risk and action: a neurobehavioral model with proof-of-concept in healthy young adults
title_sort anger, agency, risk and action: a neurobehavioral model with proof-of-concept in healthy young adults
topic Psychology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10261990/
https://www.ncbi.nlm.nih.gov/pubmed/37325735
http://dx.doi.org/10.3389/fpsyg.2023.1060877
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