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Context-dependent amygdala–prefrontal connectivity during the dot-probe task varies by irritability and attention bias to angry faces

Irritability, defined as proneness to anger, is among the most common reasons youth are seen for psychiatric care. Youth with irritability demonstrate aberrant processing of anger-related stimuli; however, the neural mechanisms remain unknown. We applied a drift-diffusion model (DDM), a computationa...

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Autores principales: Naim, Reut, Haller, Simone P., Linke, Julia O., Jaffe, Allison, Stoddard, Joel, Jones, Matt, Harrewijn, Anita, Kircanski, Katharina, Bar-Haim, Yair, Brotman, Melissa A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer International Publishing 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9630440/
https://www.ncbi.nlm.nih.gov/pubmed/35641787
http://dx.doi.org/10.1038/s41386-022-01307-3
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author Naim, Reut
Haller, Simone P.
Linke, Julia O.
Jaffe, Allison
Stoddard, Joel
Jones, Matt
Harrewijn, Anita
Kircanski, Katharina
Bar-Haim, Yair
Brotman, Melissa A.
author_facet Naim, Reut
Haller, Simone P.
Linke, Julia O.
Jaffe, Allison
Stoddard, Joel
Jones, Matt
Harrewijn, Anita
Kircanski, Katharina
Bar-Haim, Yair
Brotman, Melissa A.
author_sort Naim, Reut
collection PubMed
description Irritability, defined as proneness to anger, is among the most common reasons youth are seen for psychiatric care. Youth with irritability demonstrate aberrant processing of anger-related stimuli; however, the neural mechanisms remain unknown. We applied a drift-diffusion model (DDM), a computational tool, to derive a latent behavioral metric of attentional bias to angry faces in youth with varying levels of irritability during functional magnetic resonance imaging (fMRI). We examined associations among irritability, task behavior using a DDM-based index for preferential allocation of attention to angry faces (i.e., extra-decisional time bias; Δt(0)), and amygdala context-dependent connectivity during the dot-probe task. Our transdiagnostic sample, enriched for irritability, included 351 youth (ages 8–18; M = 12.92 years, 51% male, with primary diagnoses of either attention deficit/hyperactivity disorder [ADHD], disruptive mood dysregulation disorder [DMDD], an anxiety disorder, or healthy controls). Models accounted for age, sex, in-scanner motion, and co-occurring symptoms of anxiety. Youth and parents rated youth’s irritability using the Affective Reactivity Index. An fMRI dot-probe task was used to assess attention orienting to angry faces. In the angry-incongruent vs. angry-congruent contrast, amygdala connectivity with the bilateral inferior frontal gyrus (IFG), insula, caudate, and thalamus/pulvinar was modulated by irritability level and attention bias to angry faces, Δt(0), all ts(350) > 4.46, ps < 0.001. In youth with high irritability, elevated Δt(0) was associated with a weaker amygdala connectivity. In contrast, in youth with low irritability, elevated Δt(0) was associated with stronger connectivity in those regions. No main effect emerged for irritability. As irritability is associated with reactive aggression, these results suggest a potential neural regulatory deficit in irritable youth who have elevated attention bias to angry cues.
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spelling pubmed-96304402022-11-04 Context-dependent amygdala–prefrontal connectivity during the dot-probe task varies by irritability and attention bias to angry faces Naim, Reut Haller, Simone P. Linke, Julia O. Jaffe, Allison Stoddard, Joel Jones, Matt Harrewijn, Anita Kircanski, Katharina Bar-Haim, Yair Brotman, Melissa A. Neuropsychopharmacology Article Irritability, defined as proneness to anger, is among the most common reasons youth are seen for psychiatric care. Youth with irritability demonstrate aberrant processing of anger-related stimuli; however, the neural mechanisms remain unknown. We applied a drift-diffusion model (DDM), a computational tool, to derive a latent behavioral metric of attentional bias to angry faces in youth with varying levels of irritability during functional magnetic resonance imaging (fMRI). We examined associations among irritability, task behavior using a DDM-based index for preferential allocation of attention to angry faces (i.e., extra-decisional time bias; Δt(0)), and amygdala context-dependent connectivity during the dot-probe task. Our transdiagnostic sample, enriched for irritability, included 351 youth (ages 8–18; M = 12.92 years, 51% male, with primary diagnoses of either attention deficit/hyperactivity disorder [ADHD], disruptive mood dysregulation disorder [DMDD], an anxiety disorder, or healthy controls). Models accounted for age, sex, in-scanner motion, and co-occurring symptoms of anxiety. Youth and parents rated youth’s irritability using the Affective Reactivity Index. An fMRI dot-probe task was used to assess attention orienting to angry faces. In the angry-incongruent vs. angry-congruent contrast, amygdala connectivity with the bilateral inferior frontal gyrus (IFG), insula, caudate, and thalamus/pulvinar was modulated by irritability level and attention bias to angry faces, Δt(0), all ts(350) > 4.46, ps < 0.001. In youth with high irritability, elevated Δt(0) was associated with a weaker amygdala connectivity. In contrast, in youth with low irritability, elevated Δt(0) was associated with stronger connectivity in those regions. No main effect emerged for irritability. As irritability is associated with reactive aggression, these results suggest a potential neural regulatory deficit in irritable youth who have elevated attention bias to angry cues. Springer International Publishing 2022-06-01 2022-12 /pmc/articles/PMC9630440/ /pubmed/35641787 http://dx.doi.org/10.1038/s41386-022-01307-3 Text en © This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Naim, Reut
Haller, Simone P.
Linke, Julia O.
Jaffe, Allison
Stoddard, Joel
Jones, Matt
Harrewijn, Anita
Kircanski, Katharina
Bar-Haim, Yair
Brotman, Melissa A.
Context-dependent amygdala–prefrontal connectivity during the dot-probe task varies by irritability and attention bias to angry faces
title Context-dependent amygdala–prefrontal connectivity during the dot-probe task varies by irritability and attention bias to angry faces
title_full Context-dependent amygdala–prefrontal connectivity during the dot-probe task varies by irritability and attention bias to angry faces
title_fullStr Context-dependent amygdala–prefrontal connectivity during the dot-probe task varies by irritability and attention bias to angry faces
title_full_unstemmed Context-dependent amygdala–prefrontal connectivity during the dot-probe task varies by irritability and attention bias to angry faces
title_short Context-dependent amygdala–prefrontal connectivity during the dot-probe task varies by irritability and attention bias to angry faces
title_sort context-dependent amygdala–prefrontal connectivity during the dot-probe task varies by irritability and attention bias to angry faces
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9630440/
https://www.ncbi.nlm.nih.gov/pubmed/35641787
http://dx.doi.org/10.1038/s41386-022-01307-3
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