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Behavioral and neural responses during fear conditioning and extinction in a large transdiagnostic sample
BACKGROUND: Dysregulation of fear learning has been associated with psychiatric disorders that have altered positive and negative valence domain function. While amygdala-insula-prefrontal circuitry is considered important for fear learning, there have been inconsistencies in neural findings in healt...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Elsevier
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9189200/ https://www.ncbi.nlm.nih.gov/pubmed/35679785 http://dx.doi.org/10.1016/j.nicl.2022.103060 |
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author | Kirlic, Namik Kuplicki, Rayus Touthang, James Cohen, Zsofia P. Stewart, Jennifer L. Paulus, Martin P. Aupperle, Robin L. |
author_facet | Kirlic, Namik Kuplicki, Rayus Touthang, James Cohen, Zsofia P. Stewart, Jennifer L. Paulus, Martin P. Aupperle, Robin L. |
author_sort | Kirlic, Namik |
collection | PubMed |
description | BACKGROUND: Dysregulation of fear learning has been associated with psychiatric disorders that have altered positive and negative valence domain function. While amygdala-insula-prefrontal circuitry is considered important for fear learning, there have been inconsistencies in neural findings in healthy and clinical human samples. This study aimed to delineate the neural substrates and behavioral responses during fear learning in a large, transdiagnostic sample with predominantly depressive and/or anxious dysfunction. METHODS: Two-hundred and eighty-two individuals (52 healthy participants; 230 participants with depression and/or anxiety-related problems) from the Tulsa 1000 study, an ongoing, naturalistic longitudinal study based on a dimensional psychopathological framework, completed a Pavlovian fear learning task during functional magnetic resonance imaging. Linear mixed-effects analyses examined condition-by-time effects on brain activation (CS+, CS- across familiarization, conditioning, and extinction trials). A data-driven latent profile analysis (LPA) examined distinct patterns of behavioral and neural responses to threat across fear conditioning and extinction, while logistic regression analyses evaluated cognitive-affective predictors of latent profiles. RESULTS: Whole-brain analyses revealed a condition-by-time interaction in the anterior insula, postcentral gyrus, superior temporal gyrus, middle frontal gyrus, and cerebellum but not amygdala. The LPA identified distinct latent profiles across subjective and neural levels of measurement. Anterior insula profiles were characterized by marginal differences in age and state anxiety. CONCLUSIONS: Our findings demonstrate that human fear learning recruits a distributed network of regions involved in interoceptive, cognitive, motivational, and psychomotor processes. Data-driven analyses identified distinct profiles of subjective and neural responses during fear learning that transcended clinical diagnoses, but no robust relationships to demographic or cognitive-affective variable were identified. |
format | Online Article Text |
id | pubmed-9189200 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Elsevier |
record_format | MEDLINE/PubMed |
spelling | pubmed-91892002022-06-14 Behavioral and neural responses during fear conditioning and extinction in a large transdiagnostic sample Kirlic, Namik Kuplicki, Rayus Touthang, James Cohen, Zsofia P. Stewart, Jennifer L. Paulus, Martin P. Aupperle, Robin L. Neuroimage Clin Regular Article BACKGROUND: Dysregulation of fear learning has been associated with psychiatric disorders that have altered positive and negative valence domain function. While amygdala-insula-prefrontal circuitry is considered important for fear learning, there have been inconsistencies in neural findings in healthy and clinical human samples. This study aimed to delineate the neural substrates and behavioral responses during fear learning in a large, transdiagnostic sample with predominantly depressive and/or anxious dysfunction. METHODS: Two-hundred and eighty-two individuals (52 healthy participants; 230 participants with depression and/or anxiety-related problems) from the Tulsa 1000 study, an ongoing, naturalistic longitudinal study based on a dimensional psychopathological framework, completed a Pavlovian fear learning task during functional magnetic resonance imaging. Linear mixed-effects analyses examined condition-by-time effects on brain activation (CS+, CS- across familiarization, conditioning, and extinction trials). A data-driven latent profile analysis (LPA) examined distinct patterns of behavioral and neural responses to threat across fear conditioning and extinction, while logistic regression analyses evaluated cognitive-affective predictors of latent profiles. RESULTS: Whole-brain analyses revealed a condition-by-time interaction in the anterior insula, postcentral gyrus, superior temporal gyrus, middle frontal gyrus, and cerebellum but not amygdala. The LPA identified distinct latent profiles across subjective and neural levels of measurement. Anterior insula profiles were characterized by marginal differences in age and state anxiety. CONCLUSIONS: Our findings demonstrate that human fear learning recruits a distributed network of regions involved in interoceptive, cognitive, motivational, and psychomotor processes. Data-driven analyses identified distinct profiles of subjective and neural responses during fear learning that transcended clinical diagnoses, but no robust relationships to demographic or cognitive-affective variable were identified. Elsevier 2022-05-25 /pmc/articles/PMC9189200/ /pubmed/35679785 http://dx.doi.org/10.1016/j.nicl.2022.103060 Text en © 2022 The Author(s) https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). |
spellingShingle | Regular Article Kirlic, Namik Kuplicki, Rayus Touthang, James Cohen, Zsofia P. Stewart, Jennifer L. Paulus, Martin P. Aupperle, Robin L. Behavioral and neural responses during fear conditioning and extinction in a large transdiagnostic sample |
title | Behavioral and neural responses during fear conditioning and extinction in a large transdiagnostic sample |
title_full | Behavioral and neural responses during fear conditioning and extinction in a large transdiagnostic sample |
title_fullStr | Behavioral and neural responses during fear conditioning and extinction in a large transdiagnostic sample |
title_full_unstemmed | Behavioral and neural responses during fear conditioning and extinction in a large transdiagnostic sample |
title_short | Behavioral and neural responses during fear conditioning and extinction in a large transdiagnostic sample |
title_sort | behavioral and neural responses during fear conditioning and extinction in a large transdiagnostic sample |
topic | Regular Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9189200/ https://www.ncbi.nlm.nih.gov/pubmed/35679785 http://dx.doi.org/10.1016/j.nicl.2022.103060 |
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