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Anxiety attenuates learning advantages conferred by statistical stability and induces loss of volatility‐attuning in brain activity

Anxiety can alter an individual's perception of their external sensory environment. Previous studies suggest that anxiety can increase the magnitude of neural responses to unexpected (or surprising) stimuli. Additionally, surprise responses are reported to be boosted during stable compared to v...

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Autores principales: Rowe, Elise G., Harris, Clare D., Dzafic, Ilvana, Garrido, Marta I.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley & Sons, Inc. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10028666/
https://www.ncbi.nlm.nih.gov/pubmed/36811216
http://dx.doi.org/10.1002/hbm.26230
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author Rowe, Elise G.
Harris, Clare D.
Dzafic, Ilvana
Garrido, Marta I.
author_facet Rowe, Elise G.
Harris, Clare D.
Dzafic, Ilvana
Garrido, Marta I.
author_sort Rowe, Elise G.
collection PubMed
description Anxiety can alter an individual's perception of their external sensory environment. Previous studies suggest that anxiety can increase the magnitude of neural responses to unexpected (or surprising) stimuli. Additionally, surprise responses are reported to be boosted during stable compared to volatile environments. Few studies, however, have examined how learning is impacted by both threat and volatility. To investigate these effects, we used threat‐of‐shock to transiently increase subjective anxiety in healthy adults while they performed an auditory oddball task under stable and volatile environments and while undergoing functional Magnetic Resonance Imaging (fMRI) scanning. We then used Bayesian Model Selection (BMS) mapping to identify the brain areas where different models of anxiety displayed the highest evidence. Behaviourally, we found that threat‐of‐shock eliminated the accuracy advantage conferred by environmental stability over volatility. Neurally, we found that threat‐of‐shock led to attenuation and loss of volatility‐attuning of brain activity evoked by surprising sounds across most subcortical and limbic regions including the thalamus, basal ganglia, claustrum, insula, anterior cingulate, hippocampal gyrus and the superior temporal gyrus. Taken together, our findings suggest that threat eliminates learning advantages conferred by statistical stability compared to volatility. Thus, we propose that anxiety disrupts behavioural adaptation to environmental statistics, and that multiple subcortical and limbic regions are implicated in this process.
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spelling pubmed-100286662023-03-22 Anxiety attenuates learning advantages conferred by statistical stability and induces loss of volatility‐attuning in brain activity Rowe, Elise G. Harris, Clare D. Dzafic, Ilvana Garrido, Marta I. Hum Brain Mapp Research Articles Anxiety can alter an individual's perception of their external sensory environment. Previous studies suggest that anxiety can increase the magnitude of neural responses to unexpected (or surprising) stimuli. Additionally, surprise responses are reported to be boosted during stable compared to volatile environments. Few studies, however, have examined how learning is impacted by both threat and volatility. To investigate these effects, we used threat‐of‐shock to transiently increase subjective anxiety in healthy adults while they performed an auditory oddball task under stable and volatile environments and while undergoing functional Magnetic Resonance Imaging (fMRI) scanning. We then used Bayesian Model Selection (BMS) mapping to identify the brain areas where different models of anxiety displayed the highest evidence. Behaviourally, we found that threat‐of‐shock eliminated the accuracy advantage conferred by environmental stability over volatility. Neurally, we found that threat‐of‐shock led to attenuation and loss of volatility‐attuning of brain activity evoked by surprising sounds across most subcortical and limbic regions including the thalamus, basal ganglia, claustrum, insula, anterior cingulate, hippocampal gyrus and the superior temporal gyrus. Taken together, our findings suggest that threat eliminates learning advantages conferred by statistical stability compared to volatility. Thus, we propose that anxiety disrupts behavioural adaptation to environmental statistics, and that multiple subcortical and limbic regions are implicated in this process. John Wiley & Sons, Inc. 2023-02-22 /pmc/articles/PMC10028666/ /pubmed/36811216 http://dx.doi.org/10.1002/hbm.26230 Text en © 2023 The Authors. Human Brain Mapping published by Wiley Periodicals LLC. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ (https://creativecommons.org/licenses/by-nc-nd/4.0/) License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
spellingShingle Research Articles
Rowe, Elise G.
Harris, Clare D.
Dzafic, Ilvana
Garrido, Marta I.
Anxiety attenuates learning advantages conferred by statistical stability and induces loss of volatility‐attuning in brain activity
title Anxiety attenuates learning advantages conferred by statistical stability and induces loss of volatility‐attuning in brain activity
title_full Anxiety attenuates learning advantages conferred by statistical stability and induces loss of volatility‐attuning in brain activity
title_fullStr Anxiety attenuates learning advantages conferred by statistical stability and induces loss of volatility‐attuning in brain activity
title_full_unstemmed Anxiety attenuates learning advantages conferred by statistical stability and induces loss of volatility‐attuning in brain activity
title_short Anxiety attenuates learning advantages conferred by statistical stability and induces loss of volatility‐attuning in brain activity
title_sort anxiety attenuates learning advantages conferred by statistical stability and induces loss of volatility‐attuning in brain activity
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10028666/
https://www.ncbi.nlm.nih.gov/pubmed/36811216
http://dx.doi.org/10.1002/hbm.26230
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