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A neural oscillatory signature of sustained anxiety

BACKGROUND: Anxiety is a sustained response to uncertain threats; yet few studies have explored sustained neurobiological activities underlying anxious states, particularly spontaneous neural oscillations. To address this gap, we reanalysed magnetoencephalographic (MEG) data recorded during induced...

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Autores principales: Roxburgh, Ariel D., White, David J., Grillon, Christian, Cornwell, Brian R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer US 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10684633/
https://www.ncbi.nlm.nih.gov/pubmed/37880568
http://dx.doi.org/10.3758/s13415-023-01132-1
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author Roxburgh, Ariel D.
White, David J.
Grillon, Christian
Cornwell, Brian R.
author_facet Roxburgh, Ariel D.
White, David J.
Grillon, Christian
Cornwell, Brian R.
author_sort Roxburgh, Ariel D.
collection PubMed
description BACKGROUND: Anxiety is a sustained response to uncertain threats; yet few studies have explored sustained neurobiological activities underlying anxious states, particularly spontaneous neural oscillations. To address this gap, we reanalysed magnetoencephalographic (MEG) data recorded during induced anxiety to identify differences in sustained oscillatory activity between high- and low-anxiety states. METHODS: We combined data from three previous MEG studies in which healthy adults (total N = 51) were exposed to alternating periods of threat of unpredictable shock and safety while performing a range of cognitive tasks (passive oddball, mixed–saccade or stop-signal tasks). Spontaneous, band-limited, oscillatory activity was extracted from middle and late intervals of the threat and safe periods, and regional power distributions were reconstructed with adaptive beamforming. Conjunction analyses were used to identify regions showing overlapping spectral power differences between threat and safe periods across the three task paradigms. RESULTS: MEG source analyses revealed a robust and widespread reduction in beta (14-30 Hz) power during threat periods in bilateral sensorimotor cortices extending into right prefrontal regions. Alpha (8-13 Hz) power reductions during threat were more circumscribed, with notable peaks in left intraparietal sulcus and thalamus. CONCLUSIONS: Threat-induced anxiety is underpinned by a sustained reduction in spontaneous beta- and alpha-band activity in sensorimotor and parietal cortical regions. This general oscillatory pattern likely reflects a state of heightened action readiness and vigilance to cope with uncertain threats. Our findings provide a critical reference for which to identify abnormalities in cortical oscillatory activities in clinically anxious patients as well as evaluating the efficacy of anxiolytic treatments. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.3758/s13415-023-01132-1.
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spelling pubmed-106846332023-11-30 A neural oscillatory signature of sustained anxiety Roxburgh, Ariel D. White, David J. Grillon, Christian Cornwell, Brian R. Cogn Affect Behav Neurosci Research Article BACKGROUND: Anxiety is a sustained response to uncertain threats; yet few studies have explored sustained neurobiological activities underlying anxious states, particularly spontaneous neural oscillations. To address this gap, we reanalysed magnetoencephalographic (MEG) data recorded during induced anxiety to identify differences in sustained oscillatory activity between high- and low-anxiety states. METHODS: We combined data from three previous MEG studies in which healthy adults (total N = 51) were exposed to alternating periods of threat of unpredictable shock and safety while performing a range of cognitive tasks (passive oddball, mixed–saccade or stop-signal tasks). Spontaneous, band-limited, oscillatory activity was extracted from middle and late intervals of the threat and safe periods, and regional power distributions were reconstructed with adaptive beamforming. Conjunction analyses were used to identify regions showing overlapping spectral power differences between threat and safe periods across the three task paradigms. RESULTS: MEG source analyses revealed a robust and widespread reduction in beta (14-30 Hz) power during threat periods in bilateral sensorimotor cortices extending into right prefrontal regions. Alpha (8-13 Hz) power reductions during threat were more circumscribed, with notable peaks in left intraparietal sulcus and thalamus. CONCLUSIONS: Threat-induced anxiety is underpinned by a sustained reduction in spontaneous beta- and alpha-band activity in sensorimotor and parietal cortical regions. This general oscillatory pattern likely reflects a state of heightened action readiness and vigilance to cope with uncertain threats. Our findings provide a critical reference for which to identify abnormalities in cortical oscillatory activities in clinically anxious patients as well as evaluating the efficacy of anxiolytic treatments. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.3758/s13415-023-01132-1. Springer US 2023-10-25 2023 /pmc/articles/PMC10684633/ /pubmed/37880568 http://dx.doi.org/10.3758/s13415-023-01132-1 Text en © The Author(s) 2023 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Roxburgh, Ariel D.
White, David J.
Grillon, Christian
Cornwell, Brian R.
A neural oscillatory signature of sustained anxiety
title A neural oscillatory signature of sustained anxiety
title_full A neural oscillatory signature of sustained anxiety
title_fullStr A neural oscillatory signature of sustained anxiety
title_full_unstemmed A neural oscillatory signature of sustained anxiety
title_short A neural oscillatory signature of sustained anxiety
title_sort neural oscillatory signature of sustained anxiety
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10684633/
https://www.ncbi.nlm.nih.gov/pubmed/37880568
http://dx.doi.org/10.3758/s13415-023-01132-1
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