Altered task-related decoupling of the rostral anterior cingulate cortex in depression

Dysfunctional activity of the rostral anterior cingulate cortex (rACC) – an extensively connected hub region of the default mode network – has been broadly linked to cognitive and affective impairments in depression. However, the nature of aberrant task-related rACC suppression in depression is inco...

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Main Authors: Christine A. Leonards, Ben J. Harrison, Alec J. Jamieson, James Agathos, Trevor Steward, Christopher G. Davey
Format: Article
Language:English
Published: Elsevier 2024-01-01
Series:NeuroImage: Clinical
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158224000032
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author Christine A. Leonards
Ben J. Harrison
Alec J. Jamieson
James Agathos
Trevor Steward
Christopher G. Davey
author_facet Christine A. Leonards
Ben J. Harrison
Alec J. Jamieson
James Agathos
Trevor Steward
Christopher G. Davey
author_sort Christine A. Leonards
collection DOAJ
description Dysfunctional activity of the rostral anterior cingulate cortex (rACC) – an extensively connected hub region of the default mode network – has been broadly linked to cognitive and affective impairments in depression. However, the nature of aberrant task-related rACC suppression in depression is incompletely understood. In this study, we sought to characterize functional connectivity of rACC activity suppression (‘deactivation’) – an essential feature of rACC function – during external task engagement in depression. Specifically, we aimed to explore neural patterns of functional decoupling and coupling with the rACC during its task-driven suppression. We enrolled 81 15- to 25-year-old young people with moderate-to-severe major depressive disorder (MDD) before they commenced a 12-week clinical trial that assessed the effectiveness of cognitive behavioral therapy plus either fluoxetine or placebo. Ninety-four matched healthy controls were also recruited. Participants completed a functional magnetic resonance imaging face matching task known to elicit rACC suppression. To identify brain regions associated with the rACC during its task-driven suppression, we employed a seed-based functional connectivity analysis. We found MDD participants, compared to controls, showed significantly reduced ‘decoupling’ of the rACC with extended task-specific regions during task performance. Specifically, less decoupling was observed in the occipital and fusiform gyrus, dorsal ACC, medial prefrontal cortex, cuneus, amygdala, thalamus, and hippocampus. Notably, impaired decoupling was apparent in participants who did not remit to treatment, but not treatment remitters. Further, we found MDD participants showed significant increased coupling with the anterior insula cortex during task engagement. Our findings indicate that aberrant task-related rACC suppression is associated with disruptions in adaptive neural communication and dynamic switching between internal and external cognitive modes that may underpin maladaptive cognitions and biased emotional processing in depression.
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spelling doaj.art-f26a3779d5354a65bbc44c60023842f42024-03-13T04:45:36ZengElsevierNeuroImage: Clinical2213-15822024-01-0141103564Altered task-related decoupling of the rostral anterior cingulate cortex in depressionChristine A. Leonards0Ben J. Harrison1Alec J. Jamieson2James Agathos3Trevor Steward4Christopher G. Davey5Department of Psychiatry, The University of Melbourne, Parkville, Victoria, AustraliaDepartment of Psychiatry, The University of Melbourne, Parkville, Victoria, AustraliaDepartment of Psychiatry, The University of Melbourne, Parkville, Victoria, AustraliaDepartment of Psychiatry, The University of Melbourne, Parkville, Victoria, AustraliaDepartment of Psychiatry, The University of Melbourne, Parkville, Victoria, Australia; Melbourne School of Psychological Sciences, The University of Melbourne, Parkville, Victoria, AustraliaDepartment of Psychiatry, The University of Melbourne, Parkville, Victoria, Australia; Corresponding author at: Level 3, Alan Gilbert Building, 161 Barry Street, The University of Melbourne, Victoria 3010, Australia.Dysfunctional activity of the rostral anterior cingulate cortex (rACC) – an extensively connected hub region of the default mode network – has been broadly linked to cognitive and affective impairments in depression. However, the nature of aberrant task-related rACC suppression in depression is incompletely understood. In this study, we sought to characterize functional connectivity of rACC activity suppression (‘deactivation’) – an essential feature of rACC function – during external task engagement in depression. Specifically, we aimed to explore neural patterns of functional decoupling and coupling with the rACC during its task-driven suppression. We enrolled 81 15- to 25-year-old young people with moderate-to-severe major depressive disorder (MDD) before they commenced a 12-week clinical trial that assessed the effectiveness of cognitive behavioral therapy plus either fluoxetine or placebo. Ninety-four matched healthy controls were also recruited. Participants completed a functional magnetic resonance imaging face matching task known to elicit rACC suppression. To identify brain regions associated with the rACC during its task-driven suppression, we employed a seed-based functional connectivity analysis. We found MDD participants, compared to controls, showed significantly reduced ‘decoupling’ of the rACC with extended task-specific regions during task performance. Specifically, less decoupling was observed in the occipital and fusiform gyrus, dorsal ACC, medial prefrontal cortex, cuneus, amygdala, thalamus, and hippocampus. Notably, impaired decoupling was apparent in participants who did not remit to treatment, but not treatment remitters. Further, we found MDD participants showed significant increased coupling with the anterior insula cortex during task engagement. Our findings indicate that aberrant task-related rACC suppression is associated with disruptions in adaptive neural communication and dynamic switching between internal and external cognitive modes that may underpin maladaptive cognitions and biased emotional processing in depression.http://www.sciencedirect.com/science/article/pii/S2213158224000032Cognitive flexibilityDefault mode networkfMRIFunctional connectivityMajor depressive disorderSuppression
spellingShingle Christine A. Leonards
Ben J. Harrison
Alec J. Jamieson
James Agathos
Trevor Steward
Christopher G. Davey
Altered task-related decoupling of the rostral anterior cingulate cortex in depression
NeuroImage: Clinical
Cognitive flexibility
Default mode network
fMRI
Functional connectivity
Major depressive disorder
Suppression
title Altered task-related decoupling of the rostral anterior cingulate cortex in depression
title_full Altered task-related decoupling of the rostral anterior cingulate cortex in depression
title_fullStr Altered task-related decoupling of the rostral anterior cingulate cortex in depression
title_full_unstemmed Altered task-related decoupling of the rostral anterior cingulate cortex in depression
title_short Altered task-related decoupling of the rostral anterior cingulate cortex in depression
title_sort altered task related decoupling of the rostral anterior cingulate cortex in depression
topic Cognitive flexibility
Default mode network
fMRI
Functional connectivity
Major depressive disorder
Suppression
url http://www.sciencedirect.com/science/article/pii/S2213158224000032
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