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Deficient prefrontal-amygdalar connectivity underlies inefficient face processing in adolescent major depressive disorder

Adolescence represents a critical developmental period where the prevalence of major depressive disorder (MDD) increases. Aberrant emotion processing is a core feature of adolescent MDD that has been associated with functional alterations within the prefrontal-amygdala circuitry. In this study, we t...

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Autores principales: Willinger, David, Karipidis, Iliana I., Häberling, Isabelle, Berger, Gregor, Walitza, Susanne, Brem, Silvia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9090758/
https://www.ncbi.nlm.nih.gov/pubmed/35538052
http://dx.doi.org/10.1038/s41398-022-01955-5
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author Willinger, David
Karipidis, Iliana I.
Häberling, Isabelle
Berger, Gregor
Walitza, Susanne
Brem, Silvia
author_facet Willinger, David
Karipidis, Iliana I.
Häberling, Isabelle
Berger, Gregor
Walitza, Susanne
Brem, Silvia
author_sort Willinger, David
collection PubMed
description Adolescence represents a critical developmental period where the prevalence of major depressive disorder (MDD) increases. Aberrant emotion processing is a core feature of adolescent MDD that has been associated with functional alterations within the prefrontal-amygdala circuitry. In this study, we tested cognitive and neural mechanisms of emotional face processing in adolescents with MDD utilizing a combination of computational modeling and neuroimaging. Thirty adolescents with MDD (age: M = 16.1 SD = 1.4, 20 females) and 33 healthy controls (age: M = 16.2 SD = 1.9, 20 females) performed a dynamic face- and shape-matching task. A linear ballistic accumulator model was fit to the behavioral data to study differences in evidence accumulation. We used dynamic causal modeling (DCM) to study effective connectivity in the prefrontal-amygdala network to reveal the neural underpinnings of cognitive impairments while performing the task. Face processing efficiency was reduced in the MDD group and most pronounced for ambiguous faces with neutral emotional expressions. Critically, this reduction was related to increased deactivation of the subgenual anterior cingulate (sgACC). Connectivity analysis showed that MDD exhibited altered functional coupling in a distributed network spanning the fusiform face area–lateral prefrontal cortex–sgACC and the sgACC–amygdala pathway. Our results suggest that MDD is related to impairments of processing nuanced facial expressions. Distributed dysfunctional coupling in the face processing network might result in inefficient evidence sampling and inappropriate emotional responses contributing to depressive symptomatology. Our study provides novel insights in the characterization of brain function in adolescents with MDD that strongly emphasize the critical role of aberrant prefrontal-amygdala interactions during emotional face processing.
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spelling pubmed-90907582022-05-12 Deficient prefrontal-amygdalar connectivity underlies inefficient face processing in adolescent major depressive disorder Willinger, David Karipidis, Iliana I. Häberling, Isabelle Berger, Gregor Walitza, Susanne Brem, Silvia Transl Psychiatry Article Adolescence represents a critical developmental period where the prevalence of major depressive disorder (MDD) increases. Aberrant emotion processing is a core feature of adolescent MDD that has been associated with functional alterations within the prefrontal-amygdala circuitry. In this study, we tested cognitive and neural mechanisms of emotional face processing in adolescents with MDD utilizing a combination of computational modeling and neuroimaging. Thirty adolescents with MDD (age: M = 16.1 SD = 1.4, 20 females) and 33 healthy controls (age: M = 16.2 SD = 1.9, 20 females) performed a dynamic face- and shape-matching task. A linear ballistic accumulator model was fit to the behavioral data to study differences in evidence accumulation. We used dynamic causal modeling (DCM) to study effective connectivity in the prefrontal-amygdala network to reveal the neural underpinnings of cognitive impairments while performing the task. Face processing efficiency was reduced in the MDD group and most pronounced for ambiguous faces with neutral emotional expressions. Critically, this reduction was related to increased deactivation of the subgenual anterior cingulate (sgACC). Connectivity analysis showed that MDD exhibited altered functional coupling in a distributed network spanning the fusiform face area–lateral prefrontal cortex–sgACC and the sgACC–amygdala pathway. Our results suggest that MDD is related to impairments of processing nuanced facial expressions. Distributed dysfunctional coupling in the face processing network might result in inefficient evidence sampling and inappropriate emotional responses contributing to depressive symptomatology. Our study provides novel insights in the characterization of brain function in adolescents with MDD that strongly emphasize the critical role of aberrant prefrontal-amygdala interactions during emotional face processing. Nature Publishing Group UK 2022-05-10 /pmc/articles/PMC9090758/ /pubmed/35538052 http://dx.doi.org/10.1038/s41398-022-01955-5 Text en © The Author(s) 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
Willinger, David
Karipidis, Iliana I.
Häberling, Isabelle
Berger, Gregor
Walitza, Susanne
Brem, Silvia
Deficient prefrontal-amygdalar connectivity underlies inefficient face processing in adolescent major depressive disorder
title Deficient prefrontal-amygdalar connectivity underlies inefficient face processing in adolescent major depressive disorder
title_full Deficient prefrontal-amygdalar connectivity underlies inefficient face processing in adolescent major depressive disorder
title_fullStr Deficient prefrontal-amygdalar connectivity underlies inefficient face processing in adolescent major depressive disorder
title_full_unstemmed Deficient prefrontal-amygdalar connectivity underlies inefficient face processing in adolescent major depressive disorder
title_short Deficient prefrontal-amygdalar connectivity underlies inefficient face processing in adolescent major depressive disorder
title_sort deficient prefrontal-amygdalar connectivity underlies inefficient face processing in adolescent major depressive disorder
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9090758/
https://www.ncbi.nlm.nih.gov/pubmed/35538052
http://dx.doi.org/10.1038/s41398-022-01955-5
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