Setting the tone for the day: Cortisol awakening response proactively modulates fronto-limbic circuitry for emotion processing

The cortisol awakening response (CAR) has been linked to a variety of emotion-related psychiatric conditions and is proposed to prepare the brain for upcoming stress and challenges. Yet, the underlying neurobiological mechanisms of such proactive effects on emotional processing remain elusive. In th...

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Main Authors: Changming Chen, Bingsen Xiong, Wenlong Tan, Yanqiu Tian, Shouwen Zhang, Jianhui Wu, Peng Song, Shaozheng Qin
Format: Article
Language:English
Published: Elsevier 2025-07-01
Series:NeuroImage
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Online Access:http://www.sciencedirect.com/science/article/pii/S105381192500254X
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author Changming Chen
Bingsen Xiong
Wenlong Tan
Yanqiu Tian
Shouwen Zhang
Jianhui Wu
Peng Song
Shaozheng Qin
author_facet Changming Chen
Bingsen Xiong
Wenlong Tan
Yanqiu Tian
Shouwen Zhang
Jianhui Wu
Peng Song
Shaozheng Qin
author_sort Changming Chen
collection DOAJ
description The cortisol awakening response (CAR) has been linked to a variety of emotion-related psychiatric conditions and is proposed to prepare the brain for upcoming stress and challenges. Yet, the underlying neurobiological mechanisms of such proactive effects on emotional processing remain elusive. In the current double-blinded, pharmacologically-manipulated study, 36 male adults (DXM group) received cortisol-repressive dexamethasone on the previous night, then performed the Emotional Face Matching Task (EFMT) during fMRI scanning the next afternoon. Relative to the placebo group (31 male adults), the DXM group exhibited lower accuracy in the emotion matching condition, but not in the sensorimotor control condition. Psychophysiological interaction (PPI) analyses revealed significant task-by-group interaction involving the right and left amygdala, but not the medial orbitofrontal cortex (MOFC) or hippocampus. Specifically, the DXM group exhibited stronger functional connectivity between the right amygdala and left dorsolateral prefrontal cortex (lDLPFC) during emotion condition but reduced connectivity in the same network during control condition, as compared to the placebo group. Meanwhile, the DXM group exhibited weaker left amygdala–right posterior middle temporal gyrus (rMTG) connectivity than the placebo group during control condition, but there was no group effect in the connectivity during emotion condition. These results indicate that the CAR proactively modulates fronto-limbic functional organization for emotion processing in male adults. Our findings support a causal link between CAR and its proactive effects on emotional processing, and suggest a model of CAR-mediated brain preparedness where CAR sets a tonic tone for the upcoming day to actively regulate neuroendocrinological responses to emotionally charged stimuli on a moment-to-moment basis.
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spelling doaj-art-933e5ca9219a4904bea328829dba114c2025-08-20T03:48:15ZengElsevierNeuroImage1095-95722025-07-0131512125110.1016/j.neuroimage.2025.121251Setting the tone for the day: Cortisol awakening response proactively modulates fronto-limbic circuitry for emotion processingChangming Chen0Bingsen Xiong1Wenlong Tan2Yanqiu Tian3Shouwen Zhang4Jianhui Wu5Peng Song6Shaozheng Qin7School of Educational Sciences, Chongqing Normal University, Chongqing, 401331, ChinaBeijing Key Laboratory of Applied Experimental Psychology, National Demonstration Center for Experimental Psychology Education, Faculty of Psychology, Beijing Normal University, Beijing 100875, ChinaBeijing Key Laboratory of Applied Experimental Psychology, National Demonstration Center for Experimental Psychology Education, Faculty of Psychology, Beijing Normal University, Beijing 100875, ChinaBeijing Key Laboratory of Applied Experimental Psychology, National Demonstration Center for Experimental Psychology Education, Faculty of Psychology, Beijing Normal University, Beijing 100875, ChinaNeuroelectrophysiology Department, Beijing DaWangLu Emergency Hospital, Beijing, 100122, China; Corresponding authors.Shenzhen Key Laboratory of Affective and Social Cognitive Science, Shenzhen University, Shenzhen, 518060, ChinaDepartment of Medical Oncology, The Second Medical Center and National Clinical Research Center for Geriatric Diseases, Chinese PLA General Hospital, Beijing, 100853, China; Corresponding authors.Beijing Key Laboratory of Applied Experimental Psychology, National Demonstration Center for Experimental Psychology Education, Faculty of Psychology, Beijing Normal University, Beijing 100875, China; State Key Laboratory of Cognitive Neuroscience and Learning & International Data Group/McGovern Institute for Brain Research, Beijing Normal University, Beijing 100875, China; Corresponding authors.The cortisol awakening response (CAR) has been linked to a variety of emotion-related psychiatric conditions and is proposed to prepare the brain for upcoming stress and challenges. Yet, the underlying neurobiological mechanisms of such proactive effects on emotional processing remain elusive. In the current double-blinded, pharmacologically-manipulated study, 36 male adults (DXM group) received cortisol-repressive dexamethasone on the previous night, then performed the Emotional Face Matching Task (EFMT) during fMRI scanning the next afternoon. Relative to the placebo group (31 male adults), the DXM group exhibited lower accuracy in the emotion matching condition, but not in the sensorimotor control condition. Psychophysiological interaction (PPI) analyses revealed significant task-by-group interaction involving the right and left amygdala, but not the medial orbitofrontal cortex (MOFC) or hippocampus. Specifically, the DXM group exhibited stronger functional connectivity between the right amygdala and left dorsolateral prefrontal cortex (lDLPFC) during emotion condition but reduced connectivity in the same network during control condition, as compared to the placebo group. Meanwhile, the DXM group exhibited weaker left amygdala–right posterior middle temporal gyrus (rMTG) connectivity than the placebo group during control condition, but there was no group effect in the connectivity during emotion condition. These results indicate that the CAR proactively modulates fronto-limbic functional organization for emotion processing in male adults. Our findings support a causal link between CAR and its proactive effects on emotional processing, and suggest a model of CAR-mediated brain preparedness where CAR sets a tonic tone for the upcoming day to actively regulate neuroendocrinological responses to emotionally charged stimuli on a moment-to-moment basis.http://www.sciencedirect.com/science/article/pii/S105381192500254XCortisol awakening responseAmygdalaPrefrontal cortexHippocampusfMRIEmotion
spellingShingle Changming Chen
Bingsen Xiong
Wenlong Tan
Yanqiu Tian
Shouwen Zhang
Jianhui Wu
Peng Song
Shaozheng Qin
Setting the tone for the day: Cortisol awakening response proactively modulates fronto-limbic circuitry for emotion processing
NeuroImage
Cortisol awakening response
Amygdala
Prefrontal cortex
Hippocampus
fMRI
Emotion
title Setting the tone for the day: Cortisol awakening response proactively modulates fronto-limbic circuitry for emotion processing
title_full Setting the tone for the day: Cortisol awakening response proactively modulates fronto-limbic circuitry for emotion processing
title_fullStr Setting the tone for the day: Cortisol awakening response proactively modulates fronto-limbic circuitry for emotion processing
title_full_unstemmed Setting the tone for the day: Cortisol awakening response proactively modulates fronto-limbic circuitry for emotion processing
title_short Setting the tone for the day: Cortisol awakening response proactively modulates fronto-limbic circuitry for emotion processing
title_sort setting the tone for the day cortisol awakening response proactively modulates fronto limbic circuitry for emotion processing
topic Cortisol awakening response
Amygdala
Prefrontal cortex
Hippocampus
fMRI
Emotion
url http://www.sciencedirect.com/science/article/pii/S105381192500254X
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