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Cited by 7Neural and Behavioral Psychology StudiesChild and Adolescent Psychosocial and Emotional DevelopmentPsychopathy, Forensic Psychiatry, Sexual Offending

Mediating effect of amygdala activity on response to fear vs. happiness in youth with significant levels of irritability and disruptive mood and behavior disorders

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Suk, Ji-Woo, Blair, Robert J. R., Vaughan, Brigette, Lerdahl, Arica, Garvey, William F., Edwards, Ryan, Leibenluft, Ellen, Hwang, Soonjo·2023·Frontiers in Behavioral Neuroscience
DOI 10.3389/fnbeh.2023.1204574PMC PMC10602729
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Abstract

Introduction: Irritability, characterized by a tendency to exhibit increased anger, is a common clinical problem in youth. Irritability is a significant clinical issue in youth with various psychiatric diagnoses, especially disruptive behavior, and mood disorders (Attention-Deficit/Hyperactivity Disorder, Oppositional Defiant Disorder, Conduct Disorder, and Disruptive Mood Dysregulation Disorder). Although there have been previous studies focusing on functional alteration in the amygdala related to irritability, there is no comprehensive model between emotional, neuronal, and behavioral characteristics. Methods: Using an functional magnetic resonance imaging (fMRI) procedure, we investigated the relationships between behavioral irritability, selective impairments in processing facial emotions and the amygdala neural response in youth with increased irritability. Fifty-nine youth with disruptive mood and behavior disorder completed a facial expression processing task with an event-related fMRI paradigm. The severity of irritability was evaluated using the Affective Reactivity Index. Results: In the result of behavioral data, irritability, and reaction time (RT) differences between interpreting negative (fear) and positive (happiness) facial expressions were positively correlated. In the fMRI result, youth showed higher activation in the right cingulate gyrus, bilateral cerebellum, right amygdala, right precuneus, right superior frontal gyrus, right middle occipital gyrus, and middle temporal gyrus, during the happiness condition vs. fear condition. No brain region exhibited greater activation in the fear than in the happiness conditions. In the result of the mediator analysis, increased irritability was associated with a longer RT toward positive vs. negative facial expressions. Irritability was also positively associated with the difference in amygdala blood oxygen level-dependent responses between the two emotional conditions (happiness > fear). This difference in amygdala activity mediated the interaction between irritability and the RT difference between negative and positive facial expressions. Discussion: We suggest that impairment in the implicit processing of facial emotional expressions with different valences causes distinct patterns of amygdala response, which correlate with the level of irritability. These results broaden our understanding of the biological mechanism of irritability at the neural level and provide information for the future direction of the study.

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Authors
Suk, J.-W., Blair, R. J. R., Vaughan, B., Lerdahl, A., Garvey, W. F., Edwards, R., Leibenluft, E., & Hwang, S.
Affiliations
  • Korea Institute of Oriental Medicine (KR)
  • University of Nebraska Medical Center (US)
  • National Institute of Mental Health (US)
Corresponding author
Hwang, Soonjo
ORCID
Venue
Frontiers in Behavioral Neuroscience
Publisher
Frontiers Media SA
Published
2023-10-12
Volume
17
Pages
1204574-1204574
ISSN
1662-5153 (ISSN-L)
DOI
10.3389/fnbeh.2023.1204574
PMC
PMC10602729
OpenAlex
W4387580321
Cited by
7
References
70
Citations by year
2026: 1 · 2025: 6
FWCI
0.26
Type
journal article
Language
en
Open access
Licence
Locations
  • Frontiers in Behavioral Neuroscience (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Institutes of Health (5u01mh120155-03)
  • National Institute of Mental Health (U01-MH120155, U01MH120155-01A1)
  • National Institute of General Medical Sciences (U54GM115458)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
  • Social Sciences › Psychology › Clinical Psychology › Child and Adolescent Psychosocial and Emotional Development
  • Social Sciences › Psychology › Clinical Psychology › Psychopathy, Forensic Psychiatry, Sexual Offending
Keywords
irritability, amygdala, emotional face processing, reaction time, mediation, youth, Affective Reactivity Index, attention deficit hyperactivity disorder, oppositional defiant disorder, conduct disorder, disruptive mood dysregulation disorder

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