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Published Online: 19 October 2018

Brain Mechanisms of Attention Orienting Following Frustration: Associations With Irritability and Age in Youths

Wan-Ling Tseng, Ph.D. [email protected], Christen M. Deveney, Ph.D., Joel Stoddard, M.D., Katharina Kircanski, Ph.D., Anna E. Frackman, M.D., Jennifer Y. Yi, M.A., Derek Hsu, M.D., Elizabeth Moroney, B.A., Laura Machlin, B.A., Laura Donahue, B.A., Alexandra Roule, B.A., Gretchen Perhamus, B.A., Richard C. Reynolds, M.S., Roxann Roberson-Nay, Ph.D., John M. Hettema, M.D., Ph.D., Kenneth E. Towbin, M.D., Argyris Stringaris, M.D., Ph.D., Daniel S. Pine, M.D., Melissa A. Brotman, Ph.D., and Ellen Leibenluft, M.D.Authors Info & Affiliations
Publication: American Journal of Psychiatry
Volume 176, Number 1
https://doi.org/10.1176/appi.ajp.2018.18040491
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Abstract

Objective:

Childhood irritability is a common, impairing problem with changing age-related manifestations that predict long-term adverse outcomes. However, more investigation of overall and age-specific neural correlates is needed. Because youths with irritability exhibit exaggerated responses to frustrating stimuli, the authors used a frustration functional MRI (fMRI) paradigm to examine associations between irritability and neural activation and tested the moderating effect of age.

Method:

The authors studied a transdiagnostic sample of 195 youths with varying levels of irritability (disruptive mood dysregulation disorder, N=52; anxiety disorder, N=42; attention deficit hyperactivity disorder, N=40; and healthy volunteers, N=61). Irritability was measured by parent and child reports on the Affective Reactivity Index. The fMRI paradigm was a cued-attention task differentiating neural activity in response to frustration (rigged feedback) from activity during attention orienting in the trial following frustration.

Results:

Whole-brain activation analyses revealed associations with irritability during attention orienting following frustration. Irritability was positively associated with frontal-striatal activation, specifically in the dorsolateral prefrontal cortex, inferior frontal gyrus, and caudate. Age moderated the association between irritability and activation in some frontal and posterior regions (the anterior cingulate cortex, medial frontal gyrus, cuneus, precuneus, and superior parietal lobule [F=19.04–28.51, df=1, 189, partial eta squared=0.09–0.13]). Specifically, higher irritability was more strongly related to increased activation in younger youths compared with older youths.

Conclusions:

Following frustration, levels of irritability correlated with activity in neural systems mediating attention orienting, top-down regulation of emotions, and motor execution. Although most associations were independent of age, dysfunction in the anterior cingulate cortex and posterior regions was more pronounced in young children with irritability.

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Information & Authors

Information

Published In

Go to American Journal of Psychiatry
Go to American Journal of Psychiatry
American Journal of Psychiatry
Volume 176 • Number 1 • January 01, 2019
Pages: 67 - 76
PubMed: 30336704

History

Received: 30 April 2018
Revision received: 3 July 2018
Accepted: 30 July 2018
Published online: 19 October 2018
Published in print: January 01, 2019

Keywords

  1. Irritability
  2. fMRI
  3. Age
  4. Frustrative Non-Reward
  5. Attention Orienting

Authors

Affiliations

Wan-Ling Tseng, Ph.D. [email protected]
From the Department of Health and Human Services, Emotion and Development Branch and Scientific and Statistical Computing Core, NIMH, Bethesda, Md.; the Department of Psychiatry and the Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, Richmond; the Department of Psychology, Wellesley College, Wellesley, Mass.; the University of Colorado School of Medicine, Aurora, Colo.; the Department of Medicine, Stanford University, Stanford, Calif.; the Departments of Psychology and Neuroscience, University of North Carolina at Chapel Hill; Emory University School of Medicine, Atlanta; the Department of Psychology, University of California at Los Angeles; and University of Michigan Medical School, Ann Arbor.
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Christen M. Deveney, Ph.D.
From the Department of Health and Human Services, Emotion and Development Branch and Scientific and Statistical Computing Core, NIMH, Bethesda, Md.; the Department of Psychiatry and the Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, Richmond; the Department of Psychology, Wellesley College, Wellesley, Mass.; the University of Colorado School of Medicine, Aurora, Colo.; the Department of Medicine, Stanford University, Stanford, Calif.; the Departments of Psychology and Neuroscience, University of North Carolina at Chapel Hill; Emory University School of Medicine, Atlanta; the Department of Psychology, University of California at Los Angeles; and University of Michigan Medical School, Ann Arbor.
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Joel Stoddard, M.D.
From the Department of Health and Human Services, Emotion and Development Branch and Scientific and Statistical Computing Core, NIMH, Bethesda, Md.; the Department of Psychiatry and the Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, Richmond; the Department of Psychology, Wellesley College, Wellesley, Mass.; the University of Colorado School of Medicine, Aurora, Colo.; the Department of Medicine, Stanford University, Stanford, Calif.; the Departments of Psychology and Neuroscience, University of North Carolina at Chapel Hill; Emory University School of Medicine, Atlanta; the Department of Psychology, University of California at Los Angeles; and University of Michigan Medical School, Ann Arbor.
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Katharina Kircanski, Ph.D.
From the Department of Health and Human Services, Emotion and Development Branch and Scientific and Statistical Computing Core, NIMH, Bethesda, Md.; the Department of Psychiatry and the Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, Richmond; the Department of Psychology, Wellesley College, Wellesley, Mass.; the University of Colorado School of Medicine, Aurora, Colo.; the Department of Medicine, Stanford University, Stanford, Calif.; the Departments of Psychology and Neuroscience, University of North Carolina at Chapel Hill; Emory University School of Medicine, Atlanta; the Department of Psychology, University of California at Los Angeles; and University of Michigan Medical School, Ann Arbor.
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Anna E. Frackman, M.D.
From the Department of Health and Human Services, Emotion and Development Branch and Scientific and Statistical Computing Core, NIMH, Bethesda, Md.; the Department of Psychiatry and the Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, Richmond; the Department of Psychology, Wellesley College, Wellesley, Mass.; the University of Colorado School of Medicine, Aurora, Colo.; the Department of Medicine, Stanford University, Stanford, Calif.; the Departments of Psychology and Neuroscience, University of North Carolina at Chapel Hill; Emory University School of Medicine, Atlanta; the Department of Psychology, University of California at Los Angeles; and University of Michigan Medical School, Ann Arbor.
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Jennifer Y. Yi, M.A.
From the Department of Health and Human Services, Emotion and Development Branch and Scientific and Statistical Computing Core, NIMH, Bethesda, Md.; the Department of Psychiatry and the Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, Richmond; the Department of Psychology, Wellesley College, Wellesley, Mass.; the University of Colorado School of Medicine, Aurora, Colo.; the Department of Medicine, Stanford University, Stanford, Calif.; the Departments of Psychology and Neuroscience, University of North Carolina at Chapel Hill; Emory University School of Medicine, Atlanta; the Department of Psychology, University of California at Los Angeles; and University of Michigan Medical School, Ann Arbor.
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Derek Hsu, M.D.
From the Department of Health and Human Services, Emotion and Development Branch and Scientific and Statistical Computing Core, NIMH, Bethesda, Md.; the Department of Psychiatry and the Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, Richmond; the Department of Psychology, Wellesley College, Wellesley, Mass.; the University of Colorado School of Medicine, Aurora, Colo.; the Department of Medicine, Stanford University, Stanford, Calif.; the Departments of Psychology and Neuroscience, University of North Carolina at Chapel Hill; Emory University School of Medicine, Atlanta; the Department of Psychology, University of California at Los Angeles; and University of Michigan Medical School, Ann Arbor.
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Elizabeth Moroney, B.A.
From the Department of Health and Human Services, Emotion and Development Branch and Scientific and Statistical Computing Core, NIMH, Bethesda, Md.; the Department of Psychiatry and the Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, Richmond; the Department of Psychology, Wellesley College, Wellesley, Mass.; the University of Colorado School of Medicine, Aurora, Colo.; the Department of Medicine, Stanford University, Stanford, Calif.; the Departments of Psychology and Neuroscience, University of North Carolina at Chapel Hill; Emory University School of Medicine, Atlanta; the Department of Psychology, University of California at Los Angeles; and University of Michigan Medical School, Ann Arbor.
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Laura Machlin, B.A.
From the Department of Health and Human Services, Emotion and Development Branch and Scientific and Statistical Computing Core, NIMH, Bethesda, Md.; the Department of Psychiatry and the Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, Richmond; the Department of Psychology, Wellesley College, Wellesley, Mass.; the University of Colorado School of Medicine, Aurora, Colo.; the Department of Medicine, Stanford University, Stanford, Calif.; the Departments of Psychology and Neuroscience, University of North Carolina at Chapel Hill; Emory University School of Medicine, Atlanta; the Department of Psychology, University of California at Los Angeles; and University of Michigan Medical School, Ann Arbor.
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Laura Donahue, B.A.
From the Department of Health and Human Services, Emotion and Development Branch and Scientific and Statistical Computing Core, NIMH, Bethesda, Md.; the Department of Psychiatry and the Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, Richmond; the Department of Psychology, Wellesley College, Wellesley, Mass.; the University of Colorado School of Medicine, Aurora, Colo.; the Department of Medicine, Stanford University, Stanford, Calif.; the Departments of Psychology and Neuroscience, University of North Carolina at Chapel Hill; Emory University School of Medicine, Atlanta; the Department of Psychology, University of California at Los Angeles; and University of Michigan Medical School, Ann Arbor.
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Alexandra Roule, B.A.
From the Department of Health and Human Services, Emotion and Development Branch and Scientific and Statistical Computing Core, NIMH, Bethesda, Md.; the Department of Psychiatry and the Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, Richmond; the Department of Psychology, Wellesley College, Wellesley, Mass.; the University of Colorado School of Medicine, Aurora, Colo.; the Department of Medicine, Stanford University, Stanford, Calif.; the Departments of Psychology and Neuroscience, University of North Carolina at Chapel Hill; Emory University School of Medicine, Atlanta; the Department of Psychology, University of California at Los Angeles; and University of Michigan Medical School, Ann Arbor.
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Gretchen Perhamus, B.A.
From the Department of Health and Human Services, Emotion and Development Branch and Scientific and Statistical Computing Core, NIMH, Bethesda, Md.; the Department of Psychiatry and the Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, Richmond; the Department of Psychology, Wellesley College, Wellesley, Mass.; the University of Colorado School of Medicine, Aurora, Colo.; the Department of Medicine, Stanford University, Stanford, Calif.; the Departments of Psychology and Neuroscience, University of North Carolina at Chapel Hill; Emory University School of Medicine, Atlanta; the Department of Psychology, University of California at Los Angeles; and University of Michigan Medical School, Ann Arbor.
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Richard C. Reynolds, M.S.
From the Department of Health and Human Services, Emotion and Development Branch and Scientific and Statistical Computing Core, NIMH, Bethesda, Md.; the Department of Psychiatry and the Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, Richmond; the Department of Psychology, Wellesley College, Wellesley, Mass.; the University of Colorado School of Medicine, Aurora, Colo.; the Department of Medicine, Stanford University, Stanford, Calif.; the Departments of Psychology and Neuroscience, University of North Carolina at Chapel Hill; Emory University School of Medicine, Atlanta; the Department of Psychology, University of California at Los Angeles; and University of Michigan Medical School, Ann Arbor.
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Roxann Roberson-Nay, Ph.D.
From the Department of Health and Human Services, Emotion and Development Branch and Scientific and Statistical Computing Core, NIMH, Bethesda, Md.; the Department of Psychiatry and the Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, Richmond; the Department of Psychology, Wellesley College, Wellesley, Mass.; the University of Colorado School of Medicine, Aurora, Colo.; the Department of Medicine, Stanford University, Stanford, Calif.; the Departments of Psychology and Neuroscience, University of North Carolina at Chapel Hill; Emory University School of Medicine, Atlanta; the Department of Psychology, University of California at Los Angeles; and University of Michigan Medical School, Ann Arbor.
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John M. Hettema, M.D., Ph.D.
From the Department of Health and Human Services, Emotion and Development Branch and Scientific and Statistical Computing Core, NIMH, Bethesda, Md.; the Department of Psychiatry and the Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, Richmond; the Department of Psychology, Wellesley College, Wellesley, Mass.; the University of Colorado School of Medicine, Aurora, Colo.; the Department of Medicine, Stanford University, Stanford, Calif.; the Departments of Psychology and Neuroscience, University of North Carolina at Chapel Hill; Emory University School of Medicine, Atlanta; the Department of Psychology, University of California at Los Angeles; and University of Michigan Medical School, Ann Arbor.
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Kenneth E. Towbin, M.D.
From the Department of Health and Human Services, Emotion and Development Branch and Scientific and Statistical Computing Core, NIMH, Bethesda, Md.; the Department of Psychiatry and the Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, Richmond; the Department of Psychology, Wellesley College, Wellesley, Mass.; the University of Colorado School of Medicine, Aurora, Colo.; the Department of Medicine, Stanford University, Stanford, Calif.; the Departments of Psychology and Neuroscience, University of North Carolina at Chapel Hill; Emory University School of Medicine, Atlanta; the Department of Psychology, University of California at Los Angeles; and University of Michigan Medical School, Ann Arbor.
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Argyris Stringaris, M.D., Ph.D.
From the Department of Health and Human Services, Emotion and Development Branch and Scientific and Statistical Computing Core, NIMH, Bethesda, Md.; the Department of Psychiatry and the Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, Richmond; the Department of Psychology, Wellesley College, Wellesley, Mass.; the University of Colorado School of Medicine, Aurora, Colo.; the Department of Medicine, Stanford University, Stanford, Calif.; the Departments of Psychology and Neuroscience, University of North Carolina at Chapel Hill; Emory University School of Medicine, Atlanta; the Department of Psychology, University of California at Los Angeles; and University of Michigan Medical School, Ann Arbor.
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Daniel S. Pine, M.D.
From the Department of Health and Human Services, Emotion and Development Branch and Scientific and Statistical Computing Core, NIMH, Bethesda, Md.; the Department of Psychiatry and the Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, Richmond; the Department of Psychology, Wellesley College, Wellesley, Mass.; the University of Colorado School of Medicine, Aurora, Colo.; the Department of Medicine, Stanford University, Stanford, Calif.; the Departments of Psychology and Neuroscience, University of North Carolina at Chapel Hill; Emory University School of Medicine, Atlanta; the Department of Psychology, University of California at Los Angeles; and University of Michigan Medical School, Ann Arbor.
View all articles by this author
Melissa A. Brotman, Ph.D.
From the Department of Health and Human Services, Emotion and Development Branch and Scientific and Statistical Computing Core, NIMH, Bethesda, Md.; the Department of Psychiatry and the Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, Richmond; the Department of Psychology, Wellesley College, Wellesley, Mass.; the University of Colorado School of Medicine, Aurora, Colo.; the Department of Medicine, Stanford University, Stanford, Calif.; the Departments of Psychology and Neuroscience, University of North Carolina at Chapel Hill; Emory University School of Medicine, Atlanta; the Department of Psychology, University of California at Los Angeles; and University of Michigan Medical School, Ann Arbor.
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Ellen Leibenluft, M.D.
From the Department of Health and Human Services, Emotion and Development Branch and Scientific and Statistical Computing Core, NIMH, Bethesda, Md.; the Department of Psychiatry and the Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, Richmond; the Department of Psychology, Wellesley College, Wellesley, Mass.; the University of Colorado School of Medicine, Aurora, Colo.; the Department of Medicine, Stanford University, Stanford, Calif.; the Departments of Psychology and Neuroscience, University of North Carolina at Chapel Hill; Emory University School of Medicine, Atlanta; the Department of Psychology, University of California at Los Angeles; and University of Michigan Medical School, Ann Arbor.
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Notes

Send correspondence to Dr. Tseng ([email protected]).

Competing Interests

Drs. Tseng and Stoddard have received research grant support from NIMH (grant K99MH110570 to Dr. Tseng and grant K23MH113731 to Dr. Stoddard). The other authors report no financial relationships with commercial interests.

Funding Information

National Institute of Mental Health10.13039/100000025: ZIA-MH-002781, ZIA-MH002778, ZIA44 MH002786
Supported by the Intramural Research Program of NIMH, conducted under projects ZIA-MH002778 (clinical protocol NCT00006177), ZIA-MH002781 (clinical protocol NCT00018057), and ZIA-MH002786 (clinical protocol NCT00025935).

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