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Fronto-limbic-striatal dysfunction in pediatric and adult patients with bipolar disorder: impact of face emotion and attentional demands

Published online by Cambridge University Press:  12 August 2013

M. A. Brotman ,
W.-L. Tseng ,
A. K. Olsavsky ,
S. J. Fromm ,
E. J. Muhrer ,
J. G. Rutenberg ,
C. M. Deveney ,
N. E. Adleman ,
C. A. Zarate Jr.  and
D. S. Pine
...Show all authors
M. A. Brotman*
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
W.-L. Tseng
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
A. K. Olsavsky
Affiliation:
Semel Institute for Neuroscience and Human Behavior at UCLA, Los Angeles, CA, USA
S. J. Fromm
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
E. J. Muhrer
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
J. G. Rutenberg
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
C. M. Deveney
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
N. E. Adleman
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
C. A. Zarate Jr.
Affiliation:
Experimental Therapeutics and Pathophysiology Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
D. S. Pine
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
E. Leibenluft
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, MD, USA
*
*Address for correspondence: M. A. Brotman, Ph.D., Building 10, Room B1D43C, 10 Center Drive, Bethesda, MD 20892, USA. (Email: [email protected])
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Abstract

Background

Research in bipolar disorder (BD) implicates fronto-limbic-striatal dysfunction during face emotion processing but it is unknown how such dysfunction varies by task demands, face emotion and patient age.

Method

During functional magnetic resonance imaging (fMRI), 181 participants, including 62 BD (36 children and 26 adults) and 119 healthy comparison (HC) subjects (57 children and 62 adults), engaged in constrained and unconstrained processing of emotional (angry, fearful, happy) and non-emotional (neutral) faces. During constrained processing, subjects answered questions focusing their attention on the face; this was processed either implicitly (nose width rating) or explicitly (hostility; subjective fear ratings). Unconstrained processing consisted of passive viewing.

Results

Pediatric BD rated neutral faces as more hostile than did other groups. In BD patients, family-wise error (FWE)-corrected region of interest (ROI) analyses revealed dysfunction in the amygdala, inferior frontal gyrus (IFG), anterior cingulate cortex (ACC) and putamen. Patients with BD showed amygdala hyperactivation during explicit processing (hostility ratings) of fearful faces and passive viewing of angry and neutral faces but IFG hypoactivation during implicit processing of neutral and happy faces. In the ACC and striatum, the direction of dysfunction varied by task demand: BD demonstrated hyperactivation during unconstrained processing of angry or neutral faces but hypoactivation during constrained processing (implicit or explicit) of angry, neutral or happy faces.

Conclusions

Findings suggest amygdala hyperactivation in BD while processing negatively valenced and neutral faces, regardless of attentional condition, and BD IFG hypoactivation during implicit processing. In the cognitive control circuit involving the ACC and putamen, BD neural dysfunction was sensitive to task demands.

Keywords

Attentionbipolar disorderface emotionfronto-limbic-striatal dysfunctionimagingpediatric
Type
Original Articles
Information
Psychological Medicine , Volume 44 , Issue 8 , June 2014 , pp. 1639 - 1651
Copyright
Copyright © Cambridge University Press 2013 

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