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Original Investigation |

Parsing Dimensional vs Diagnostic Category–Related Patterns of Reward Circuitry Function in Behaviorally and Emotionally Dysregulated Youth in the Longitudinal Assessment of Manic Symptoms Study

Genna Bebko, PhD1; Michele A. Bertocci, PhD1; Jay C. Fournier, PhD1; Amanda K. Hinze, MS1; Lisa Bonar, BS1; Jorge R. C. Almeida, MD, PhD1; Susan B. Perlman, PhD1; Amelia Versace, MD1; Claudiu Schirda, PhD1; Michael Travis, MD1; Mary Kay Gill, RN, MSN1; Christine Demeter, MA2; Vaibhav A. Diwadkar, PhD3; Gary Ciuffetelli, BA1; Eric Rodriguez, BS1; Thomas Olino, PhD1; Erika Forbes, PhD1; Jeffrey L. Sunshine, MD, PhD2; Scott K. Holland, PhD4; Robert A. Kowatch, MD, PhD5; Boris Birmaher, MD1; David Axelson, MD1; Sarah M. Horwitz, PhD6; L. Eugene Arnold, MD, MEd7; Mary A. Fristad, PhD, ABPP7; Eric A. Youngstrom, PhD8; Robert L. Findling, MD, MBA2,9; Mary L. Phillips, MD, MD (Cantab)1,10
[+] Author Affiliations
1Department of Psychiatry, Western Psychiatric Institute and Clinic, University of Pittsburgh Medical Center, University of Pittsburgh, Pittsburgh, Pennsylvania
2Division of Child and Adolescent Psychiatry, University Hospitals Case Medical Center/Case Western Reserve University, Cleveland, Ohio
3Department of Psychiatry and Behavioral Neuroscience, Wayne State University, Detroit, Michigan
4Division of Pediatric Radiology, Cincinnati Children’s Hospital Medical Center, University of Cincinnati, Cincinnati, Ohio
5Research Institute, Nationwide Children’s Hospital, Columbus, Ohio
6Department of Child Psychiatry, School of Medicine, New York University, New York
7Department of Psychiatry, The Ohio State University, Columbus
8Department of Psychology, University of North Carolina, Chapel Hill
9Department of Psychiatry, Johns Hopkins University, Baltimore, Maryland
10Department of Psychological Medicine, Cardiff University, Cardiff, United Kingdom
JAMA Psychiatry. 2014;71(1):71-80. doi:10.1001/jamapsychiatry.2013.2870.
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Importance  Pediatric disorders characterized by behavioral and emotional dysregulation pose diagnostic and treatment challenges because of high comorbidity, suggesting that they may be better conceptualized dimensionally rather than categorically. Identifying neuroimaging measures associated with behavioral and emotional dysregulation in youth may inform understanding of underlying dimensional vs disorder-specific pathophysiologic features.

Objective  To identify, in a large cohort of behaviorally and emotionally dysregulated youth, neuroimaging measures that (1) are associated with behavioral and emotional dysregulation pathologic dimensions (behavioral and emotional dysregulation measured with the Parent General Behavior Inventory 10-Item Mania Scale [PGBI-10M], mania, depression, and anxiety) or (2) differentiate diagnostic categories (bipolar spectrum disorders, attention-deficit/hyperactivity disorder, anxiety, and disruptive behavior disorders).

Design, Setting, and Participants  A multisite neuroimaging study was conducted from February 1, 2011, to April 15, 2012, at 3 academic medical centers: University Hospitals Case Medical Center, Cincinnati Children’s Hospital Medical Center, and University of Pittsburgh Medical Center. Participants included a referred sample of behaviorally and emotionally dysregulated youth from the Longitudinal Assessment of Manic Symptoms (LAMS) study (n = 85) and healthy youth (n = 20).

Main Outcomes and Measures  Region-of-interest analyses examined relationships among prefrontal-ventral striatal reward circuitry during a reward paradigm (win, loss, and control conditions), symptom dimensions, and diagnostic categories.

Results  Regardless of diagnosis, higher PGBI-10M scores were associated with greater left middle prefrontal cortical activity (r = 0.28) and anxiety with greater right dorsal anterior cingulate cortical (r = 0.27) activity to win. The 20 highest (t = 2.75) and 20 lowest (t = 2.42) PGBI-10M–scoring youth showed significantly greater left middle prefrontal cortical activity to win compared with 20 healthy youth. Disruptive behavior disorders were associated with lower left ventrolateral prefrontal cortex activity to win (t = 2.68) (all P < .05, corrected).

Conclusions and Relevance  Greater PGBI-10M–related left middle prefrontal cortical activity and anxiety-related right dorsal anterior cingulate cortical activity to win may reflect heightened reward sensitivity and greater attention to reward in behaviorally and emotionally dysregulated youth regardless of diagnosis. Reduced left ventrolateral prefrontal cortex activity to win may reflect reward insensitivity in youth with disruptive behavior disorders. Despite a distinct reward-related neurophysiologic feature in disruptive behavior disorders, findings generally support a dimensional approach to studying neural mechanisms in behaviorally and emotionally dysregulated youth.

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Figure 1.
Adapted Reward Task40

Participants guessed whether a card (value, 1-9) was higher/lower than 5, then viewed the number, outcome (win, green arrow; loss, red arrow), and fixation cross. In control trials, participants pressed a button marked “X,” then viewed an asterisk, circle, and fixation cross.

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Figure 2.
Entire Bilateral Region of Interest Mask Analysis to Win > Control in 85 Longitudinal Assessment of Manic Symptoms Youth

A, Left middle prefrontal cortical (mPFC), bilateral dorsal anterior cingulate cortical (dACC), and bilateral ventrolateral prefrontal cortex (VLPFC) activity (orange). B, Left mPFC activity and Parent General Behavior Inventory 10-Item Mania Scale (PGBI-10M) (teal) (r = 0.28). C, Overlap between left mPFC activity in A and B. D, Bilateral dACC activity and Screen for Child Anxiety Related Emotional Disorders (SCARED) (purple) (r = 0.27). E, Overlap between dACC activity in A and D. Markings on color bars indicate t test values; BA, Brodmann area; BOLD, blood oxygen level dependent; and SCARED.

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Figure 3.
Group Contrast of Win > Control Activity in Left Middle Prefrontal Cortical (mPFC) Clusters Determined in Analyses Depicted in Figure 2A

Relative to healthy youth (n = 20) (black) Longitudinal Assessment of Manic Symptoms (LAMS) youth with high Parent General Behavior Inventory 10-Item Mania Scale (PGBI-10M) scores (n = 20) (red) and LAMS youth with low PGBI-10M scores (n = 20) (blue) had greater left mPFC activity. Markings on color bars indicate t test values; error bars, SD. BA indicates Brodmann area; BOLD, blood oxygen level dependent.aStatistically significant difference.

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