Amygdala-prefrontal cortical functional connectivity during implicit emotion processing differentiates youth with bipolar spectrum from youth with externalizing disorders

Danella Hafeman, Genna Bebko, Michele A. Bertocci, Jay C. Fournier, Henry W. Chase, Lisa Bonar, Susan B. Perlman, Michael Travis, Mary Kay Gill, Vaibhav A. Diwadkar, Jeffrey L. Sunshine, Scott K. Holland, Robert A. Kowatch, Boris Birmaher, David Axelson, Sarah M. Horwitz, L. Eugene Arnold, Mary A. Fristad, Thomas W. Frazier, Eric A. Youngstrom & 2 others Robert L. Findling, Mary L. Phillips

Research output: Research - peer-reviewArticle

Abstract

Objective Both bipolar spectrum disorders (BPSD) and attention deficit hyperactivity disorder (ADHD) present with emotion-regulation deficits, but require different clinical management. We examined how the neurobiological underpinnings of emotion regulation might differentiate youth with BPSD versus ADHD (and healthy controls, HCs), specifically assessing functional connectivity (FxC) of amygdala-prefrontal circuitry during an implicit emotion processing task. Methods We scanned a subset of the Longitudinal Assessment of Manic Symptoms (LAMS) sample, a clinically recruited cohort with elevated behavioral and emotional dysregulation, and age/sex-ratio matched HCs. Our sample consisted of 22 youth with BPSD, 30 youth with ADHD/no BPSD, and 26 HCs. We used generalized psychophysiological interaction (gPPI) to calculate group differences to emerging emotional faces vs. morphing shapes in FxC between bilateral amygdala and ventral prefrontal cortex/anterior cingulate cortex. Results FxC between amygdala and left ventrolateral prefrontal cortex (VLPFC) in response to emotions vs. shapes differed by group (p=.05): while BPSD showed positive FxC (emotions>shapes), HC and ADHD showed inverse FxC (emotions<shapes). A group x emotion interaction was found in amygdala-subgenual cingulate FxC (p=.025), explained by differences in FxC in response to negative emotions. While BPSD showed positive FxC, HC showed inverse FxC; ADHD were intermediate. Amygdala-subgenual FxC was also positively associated with depressive symptoms and stimulant medication. Limitations Co-morbidity and relatively small sample size. Conclusions Youth with BPSD showed abnormally positive FxC between amygdala and regions in the ventral prefrontal cortex during emotion processing. In particular, the amygdala-VLPFC finding was specific to BPSD, and not influenced by other diagnoses or medications.

LanguageEnglish (US)
Pages94-100
Number of pages7
JournalJournal of Affective Disorders
Volume208
DOIs
StatePublished - Jan 15 2017

Fingerprint

Emotions
Olfactory Cortex
Bipolar Disorder
Amygdala
Attention Deficit Disorder with Hyperactivity
Prefrontal Cortex
Symptom Assessment
Gyrus Cinguli
Sex Ratio
Sample Size
Depression
Morbidity

Keywords

  • Bipolar disorder
  • fMRI
  • Implicit emotion processing
  • Neuroimaging

ASJC Scopus subject areas

  • Clinical Psychology
  • Psychiatry and Mental health

Cite this

Amygdala-prefrontal cortical functional connectivity during implicit emotion processing differentiates youth with bipolar spectrum from youth with externalizing disorders. / Hafeman, Danella; Bebko, Genna; Bertocci, Michele A.; Fournier, Jay C.; Chase, Henry W.; Bonar, Lisa; Perlman, Susan B.; Travis, Michael; Gill, Mary Kay; Diwadkar, Vaibhav A.; Sunshine, Jeffrey L.; Holland, Scott K.; Kowatch, Robert A.; Birmaher, Boris; Axelson, David; Horwitz, Sarah M.; Arnold, L. Eugene; Fristad, Mary A.; Frazier, Thomas W.; Youngstrom, Eric A.; Findling, Robert L.; Phillips, Mary L.

In: Journal of Affective Disorders, Vol. 208, 15.01.2017, p. 94-100.

Research output: Research - peer-reviewArticle

Hafeman, D, Bebko, G, Bertocci, MA, Fournier, JC, Chase, HW, Bonar, L, Perlman, SB, Travis, M, Gill, MK, Diwadkar, VA, Sunshine, JL, Holland, SK, Kowatch, RA, Birmaher, B, Axelson, D, Horwitz, SM, Arnold, LE, Fristad, MA, Frazier, TW, Youngstrom, EA, Findling, RL & Phillips, ML 2017, 'Amygdala-prefrontal cortical functional connectivity during implicit emotion processing differentiates youth with bipolar spectrum from youth with externalizing disorders' Journal of Affective Disorders, vol 208, pp. 94-100. DOI: 10.1016/j.jad.2016.09.064
Hafeman, Danella ; Bebko, Genna ; Bertocci, Michele A. ; Fournier, Jay C. ; Chase, Henry W. ; Bonar, Lisa ; Perlman, Susan B. ; Travis, Michael ; Gill, Mary Kay ; Diwadkar, Vaibhav A. ; Sunshine, Jeffrey L. ; Holland, Scott K. ; Kowatch, Robert A. ; Birmaher, Boris ; Axelson, David ; Horwitz, Sarah M. ; Arnold, L. Eugene ; Fristad, Mary A. ; Frazier, Thomas W. ; Youngstrom, Eric A. ; Findling, Robert L. ; Phillips, Mary L./ Amygdala-prefrontal cortical functional connectivity during implicit emotion processing differentiates youth with bipolar spectrum from youth with externalizing disorders. In: Journal of Affective Disorders. 2017 ; Vol. 208. pp. 94-100
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N2 - Objective Both bipolar spectrum disorders (BPSD) and attention deficit hyperactivity disorder (ADHD) present with emotion-regulation deficits, but require different clinical management. We examined how the neurobiological underpinnings of emotion regulation might differentiate youth with BPSD versus ADHD (and healthy controls, HCs), specifically assessing functional connectivity (FxC) of amygdala-prefrontal circuitry during an implicit emotion processing task. Methods We scanned a subset of the Longitudinal Assessment of Manic Symptoms (LAMS) sample, a clinically recruited cohort with elevated behavioral and emotional dysregulation, and age/sex-ratio matched HCs. Our sample consisted of 22 youth with BPSD, 30 youth with ADHD/no BPSD, and 26 HCs. We used generalized psychophysiological interaction (gPPI) to calculate group differences to emerging emotional faces vs. morphing shapes in FxC between bilateral amygdala and ventral prefrontal cortex/anterior cingulate cortex. Results FxC between amygdala and left ventrolateral prefrontal cortex (VLPFC) in response to emotions vs. shapes differed by group (p=.05): while BPSD showed positive FxC (emotions>shapes), HC and ADHD showed inverse FxC (emotions

AB - Objective Both bipolar spectrum disorders (BPSD) and attention deficit hyperactivity disorder (ADHD) present with emotion-regulation deficits, but require different clinical management. We examined how the neurobiological underpinnings of emotion regulation might differentiate youth with BPSD versus ADHD (and healthy controls, HCs), specifically assessing functional connectivity (FxC) of amygdala-prefrontal circuitry during an implicit emotion processing task. Methods We scanned a subset of the Longitudinal Assessment of Manic Symptoms (LAMS) sample, a clinically recruited cohort with elevated behavioral and emotional dysregulation, and age/sex-ratio matched HCs. Our sample consisted of 22 youth with BPSD, 30 youth with ADHD/no BPSD, and 26 HCs. We used generalized psychophysiological interaction (gPPI) to calculate group differences to emerging emotional faces vs. morphing shapes in FxC between bilateral amygdala and ventral prefrontal cortex/anterior cingulate cortex. Results FxC between amygdala and left ventrolateral prefrontal cortex (VLPFC) in response to emotions vs. shapes differed by group (p=.05): while BPSD showed positive FxC (emotions>shapes), HC and ADHD showed inverse FxC (emotions

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