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. 2016 Nov 15:205:144-153.
doi: 10.1016/j.jad.2016.03.074. Epub 2016 Jul 1.

Preliminary investigation of the relationships between sleep duration, reward circuitry function, and mood dysregulation in youth offspring of parents with bipolar disorder

Adriane M Soehner #  1 , Michele A Bertocci #  1 , Anna Manelis  1 , Genna Bebko  1 , Cecile D Ladouceur  1 , Simona Graur  1 , Kelly Monk  1 , Lisa K Bonar  1 , Mary Beth Hickey  1 , David Axelson  2 , Benjamin I Goldstein  3 , Tina R Goldstein  1 , Boris Birmaher  1 , Mary L Phillips  1
Affiliations

Preliminary investigation of the relationships between sleep duration, reward circuitry function, and mood dysregulation in youth offspring of parents with bipolar disorder

Adriane M Soehner et al. J Affect Disord. .

Abstract

Background: Altered reward circuitry function is observed in individuals with bipolar disorder (BD) and their unaffected offspring (OBP). While OBP are at elevated risk for BD, modifiable risk factors that may exacerbate neural vulnerabilities in OBP remain under-characterized. As sleep loss is strongly linked to mania in BD, this study tested associations between sleep duration, reward circuitry function, and mood dysregulation in OBP.

Methods: Two groups of youth unaffected with BD (9-17yr) completed a number-guessing fMRI reward paradigm: 25 OBP and 21 age-sex-IQ-matched offspring of control parents with non-BD psychopathology (OCP), to differentiate risk for BD from risk for psychopathology more broadly. Regressions tested effects of group status, self-reported past-week sleep duration, and their interaction on neural activity and bilateral ventral striatum (VS) functional connectivity to win>control. Correlations with parent-reported mood dysregulation were assessed.

Results: Group effects were observed for right posterior insula activity (OCP>OBP) and VS-left posterior insula connectivity (OBP>OCP). Group⁎sleep duration interactions were observed for left dorsal anterior-mid-cingulate (daMCC) activity and VS-left anterior insula/ventrolateral prefrontal cortex (VLPFC) connectivity. Specifically, sleep duration and daMCC activity were positively related in OBP, but negatively related in OCP and sleep duration and VS-left anterior insula/VLPFC connectivity were negatively related in OBP, but positively in OCP. Additionally, increased VS-left posterior insula connectivity and VS-left anterior insula/VLPFC connectivity were associated with greater mood dysregulation in OBP only.

Limitations: Cross-sectional design and small sample size.

Conclusions: Altered reward-related VS-insula connectivity could represent a neural pathway underpinning mood dysregulation in OBP, and may be modulated by shortened sleep duration.

Keywords: Bipolar disorder risk; Functional MRI; Reward processing; Sleep.

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Figures

Figure 1
Figure 1
SPM regression analysis testing group, sleep duration, and group*sleep duration interaction as predictors of BOLD activity to win-control within the bilateral prefrontal-striatal ROI mask. (A) Significant group effect on BOLD activity in the right posterior insula [k=57, peak voxel MNI xyz= [45, −1, −5], t42=3.52, p=.001]. (B) Extracted right insula peak BOLD activity estimates plotted by group; means and standard error bars are presented, R2 represents variance explained for the overall regression. (C) Significant group*sleep duration interaction on left daMCC BOLD activity [k=41, peak voxel MNI xyz= [−3, 17, 37], t42=3.57, p<.001]. (D) Extracted left daMCC BOLD activity estimates plotted versus sleep duration for group*sleep duration interaction, trend lines indicate simple slopes for each group, R2 represents variance explained for the overall regression. OBP = offspring of bipolar parents; OCP = offspring of control parents; daMCC=dorsal anterior mid-cingulate cortex.
Figure 2
Figure 2
SPM regression analysis testing group, sleep duration, and group* sleep duration interaction as predictors of VS connectivity to win-control within the bilateral prefrontal cingulo-insular ROI mask. (A) Significant effect of group status on VS connectivity with the left posterior insula: k=59, peak voxel MNI xyz= [−42, −4, −5], t42=3.77, p<.001. (B) Extracted VS-Left posterior insula connectivity estimates displaying a significant difference between groups; means and standard error bars are presented, R2 represents variance explained for the overall regression. (C) Significant group*sleep duration interaction for VS connectivity with the left anterior insula/VLPFC: k=89, peak voxel MNI xyz= [−36, 8, −11], t42=3.11, p=.001. (D) Extracted VS-Left anterior insula/VLPFC connectivity estimates plotted versus sleep duration for group*sleep duration interaction, trend lines indicate simple slopes for each group, R2 represents variance explained for the overall regression. OBP=offspring of bipolar parents; OCP=offspring of control parents; VS=ventral striatum; VLPFC=ventrolateral prefrontal cortex.
Figure 3
Figure 3
Overlap in group (blue – left posterior insula) and group*sleep duration interaction (violet – left anterior insula/ventrolateral prefrontal cortex) effects in PPI analysis of VS connectivity to win-control within the bilateral prefrontal-cingulo-insular ROI target mask. PPI = psychophysiological interaction; VS = ventral striatum; ROI = region of interest.
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