The longitudinal association between externalizing behavior and frontoamygdalar resting-state functional connectivity in late adolescence and young adulthood

Sandra Thijssen, Paul F. Collins, Hannah Weiss, Monica Luciana

Research output: Contribution to journalArticlepeer-review

Abstract

Background: Externalizing behavior has been attributed, in part, to decreased frontolimbic control over amygdala activation. However, little is known about developmental trajectories of frontoamygdalar functional connectivity and its relation to externalizing behavior. The present study addresses this gap by examining longitudinal associations between adolescent and adult externalizing behavior and amygdala–anterior cingulate cortex (ACC) and amygdala–orbitofrontal cortex (OFC) resting-state functional connectivity in a sample of 111 typically developing participants aged 11–23 at baseline. Methods: Participants completed two-to-four data waves spaced approximately two years apart, resulting in a total of 309 data points. At each data wave, externalizing behavior was measured using the Externalizing Behavior Broadband Scale from the Achenbach Youth/Adult Self-Report questionnaire. Resting-state fMRI preprocessing was performed using FSL. Amygdala functional connectivity was examined using AFNI. The longitudinal association between externalizing behavior and amygdala–ACC/OFC functional connectivity was examined using linear mixed effect models in R. Results: Externalizing behavior was associated with increased amygdala–ACC and amygdala–OFC resting-state functional connectivity across adolescence and young adulthood. For amygdala–ACC connectivity, externalizing behavior at baseline primarily drove this association, whereas for amygdala–OFC functional connectivity, change in externalizing behavior relative to baseline drove the main effect of externalizing behavior on amygdala–OFC functional connectivity. No evidence was found for differential developmental trajectories of frontoamygdalar connectivity for different levels of externalizing behavior (i.e., age-by-externalizing behavior interaction effect). Conclusions: Higher externalizing behavior is associated with increased resting-state attunement between the amygdala and ACC/OFC, perhaps indicating a generally more vigilant state for neural networks important for emotional processing and control.

Original languageEnglish (US)
Pages (from-to)857-867
Number of pages11
JournalJournal of Child Psychology and Psychiatry and Allied Disciplines
Volume62
Issue number7
Early online dateSep 20 2020
DOIs
StatePublished - Sep 20 2020

Bibliographical note

Funding Information:
Data collection and analysis were supported by National Institute on Drug Abuse Grant R01 DA 017843 and National Institute of Alcohol Abuse and Alcoholism Grant AA020033 to M.L. The present study was also supported by BTRC grants awarded to the UMN Center for Magnetic Resonance Research, P41 RR008079, P41 EB015894, and 1P30 NS076408. S.T. was supported by a Rubicon grant (446‐16‐022) of the Netherlands Organisation for Scientific Research. The authors would like to thank the Center for Neurobehavioral Development and the University of Minnesota’s Supercomputing Institute for support of the presented research. The authors have declared that they have no competing or potential conflicts of interest. Key points

Funding Information:
Data collection and analysis were supported by National Institute on Drug Abuse Grant R01 DA 017843 and National Institute of Alcohol Abuse and Alcoholism Grant AA020033 to M.L. The present study was also supported by BTRC grants awarded to the UMN Center for Magnetic Resonance Research, P41 RR008079, P41 EB015894, and 1P30 NS076408. S.T. was supported by a Rubicon grant (446-16-022) of the Netherlands Organisation for Scientific Research. The authors would like to thank the Center for Neurobehavioral Development and the University of Minnesota?s Supercomputing Institute for support of the presented research. The authors have declared that they have no competing or potential conflicts of interest.Key points Externalizing behavior has been associated with amygdala?anterior cingulate (ACC) and amygdala?orbitofrontal cortex (OFC) resting-state functional connectivity. It is currently unknown how this association develops over age. From age 11 to 32, externalizing behavior is consistently associated with increased amygdala?anterior cingulate (ACC) and amygdala?orbitofrontal cortex (OFC) functional connectivity. For amygdala?ACC connectivity, externalizing behavior at baseline primarily drove this association. For amygdala?OFC functional connectivity, change in externalizing behavior relative to baseline drove the longitudinal effect of externalizing behavior on amygdala?OFC functional connectivity. No evidence was found for differential developmental trajectories of frontoamygdalar connectivity for different levels of externalizing behavior (i.e., age-by-externalizing behavior interaction effect). Externalizing behavior has been associated with amygdala?anterior cingulate (ACC) and amygdala?orbitofrontal cortex (OFC) resting-state functional connectivity. It is currently unknown how this association develops over age. From age 11 to 32, externalizing behavior is consistently associated with increased amygdala?anterior cingulate (ACC) and amygdala?orbitofrontal cortex (OFC) functional connectivity. For amygdala?ACC connectivity, externalizing behavior at baseline primarily drove this association. For amygdala?OFC functional connectivity, change in externalizing behavior relative to baseline drove the longitudinal effect of externalizing behavior on amygdala?OFC functional connectivity. No evidence was found for differential developmental trajectories of frontoamygdalar connectivity for different levels of externalizing behavior (i.e., age-by-externalizing behavior interaction effect).

Publisher Copyright:
© 2020 The Authors. Journal of Child Psychology and Psychiatry published by John Wiley & Sons Ltd on behalf of Association for Child and Adolescent Mental Health

Keywords

  • Externalizing behavior
  • amygdala
  • anterior cingulate cortex
  • functional connectivity
  • orbitofrontal cortex

PubMed: MeSH publication types

  • Journal Article

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