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Levels of early-childhood behavioral inhibition predict distinct neurodevelopmental pathways to pediatric anxiety

Published online by Cambridge University Press:  08 January 2019

Rany Abend ,
Caroline Swetlitz ,
Lauren K. White ,
Tomer Shechner ,
Yair Bar-Haim ,
Courtney Filippi ,
Katharina Kircanski ,
Simone P. Haller ,
Brenda E. Benson  and
Gang Chen
...Show all authors
Rany Abend*
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, Bethesda, MD, USA
Caroline Swetlitz
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, Bethesda, MD, USA
Lauren K. White
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, Bethesda, MD, USA Childrenʼs Hospital of Philadelphia, Philadelphia, PA, USA
Tomer Shechner
Affiliation:
Psychology Department, University of Haifa, Haifa, Israel
Yair Bar-Haim
Affiliation:
School of Psychological Sciences and Sagol School of Neuroscience, Tel Aviv University, Tel Aviv, Israel
Courtney Filippi
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, Bethesda, MD, USA
Katharina Kircanski
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, Bethesda, MD, USA
Simone P. Haller
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, Bethesda, MD, USA
Brenda E. Benson
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, Bethesda, MD, USA
Gang Chen
Affiliation:
Scientific and Statistical Computing Core, National Institute of Mental Health, Bethesda, MD, USA
Ellen Leibenluft
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, Bethesda, MD, USA
Nathan A. Fox
Affiliation:
Department of Human Development and Quantitative Methodology, University of Maryland, College Park, MD, USA
Daniel S. Pine
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, Bethesda, MD, USA
*
Author for correspondence: Rany Abend, E-mail: rany.abend@nih.gov
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Abstract

Background

Anxiety symptoms gradually emerge during childhood and adolescence. Individual differences in behavioral inhibition (BI), an early-childhood temperament, may shape developmental paths through which these symptoms arise. Cross-sectional research suggests that level of early-childhood BI moderates associations between later anxiety symptoms and threat-related amygdala–prefrontal cortex (PFC) circuitry function. However, no study has characterized these associations longitudinally. Here, we tested whether level of early-childhood BI predicts distinct evolving associations between amygdala–PFC function and anxiety symptoms across development.

Methods

Eighty-seven children previously assessed for BI level in early childhood provided data at ages 10 and/or 13 years, consisting of assessments of anxiety and an fMRI-based dot-probe task (including threat, happy, and neutral stimuli). Using linear-mixed-effects models, we investigated longitudinal changes in associations between anxiety symptoms and threat-related amygdala–PFC connectivity, as a function of early-childhood BI.

Results

In children with a history of high early-childhood BI, anxiety symptoms became, with age, more negatively associated with right amygdala–left dorsolateral-PFC connectivity when attention was to be maintained on threat. In contrast, with age, low-BI children showed an increasingly positive anxiety–connectivity association during the same task condition. Behaviorally, at age 10, anxiety symptoms did not relate to fluctuations in attention bias (attention bias variability, ABV) in either group; by age 13, low-BI children showed a negative anxiety–ABV association, whereas high-BI children showed a positive anxiety–ABV association.

Conclusions

Early-childhood BI levels predict distinct neurodevelopmental pathways to pediatric anxiety symptoms. These pathways involve distinct relations among brain function, behavior, and anxiety symptoms, which may inform diagnosis and treatment.

Keywords

Amygdalaanxietyattentionbehavioral inhibitionchildrenconnectivitydevelopmentalfMRIprefrontal cortex
Type
Original Articles
Information
Psychological Medicine , Volume 50 , Issue 1 , January 2020 , pp. 96 - 106
Copyright
Copyright © Cambridge University Press 2019 

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