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Dispositional Negative Emotionality in Childhood and Adolescence Predicts Structural Variation in the Amygdala and Caudal Anterior Cingulate During Early Adulthood: Theoretically and Empirically Based Tests

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Abstract

Substantial evidence implicates the amygdala and related structures in the processing of negative emotions. Furthermore, neuroimaging evidence suggests that variations in amygdala volumes are related to trait-like individual differences in neuroticism/negative emotionality, although many questions remain about the nature of such associations. We conducted planned tests of the directional prediction that dispositional negative emotionality measured at 10–17 years using parent and youth ratings on the Child and Adolescent Dispositions Scale (CADS) would predict larger volumes of the amygdala in adulthood and conducted exploratory tests of associations with other regions implicated in emotion processing. Participants were 433 twins strategically selected for neuroimaging during wave 2 from wave 1 of the Tennessee Twins Study (TTS) by oversampling on internalizing and/or externalizing psychopathology risk. Controlling for age, sex, race-ethnicity, handedness, scanner, and total brain volume, youth-rated negative emotionality positively predicted bilateral amygdala volumes after correction for multiple testing. Each unit difference of one standard deviation (SD) in negative emotionality was associated with a .12 SD unit difference in larger volumes of both amygdalae. Parent-rated negative emotionality predicted greater thickness of the left caudal/dorsal anterior cingulate cortex (β = 0.28). Associations of brain structure with negative emotionality were not moderated by sex. These results are striking because dispositions assessed at 10–17 years of age were predictive of grey matter volumes measured 12–13 years later in adulthood. Future longitudinal studies should examine the timing of amygdala/cingulate associations with dispositional negative emotionality to determine when these associations emerge during development.

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Authors and Affiliations

  1. Department of Public Health Sciences (MC 2000), University of Chicago, 5841 S. Maryland Avenue, Chicago, IL, 606036, USA

    Benjamin B. Lahey & Xiaochan Yang

  2. Vanderbilt University, Nashville, TN, USA

    Kendra E. Hinton, Leah Burgess, Francisco C. Meyer, Bennett A. Landman, Victoria Villata-Gil & David H. Zald

  3. University of Texas At Austin, Austin, TX, USA

    Paul J. Rathouz

  4. Western Michigan University, Kalamazoo, MI, USA

    Brooks Applegate

Authors
  1. Benjamin B. Lahey
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  2. Kendra E. Hinton
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  3. Leah Burgess
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  4. Francisco C. Meyer
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  5. Bennett A. Landman
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  6. Victoria Villata-Gil
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  7. Xiaochan Yang
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  8. Paul J. Rathouz
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  9. Brooks Applegate
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  10. David H. Zald
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Correspondence to Benjamin B. Lahey.

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Lahey, B.B., Hinton, K.E., Burgess, L. et al. Dispositional Negative Emotionality in Childhood and Adolescence Predicts Structural Variation in the Amygdala and Caudal Anterior Cingulate During Early Adulthood: Theoretically and Empirically Based Tests. Res Child Adolesc Psychopathol 49, 1275–1288 (2021). https://doi.org/10.1007/s10802-021-00811-2

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