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Research Articles, Behavioral/Cognitive

Functional Connectivity within the Primate Extended Amygdala Is Heritable and Associated with Early-Life Anxious Temperament

Andrew S. Fox, Jonathan A. Oler, Rasmus M. Birn, Alexander J. Shackman, Andrew L. Alexander and Ned H. Kalin
Journal of Neuroscience 29 August 2018, 38 (35) 7611-7621; DOI: https://doi.org/10.1523/JNEUROSCI.0102-18.2018
Andrew S. Fox
2Department of Psychology and California National Primate Research Center, University of California, Davis, California 95616,
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Jonathan A. Oler
1Department of Psychiatry, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin 53719,
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Rasmus M. Birn
1Department of Psychiatry, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin 53719,
3Department of Medical Physics, University of Wisconsin, Madison, Wisconsin 53705,
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Alexander J. Shackman
4Department of Psychology, Maryland Neuroimaging Center, and Neuroscience and Cognitive Science Program, University of Maryland, College Park, Maryland 20742, and
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Andrew L. Alexander
1Department of Psychiatry, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin 53719,
3Department of Medical Physics, University of Wisconsin, Madison, Wisconsin 53705,
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Ned H. Kalin
1Department of Psychiatry, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin 53719,
5Wisconsin National Primate Research Center, Madison, Wisconsin 53715
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Abstract

Children with an extremely inhibited, anxious temperament (AT) are at increased risk for anxiety disorders and depression. Using a rhesus monkey model of early-life AT, we previously demonstrated that metabolism in the central extended amygdala (EAc), including the central nucleus of the amygdala (Ce) and bed nucleus of the stria terminalis (BST), is associated with trait-like variation in AT. Here, we use fMRI to examine relationships between Ce–BST functional connectivity and AT in a large multigenerational family pedigree of rhesus monkeys (n = 170 females and 208 males). Results demonstrate that Ce–BST functional connectivity is heritable, accounts for a significant but modest portion of the variance in AT, and is coheritable with AT. Interestingly, Ce–BST functional connectivity and AT-related BST metabolism were not correlated and accounted for non-overlapping variance in AT. Exploratory analyses suggest that Ce–BST functional connectivity is associated with metabolism in the hypothalamus and periaqueductal gray. Together, these results suggest the importance of coordinated function within the EAc for determining individual differences in AT and metabolism in brain regions associated with its behavioral and neuroendocrine components.

SIGNIFICANCE STATEMENT Anxiety disorders directly impact the lives of nearly one in five people, accounting for substantial worldwide suffering and disability. Here, we use a nonhuman primate model of anxious temperament (AT) to understand the neurobiology underlying the early-life risk to develop anxiety disorders. Leveraging the same kinds of neuroimaging measures routinely used in human studies, we demonstrate that coordinated activation between the central nucleus of the amygdala and the bed nucleus of the stria terminalis is correlated with, and coinherited with, early-life AT. Understanding how these central extended amygdala regions work together to produce extreme anxiety provides a neural target for early-life interventions with the promise of preventing lifelong disability in at-risk children.

  • amygdala
  • anxiety
  • bed nucleus of the stria terminalis
  • fMRI
  • heritability
  • rhesus monkey
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The Journal of Neuroscience: 38 (35)
Journal of Neuroscience
Vol. 38, Issue 35
29 Aug 2018
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Functional Connectivity within the Primate Extended Amygdala Is Heritable and Associated with Early-Life Anxious Temperament
Andrew S. Fox, Jonathan A. Oler, Rasmus M. Birn, Alexander J. Shackman, Andrew L. Alexander, Ned H. Kalin
Journal of Neuroscience 29 August 2018, 38 (35) 7611-7621; DOI: 10.1523/JNEUROSCI.0102-18.2018

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Functional Connectivity within the Primate Extended Amygdala Is Heritable and Associated with Early-Life Anxious Temperament
Andrew S. Fox, Jonathan A. Oler, Rasmus M. Birn, Alexander J. Shackman, Andrew L. Alexander, Ned H. Kalin
Journal of Neuroscience 29 August 2018, 38 (35) 7611-7621; DOI: 10.1523/JNEUROSCI.0102-18.2018
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Keywords

  • amygdala
  • anxiety
  • bed nucleus of the stria terminalis
  • fMRI
  • heritability
  • rhesus monkey

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