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Articles, Behavioral/Cognitive

Previous Institutionalization Is Followed by Broader Amygdala–Hippocampal–PFC Network Connectivity during Aversive Learning in Human Development

Jennifer A. Silvers, Daniel S. Lumian, Laurel Gabard-Durnam, Dylan G. Gee, Bonnie Goff, Dominic S. Fareri, Christina Caldera, Jessica Flannery, Eva H. Telzer, Kathryn L. Humphreys and Nim Tottenham
Journal of Neuroscience 15 June 2016, 36 (24) 6420-6430; https://doi.org/10.1523/JNEUROSCI.0038-16.2016
Jennifer A. Silvers
1Department of Psychology, University of California, Los Angeles, Los Angeles, California 90095,
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Daniel S. Lumian
2Department of Psychology, University of Denver, Denver, Colorado 80208,
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Laurel Gabard-Durnam
3Department of Psychology, Columbia University, New York, New York 10027,
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Dylan G. Gee
4Sackler Institute for Developmental Psychobiology, Weill Cornell Medical College, New York, New York 10065,
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Bonnie Goff
1Department of Psychology, University of California, Los Angeles, Los Angeles, California 90095,
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Dominic S. Fareri
5Department of Psychology, University of Oregon, Eugene, Oregon 97403,
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Christina Caldera
1Department of Psychology, University of California, Los Angeles, Los Angeles, California 90095,
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Jessica Flannery
6Gordon F. Derner Institute of Advanced Psychological Studies, Adelphi University, Garden City, New York 11530,
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Eva H. Telzer
7Department of Psychology, University of Illinois at Urbana-Champaign, Champaign, Illinois 61820, and
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Kathryn L. Humphreys
8Department of Psychology, Stanford University, Stanford, California 94305
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Nim Tottenham
3Department of Psychology, Columbia University, New York, New York 10027,
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Abstract

Early institutional care can be profoundly stressful for the human infant, and, as such, can lead to significant alterations in brain development. In animal models, similar variants of early adversity have been shown to modify amygdala–hippocampal–prefrontal cortex development and associated aversive learning. The current study examined this rearing aberration in human development. Eighty-nine children and adolescents who were either previously institutionalized (PI youth; N = 46; 33 females and 13 males; age range, 7–16 years) or were raised by their biological parents from birth (N = 43; 22 females and 21 males; age range, 7–16 years) completed an aversive-learning paradigm while undergoing functional neuroimaging, wherein visual cues were paired with either an aversive sound (CS+) or no sound (CS−). For the PI youth, better aversive learning was associated with higher concurrent trait anxiety. Both groups showed robust learning and amygdala activation for CS+ versus CS− trials. However, PI youth also exhibited broader recruitment of several regions and increased hippocampal connectivity with prefrontal cortex. Stronger connectivity between the hippocampus and ventromedial PFC predicted significant improvements in future anxiety (measured 2 years later), and this was particularly true within the PI group. These results suggest that for humans as well as for other species, early adversity alters the neurobiology of aversive learning by engaging a broader prefrontal–subcortical circuit than same-aged peers. These differences are interpreted as ontogenetic adaptations and potential sources of resilience.

SIGNIFICANCE STATEMENT Prior institutionalization is a significant form of early adversity. While nonhuman animal research suggests that early adversity alters aversive learning and associated neurocircuitry, no prior work has examined this in humans. Here, we show that youth who experienced prior institutionalization, but not comparison youth, recruit the hippocampus during aversive learning. Among youth who experienced prior institutionalization, individual differences in aversive learning were associated with worse current anxiety. However, connectivity between the hippocampus and prefrontal cortex prospectively predicted significant improvements in anxiety 2 years following scanning for previously institutionalized youth. Among youth who experienced prior institutionalization, age-atypical engagement of a distributed set of brain regions during aversive learning may serve a protective function.

  • early life stress
  • fMRI
  • learning
  • neurodevelopment
  • threat
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The Journal of Neuroscience: 36 (24)
Journal of Neuroscience
Vol. 36, Issue 24
15 Jun 2016
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Previous Institutionalization Is Followed by Broader Amygdala–Hippocampal–PFC Network Connectivity during Aversive Learning in Human Development
Jennifer A. Silvers, Daniel S. Lumian, Laurel Gabard-Durnam, Dylan G. Gee, Bonnie Goff, Dominic S. Fareri, Christina Caldera, Jessica Flannery, Eva H. Telzer, Kathryn L. Humphreys, Nim Tottenham
Journal of Neuroscience 15 June 2016, 36 (24) 6420-6430; DOI: 10.1523/JNEUROSCI.0038-16.2016

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Previous Institutionalization Is Followed by Broader Amygdala–Hippocampal–PFC Network Connectivity during Aversive Learning in Human Development
Jennifer A. Silvers, Daniel S. Lumian, Laurel Gabard-Durnam, Dylan G. Gee, Bonnie Goff, Dominic S. Fareri, Christina Caldera, Jessica Flannery, Eva H. Telzer, Kathryn L. Humphreys, Nim Tottenham
Journal of Neuroscience 15 June 2016, 36 (24) 6420-6430; DOI: 10.1523/JNEUROSCI.0038-16.2016
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Keywords

  • early life stress
  • fMRI
  • learning
  • neurodevelopment
  • threat

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