Accelerated maturation in functional connectivity following early life stress: Circuit specific or broadly distributed?

Max P. Herzberg; Kelly Jedd McKenzie; Amanda S. Hodel; Ruskin H. Hunt; Bryon A. Mueller; Megan R. Gunnar; Kathleen M. Thomas

doi:10.1016/j.dcn.2021.100922

Accelerated maturation in functional connectivity following early life stress: Circuit specific or broadly distributed?

Max P. Herzberg, Kelly Jedd McKenzie, Amanda S. Hodel, Ruskin H. Hunt, Bryon A. Mueller, Megan R. Gunnar, Kathleen M. Thomas

Research output: Contribution to journal › Article › peer-review

22 Scopus citations

Abstract

Psychosocial acceleration theory and other frameworks adapted from life history predict a link between early life stress and accelerated maturation in several physiological systems. Those findings led researchers to suggest that the emotion-regulatory brain circuits of previously-institutionalized (PI) youth are more mature than youth raised in their biological families (non-adopted, or NA, youth) during emotion tasks. Whether this accelerated maturation is evident during resting-state fMRI has not yet been established. Resting-state fMRI data from 83 early adolescents (M_age = 12.9 years, SD = 0.57 years) including 41 PI and 42 NA youth, were used to examine seed-based functional connectivity between the amygdala and ventromedial prefrontal cortex (vmPFC). Additional whole-brain analyses assessed group differences in functional connectivity and associations with cognitive performance and behavior. We found group differences in amygdala – vmPFC connectivity that may be consistent with accelerated maturation following early life stress. Further, whole-brain connectivity analyses revealed group differences associated with internalizing and externalizing symptoms. However, the majority of whole-brain results were not consistent with an accelerated maturation framework. Our results suggest early life stress in the form of institutional care is associated with circuit-specific alterations to a frontolimbic emotion-regulatory system, while revealing limited differences in more broadly distributed networks.

Original language	English (US)
Article number	100922
Journal	Developmental Cognitive Neuroscience
Volume	48
DOIs	https://doi.org/10.1016/j.dcn.2021.100922
State	Published - Apr 2021

Bibliographical note

Funding Information:
This research was supported by a National Institute of Mental Health – United States ; P50-MH79513 ; T32-MH73129 ; T32-MH015755 ; National Institute of Child Health and Human Development – United States ; T32-HD007151 , National Centers for Research Resources – United States P41 RR008079 , National Institute of Biomedical Imaging and Bioengineering – United States P41 EB015894 , National Institute of Neurological Disorders and Stroke – United States P30 NS076408 , National Center for Advancing Translational Sciences – United States TL1R002493 and UL1TR002494 , University of Minnesota Graduate School Fellowship – United States , Doris Duke Fellowship for the Promotion of Child Well-Being – United States . The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health’s National Center for Advancing Translational Sciences. The authors thank collaborators at the Center for Brain, Genes, and Behavioral Research Across Development located at the Weill-Cornell Medical Center, the Minnesota Supercomputing Institute (MSI) at the University of Minnesota for providing resources that contributed to the research results reported within this paper ( http://www.msi.umn.edu ), and members of Kathleen M. Thomas’ Cognitive Development & Neuroimaging Lab and Megan R. Gunnar’s Human Developmental Psychobiology Lab for assistance with participant recruitment, scheduling, and testing.

Funding Information:
This research was supported by a National Institute of Mental Health ? United States; P50-MH79513; T32-MH73129; T32-MH015755;National Institute of Child Health and Human Development ? United States; T32-HD007151, National Centers for Research Resources ? United StatesP41 RR008079, National Institute of Biomedical Imaging and Bioengineering ? United StatesP41 EB015894, National Institute of Neurological Disorders and Stroke ? United StatesP30 NS076408, National Center for Advancing Translational Sciences ? United StatesTL1R002493 and UL1TR002494, University of Minnesota Graduate School Fellowship ? United States, Doris Duke Fellowship for the Promotion of Child Well-Being ? United States. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health's National Center for Advancing Translational Sciences. The authors thank collaborators at the Center for Brain, Genes, and Behavioral Research Across Development located at the Weill-Cornell Medical Center, the Minnesota Supercomputing Institute (MSI) at the University of Minnesota for providing resources that contributed to the research results reported within this paper (http://www.msi.umn.edu), and members of Kathleen M. Thomas? Cognitive Development & Neuroimaging Lab and Megan R. Gunnar's Human Developmental Psychobiology Lab for assistance with participant recruitment, scheduling, and testing.

Publisher Copyright:
© 2021

Keywords

Early life stress
Graph theory
Institutional care
Resting-state fMRI

Center for Magnetic Resonance Research (CMRR) tags

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10.1016/j.dcn.2021.100922

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@article{0b2a565f03494c6ba09eb501d72e631a,

title = "Accelerated maturation in functional connectivity following early life stress: Circuit specific or broadly distributed?",

abstract = "Psychosocial acceleration theory and other frameworks adapted from life history predict a link between early life stress and accelerated maturation in several physiological systems. Those findings led researchers to suggest that the emotion-regulatory brain circuits of previously-institutionalized (PI) youth are more mature than youth raised in their biological families (non-adopted, or NA, youth) during emotion tasks. Whether this accelerated maturation is evident during resting-state fMRI has not yet been established. Resting-state fMRI data from 83 early adolescents (Mage = 12.9 years, SD = 0.57 years) including 41 PI and 42 NA youth, were used to examine seed-based functional connectivity between the amygdala and ventromedial prefrontal cortex (vmPFC). Additional whole-brain analyses assessed group differences in functional connectivity and associations with cognitive performance and behavior. We found group differences in amygdala – vmPFC connectivity that may be consistent with accelerated maturation following early life stress. Further, whole-brain connectivity analyses revealed group differences associated with internalizing and externalizing symptoms. However, the majority of whole-brain results were not consistent with an accelerated maturation framework. Our results suggest early life stress in the form of institutional care is associated with circuit-specific alterations to a frontolimbic emotion-regulatory system, while revealing limited differences in more broadly distributed networks.",

keywords = "Early life stress, Graph theory, Institutional care, Resting-state fMRI",

author = "Herzberg, {Max P.} and McKenzie, {Kelly Jedd} and Hodel, {Amanda S.} and Hunt, {Ruskin H.} and Mueller, {Bryon A.} and Gunnar, {Megan R.} and Thomas, {Kathleen M.}",

note = "Funding Information: This research was supported by a National Institute of Mental Health – United States ; P50-MH79513 ; T32-MH73129 ; T32-MH015755 ; National Institute of Child Health and Human Development – United States ; T32-HD007151 , National Centers for Research Resources – United States P41 RR008079 , National Institute of Biomedical Imaging and Bioengineering – United States P41 EB015894 , National Institute of Neurological Disorders and Stroke – United States P30 NS076408 , National Center for Advancing Translational Sciences – United States TL1R002493 and UL1TR002494 , University of Minnesota Graduate School Fellowship – United States , Doris Duke Fellowship for the Promotion of Child Well-Being – United States . The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health{\textquoteright}s National Center for Advancing Translational Sciences. The authors thank collaborators at the Center for Brain, Genes, and Behavioral Research Across Development located at the Weill-Cornell Medical Center, the Minnesota Supercomputing Institute (MSI) at the University of Minnesota for providing resources that contributed to the research results reported within this paper ( http://www.msi.umn.edu ), and members of Kathleen M. Thomas{\textquoteright} Cognitive Development & Neuroimaging Lab and Megan R. Gunnar{\textquoteright}s Human Developmental Psychobiology Lab for assistance with participant recruitment, scheduling, and testing. Funding Information: This research was supported by a National Institute of Mental Health ? United States; P50-MH79513; T32-MH73129; T32-MH015755;National Institute of Child Health and Human Development ? United States; T32-HD007151, National Centers for Research Resources ? United StatesP41 RR008079, National Institute of Biomedical Imaging and Bioengineering ? United StatesP41 EB015894, National Institute of Neurological Disorders and Stroke ? United StatesP30 NS076408, National Center for Advancing Translational Sciences ? United StatesTL1R002493 and UL1TR002494, University of Minnesota Graduate School Fellowship ? United States, Doris Duke Fellowship for the Promotion of Child Well-Being ? United States. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health's National Center for Advancing Translational Sciences. The authors thank collaborators at the Center for Brain, Genes, and Behavioral Research Across Development located at the Weill-Cornell Medical Center, the Minnesota Supercomputing Institute (MSI) at the University of Minnesota for providing resources that contributed to the research results reported within this paper (http://www.msi.umn.edu), and members of Kathleen M. Thomas? Cognitive Development & Neuroimaging Lab and Megan R. Gunnar's Human Developmental Psychobiology Lab for assistance with participant recruitment, scheduling, and testing. Publisher Copyright: {\textcopyright} 2021",

year = "2021",

month = apr,

doi = "10.1016/j.dcn.2021.100922",

language = "English (US)",

volume = "48",

journal = "Developmental Cognitive Neuroscience",

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AU - McKenzie, Kelly Jedd

AU - Hodel, Amanda S.

AU - Hunt, Ruskin H.

AU - Mueller, Bryon A.

AU - Gunnar, Megan R.

AU - Thomas, Kathleen M.

N1 - Funding Information: This research was supported by a National Institute of Mental Health – United States ; P50-MH79513 ; T32-MH73129 ; T32-MH015755 ; National Institute of Child Health and Human Development – United States ; T32-HD007151 , National Centers for Research Resources – United States P41 RR008079 , National Institute of Biomedical Imaging and Bioengineering – United States P41 EB015894 , National Institute of Neurological Disorders and Stroke – United States P30 NS076408 , National Center for Advancing Translational Sciences – United States TL1R002493 and UL1TR002494 , University of Minnesota Graduate School Fellowship – United States , Doris Duke Fellowship for the Promotion of Child Well-Being – United States . The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health’s National Center for Advancing Translational Sciences. The authors thank collaborators at the Center for Brain, Genes, and Behavioral Research Across Development located at the Weill-Cornell Medical Center, the Minnesota Supercomputing Institute (MSI) at the University of Minnesota for providing resources that contributed to the research results reported within this paper ( http://www.msi.umn.edu ), and members of Kathleen M. Thomas’ Cognitive Development & Neuroimaging Lab and Megan R. Gunnar’s Human Developmental Psychobiology Lab for assistance with participant recruitment, scheduling, and testing. Funding Information: This research was supported by a National Institute of Mental Health ? United States; P50-MH79513; T32-MH73129; T32-MH015755;National Institute of Child Health and Human Development ? United States; T32-HD007151, National Centers for Research Resources ? United StatesP41 RR008079, National Institute of Biomedical Imaging and Bioengineering ? United StatesP41 EB015894, National Institute of Neurological Disorders and Stroke ? United StatesP30 NS076408, National Center for Advancing Translational Sciences ? United StatesTL1R002493 and UL1TR002494, University of Minnesota Graduate School Fellowship ? United States, Doris Duke Fellowship for the Promotion of Child Well-Being ? United States. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health's National Center for Advancing Translational Sciences. The authors thank collaborators at the Center for Brain, Genes, and Behavioral Research Across Development located at the Weill-Cornell Medical Center, the Minnesota Supercomputing Institute (MSI) at the University of Minnesota for providing resources that contributed to the research results reported within this paper (http://www.msi.umn.edu), and members of Kathleen M. Thomas? Cognitive Development & Neuroimaging Lab and Megan R. Gunnar's Human Developmental Psychobiology Lab for assistance with participant recruitment, scheduling, and testing. Publisher Copyright: © 2021

PY - 2021/4

Y1 - 2021/4

N2 - Psychosocial acceleration theory and other frameworks adapted from life history predict a link between early life stress and accelerated maturation in several physiological systems. Those findings led researchers to suggest that the emotion-regulatory brain circuits of previously-institutionalized (PI) youth are more mature than youth raised in their biological families (non-adopted, or NA, youth) during emotion tasks. Whether this accelerated maturation is evident during resting-state fMRI has not yet been established. Resting-state fMRI data from 83 early adolescents (Mage = 12.9 years, SD = 0.57 years) including 41 PI and 42 NA youth, were used to examine seed-based functional connectivity between the amygdala and ventromedial prefrontal cortex (vmPFC). Additional whole-brain analyses assessed group differences in functional connectivity and associations with cognitive performance and behavior. We found group differences in amygdala – vmPFC connectivity that may be consistent with accelerated maturation following early life stress. Further, whole-brain connectivity analyses revealed group differences associated with internalizing and externalizing symptoms. However, the majority of whole-brain results were not consistent with an accelerated maturation framework. Our results suggest early life stress in the form of institutional care is associated with circuit-specific alterations to a frontolimbic emotion-regulatory system, while revealing limited differences in more broadly distributed networks.

AB - Psychosocial acceleration theory and other frameworks adapted from life history predict a link between early life stress and accelerated maturation in several physiological systems. Those findings led researchers to suggest that the emotion-regulatory brain circuits of previously-institutionalized (PI) youth are more mature than youth raised in their biological families (non-adopted, or NA, youth) during emotion tasks. Whether this accelerated maturation is evident during resting-state fMRI has not yet been established. Resting-state fMRI data from 83 early adolescents (Mage = 12.9 years, SD = 0.57 years) including 41 PI and 42 NA youth, were used to examine seed-based functional connectivity between the amygdala and ventromedial prefrontal cortex (vmPFC). Additional whole-brain analyses assessed group differences in functional connectivity and associations with cognitive performance and behavior. We found group differences in amygdala – vmPFC connectivity that may be consistent with accelerated maturation following early life stress. Further, whole-brain connectivity analyses revealed group differences associated with internalizing and externalizing symptoms. However, the majority of whole-brain results were not consistent with an accelerated maturation framework. Our results suggest early life stress in the form of institutional care is associated with circuit-specific alterations to a frontolimbic emotion-regulatory system, while revealing limited differences in more broadly distributed networks.

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KW - Graph theory

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Accelerated maturation in functional connectivity following early life stress: Circuit specific or broadly distributed?

Abstract

Bibliographical note

Keywords

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