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Functional connectivity in central executive network protects youth against cardiometabolic risks linked with neighborhood violence

Gregory E. Miller, Edith Chen, Casey C. Armstrong, Ann L. Carroll, Sekine Ozturk, Kelsey J. Rydland, Gene H. Brody, Todd B. Parrish, and Robin Nusslock
PNAS November 20, 2018 115 (47) 12063-12068; published ahead of print November 5, 2018 https://doi.org/10.1073/pnas.1810067115
Gregory E. Miller
aInstitute for Policy Research, Northwestern University, Evanston, IL 60208;bDepartment of Psychology, Northwestern University, Evanston, IL 60208;
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  • For correspondence: greg.miller@northwestern.edu
Edith Chen
aInstitute for Policy Research, Northwestern University, Evanston, IL 60208;bDepartment of Psychology, Northwestern University, Evanston, IL 60208;
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Casey C. Armstrong
bDepartment of Psychology, Northwestern University, Evanston, IL 60208;
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Ann L. Carroll
bDepartment of Psychology, Northwestern University, Evanston, IL 60208;
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Sekine Ozturk
bDepartment of Psychology, Northwestern University, Evanston, IL 60208;
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Kelsey J. Rydland
cResearch and Information Services, Northwestern University, Evanston, IL 60208;
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Gene H. Brody
dCenter for Family Research, University of Georgia, Athens, GA 30602;
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Todd B. Parrish
eDepartment of Radiology, Northwestern Feinberg School of Medicine, Chicago, IL 60611
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Robin Nusslock
aInstitute for Policy Research, Northwestern University, Evanston, IL 60208;bDepartment of Psychology, Northwestern University, Evanston, IL 60208;
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  1. Edited by Robert T. Knight, University of California, Berkeley, CA, and accepted by Editorial Board Member Michael S. Gazzaniga October 10, 2018 (received for review June 11, 2018)

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Significance

There is considerable variability in how people respond to major stressors. Some remain healthy, whereas others deteriorate. Little is known about the brain networks that are involved in shaping these different outcomes, a problem we pursue here. Like previous studies, we find that youth living in neighborhoods with high levels of violence have worse cardiometabolic health than peers from safer communities. Extending this knowledge, we show this connection is absent for youth who display higher connectivity within the brain’s frontoparietal central executive network (CEN), which facilitates efforts of self-control as well as reinterpretation of threatening events and suppression of unwanted emotional imagery. These observations suggest that CEN connectivity may be a neurobiological contributor to resilience.

Abstract

Although violent crime has declined in recent decades, it remains a recurring feature of daily life in some neighborhoods. Mounting evidence indicates that such violence has a long reach, which goes beyond family and friends of the victim and undermines the health of people in the surrounding community. However, like all forms of adversity, community violence elicits a heterogeneous response: Some remain healthy, but others deteriorate. Despite much scientific attention, the neural circuitries that contribute to differential adaptation remain poorly understood. Drawing on knowledge of the brain’s intrinsic functional architecture, we predicted that individual differences in resting-state connectivity would explain variability in the strength of the association between neighborhood violence and cardiometabolic health. We enrolled 218 urban youth (age 12–14 years, 66% female; 65% black or Latino) and used geocoding to characterize their exposure to neighborhood murder over the past five years. Multiple aspects of cardiometabolic health were assessed, including obesity, insulin resistance, and metabolic syndrome. Functional MRI was used to quantify the connectivity of major intrinsic networks. Consistent with predictions, resting-state connectivity within the central executive network (CEN) emerged as a moderator of adaptation. Across six distinct outcomes, a higher neighborhood murder rate was associated with greater cardiometabolic risk, but this relationship was apparent only among youth who displayed lower CEN resting-state connectivity. By contrast, there was little evidence of moderation by the anterior salience and default mode networks. These findings advance basic and applied knowledge about adaptation by highlighting intrinsic CEN connectivity as a potential neurobiological contributor to resilience.

  • resilience
  • stress
  • children
  • neuroscience
  • cardiovascular

Footnotes

  • ↵1To whom correspondence should be addressed. Email: greg.miller{at}northwestern.edu.
  • Author contributions: G.E.M., E.C., G.H.B., and R.N. designed research; S.O. performed research; C.C.A., A.L.C., K.J.R., and T.B.P. contributed new reagents/analytic tools; G.E.M., C.C.A., A.L.C., and S.O. analyzed data; and G.E.M., E.C., C.C.A., A.L.C., G.H.B., T.B.P., and R.N. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission. R.T.K. is a guest editor invited by the Editorial Board.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1810067115/-/DCSupplemental.

Published under the PNAS license.

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Functional connectivity in central executive network protects youth against cardiometabolic risks linked with neighborhood violence
Gregory E. Miller, Edith Chen, Casey C. Armstrong, Ann L. Carroll, Sekine Ozturk, Kelsey J. Rydland, Gene H. Brody, Todd B. Parrish, Robin Nusslock
Proceedings of the National Academy of Sciences Nov 2018, 115 (47) 12063-12068; DOI: 10.1073/pnas.1810067115

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Functional connectivity in central executive network protects youth against cardiometabolic risks linked with neighborhood violence
Gregory E. Miller, Edith Chen, Casey C. Armstrong, Ann L. Carroll, Sekine Ozturk, Kelsey J. Rydland, Gene H. Brody, Todd B. Parrish, Robin Nusslock
Proceedings of the National Academy of Sciences Nov 2018, 115 (47) 12063-12068; DOI: 10.1073/pnas.1810067115
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