Higher Peripheral Inflammatory Signaling Associated With Lower Resting-State Functional Brain Connectivity in Emotion Regulation and Central Executive Networks

Robin Nusslock*, Gene H. Brody, Casey C. Armstrong, Ann L. Carroll, Lawrence H. Sweet, Tianyi Yu, Allen W. Barton, Emily S. Hallowell, Edith Chen, James P. Higgins, Todd B Parrish, Lei Wang, Greg Miller

*Corresponding author for this work

Research output: Contribution to journalArticle

4 Citations (Scopus)

Abstract

Background: Researchers document bidirectional pathways linking peripheral inflammation and neural circuitries subserving emotion processing and regulation. To extend this work, we present results from two independent studies examining the relationship between inflammation and resting-state functional connectivity (rsFC), as measured by functional magnetic resonance imaging. Methods: Study 1 involved 90 rural African American young adults, 25 years of age (52% female), and study 2 involved 82 urban African American youths, 13 to 14 years of age (66% female). Both studies measured circulating inflammatory biomarkers (C-reactive protein, interleukin 6, interleukin 10, tumor necrosis factor alpha), and the measures were averaged to form a composite. Study 2 also enumerated classical monocytes, a key leukocyte subpopulation involved in immune-to-brain signaling. All participants completed a resting-state functional magnetic resonance imaging scan. Results: Consistent with our prediction, higher scores on the inflammatory composite were associated with lower rsFC within an emotion regulation network in study 1, controlling for sex. Study 2 replicated study 1, showing that higher scores on the inflammatory composite were associated with lower rsFC within the emotion regulation network, controlling for sex, age, and pubertal status, and found a similar pattern for rsFC within a central executive network. Study 2 also found that higher numbers of classical monocytes were associated with lower rsFC within both the emotion regulation and central executive networks. There was no relationship between rsFC in the anterior salience or default mode networks with inflammation in either study. Conclusions: With these findings, we document relationships between peripheral inflammation and rsFC within an emotion regulation and central executive network and replicate these associations with the emotion regulation network across two independent samples.

Original languageEnglish (US)
Pages (from-to)153-162
Number of pages10
JournalBiological psychiatry
Volume86
Issue number2
DOIs
StatePublished - Jul 15 2019

Fingerprint

Emotions
Brain
Inflammation
African Americans
Monocytes
Magnetic Resonance Imaging
Interleukin-10
C-Reactive Protein
Young Adult
Interleukin-6
Leukocytes
Tumor Necrosis Factor-alpha
Biomarkers
Research Personnel

Keywords

  • Inflammation
  • Mental health
  • Neuroscience
  • Physical health
  • Resting state
  • fMRI

ASJC Scopus subject areas

  • Biological Psychiatry

Cite this

Nusslock, Robin ; Brody, Gene H. ; Armstrong, Casey C. ; Carroll, Ann L. ; Sweet, Lawrence H. ; Yu, Tianyi ; Barton, Allen W. ; Hallowell, Emily S. ; Chen, Edith ; Higgins, James P. ; Parrish, Todd B ; Wang, Lei ; Miller, Greg. / Higher Peripheral Inflammatory Signaling Associated With Lower Resting-State Functional Brain Connectivity in Emotion Regulation and Central Executive Networks. In: Biological psychiatry. 2019 ; Vol. 86, No. 2. pp. 153-162.
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abstract = "Background: Researchers document bidirectional pathways linking peripheral inflammation and neural circuitries subserving emotion processing and regulation. To extend this work, we present results from two independent studies examining the relationship between inflammation and resting-state functional connectivity (rsFC), as measured by functional magnetic resonance imaging. Methods: Study 1 involved 90 rural African American young adults, 25 years of age (52{\%} female), and study 2 involved 82 urban African American youths, 13 to 14 years of age (66{\%} female). Both studies measured circulating inflammatory biomarkers (C-reactive protein, interleukin 6, interleukin 10, tumor necrosis factor alpha), and the measures were averaged to form a composite. Study 2 also enumerated classical monocytes, a key leukocyte subpopulation involved in immune-to-brain signaling. All participants completed a resting-state functional magnetic resonance imaging scan. Results: Consistent with our prediction, higher scores on the inflammatory composite were associated with lower rsFC within an emotion regulation network in study 1, controlling for sex. Study 2 replicated study 1, showing that higher scores on the inflammatory composite were associated with lower rsFC within the emotion regulation network, controlling for sex, age, and pubertal status, and found a similar pattern for rsFC within a central executive network. Study 2 also found that higher numbers of classical monocytes were associated with lower rsFC within both the emotion regulation and central executive networks. There was no relationship between rsFC in the anterior salience or default mode networks with inflammation in either study. Conclusions: With these findings, we document relationships between peripheral inflammation and rsFC within an emotion regulation and central executive network and replicate these associations with the emotion regulation network across two independent samples.",
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Higher Peripheral Inflammatory Signaling Associated With Lower Resting-State Functional Brain Connectivity in Emotion Regulation and Central Executive Networks. / Nusslock, Robin; Brody, Gene H.; Armstrong, Casey C.; Carroll, Ann L.; Sweet, Lawrence H.; Yu, Tianyi; Barton, Allen W.; Hallowell, Emily S.; Chen, Edith; Higgins, James P.; Parrish, Todd B; Wang, Lei; Miller, Greg.

In: Biological psychiatry, Vol. 86, No. 2, 15.07.2019, p. 153-162.

Research output: Contribution to journalArticle

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T1 - Higher Peripheral Inflammatory Signaling Associated With Lower Resting-State Functional Brain Connectivity in Emotion Regulation and Central Executive Networks

AU - Nusslock, Robin

AU - Brody, Gene H.

AU - Armstrong, Casey C.

AU - Carroll, Ann L.

AU - Sweet, Lawrence H.

AU - Yu, Tianyi

AU - Barton, Allen W.

AU - Hallowell, Emily S.

AU - Chen, Edith

AU - Higgins, James P.

AU - Parrish, Todd B

AU - Wang, Lei

AU - Miller, Greg

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N2 - Background: Researchers document bidirectional pathways linking peripheral inflammation and neural circuitries subserving emotion processing and regulation. To extend this work, we present results from two independent studies examining the relationship between inflammation and resting-state functional connectivity (rsFC), as measured by functional magnetic resonance imaging. Methods: Study 1 involved 90 rural African American young adults, 25 years of age (52% female), and study 2 involved 82 urban African American youths, 13 to 14 years of age (66% female). Both studies measured circulating inflammatory biomarkers (C-reactive protein, interleukin 6, interleukin 10, tumor necrosis factor alpha), and the measures were averaged to form a composite. Study 2 also enumerated classical monocytes, a key leukocyte subpopulation involved in immune-to-brain signaling. All participants completed a resting-state functional magnetic resonance imaging scan. Results: Consistent with our prediction, higher scores on the inflammatory composite were associated with lower rsFC within an emotion regulation network in study 1, controlling for sex. Study 2 replicated study 1, showing that higher scores on the inflammatory composite were associated with lower rsFC within the emotion regulation network, controlling for sex, age, and pubertal status, and found a similar pattern for rsFC within a central executive network. Study 2 also found that higher numbers of classical monocytes were associated with lower rsFC within both the emotion regulation and central executive networks. There was no relationship between rsFC in the anterior salience or default mode networks with inflammation in either study. Conclusions: With these findings, we document relationships between peripheral inflammation and rsFC within an emotion regulation and central executive network and replicate these associations with the emotion regulation network across two independent samples.

AB - Background: Researchers document bidirectional pathways linking peripheral inflammation and neural circuitries subserving emotion processing and regulation. To extend this work, we present results from two independent studies examining the relationship between inflammation and resting-state functional connectivity (rsFC), as measured by functional magnetic resonance imaging. Methods: Study 1 involved 90 rural African American young adults, 25 years of age (52% female), and study 2 involved 82 urban African American youths, 13 to 14 years of age (66% female). Both studies measured circulating inflammatory biomarkers (C-reactive protein, interleukin 6, interleukin 10, tumor necrosis factor alpha), and the measures were averaged to form a composite. Study 2 also enumerated classical monocytes, a key leukocyte subpopulation involved in immune-to-brain signaling. All participants completed a resting-state functional magnetic resonance imaging scan. Results: Consistent with our prediction, higher scores on the inflammatory composite were associated with lower rsFC within an emotion regulation network in study 1, controlling for sex. Study 2 replicated study 1, showing that higher scores on the inflammatory composite were associated with lower rsFC within the emotion regulation network, controlling for sex, age, and pubertal status, and found a similar pattern for rsFC within a central executive network. Study 2 also found that higher numbers of classical monocytes were associated with lower rsFC within both the emotion regulation and central executive networks. There was no relationship between rsFC in the anterior salience or default mode networks with inflammation in either study. Conclusions: With these findings, we document relationships between peripheral inflammation and rsFC within an emotion regulation and central executive network and replicate these associations with the emotion regulation network across two independent samples.

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