Negative childhood experiences alter a prefrontal-insular-motor cortical network in healthy adults: A preliminary multimodal rsfMRI-fMRI-MRS-dMRI study

Niall W. Duncan, Dave J. Hayes, Christine Wiebking, Brice Tiret, Karin Pietruska, David Q. Chen, Pierre Rainville, Małgorzata Marjańska, Omar Ayad, Julien Doyon, Mojgan Hodaie, Georg Northoff

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37 Citations (Scopus)

Abstract

Research in humans and animals has shown that negative childhood experiences (NCE) can have long-term effects on the structure and function of the brain. Alterations have been noted in grey and white matter, in the brain's resting state, on the glutamatergic system, and on neural and behavioural responses to aversive stimuli. These effects can be linked to psychiatric disorder such as depression and anxiety disorders that are influenced by excessive exposure to early life stressors. The aim of the current study was to investigate the effect of NCEs on these systems. Resting state functional MRI (rsfMRI), aversion task fMRI, glutamate magnetic resonance spectroscopy (MRS), and diffusion magnetic resonance imaging (dMRI) were combined with the Childhood Trauma Questionnaire (CTQ) in healthy subjects to examine the impact of NCEs on the brain. Low CTQ scores, a measure of NCEs, were related to higher resting state glutamate levels and higher resting state entropy in the medial prefrontal cortex (mPFC). CTQ scores, mPFC glutamate and entropy, correlated with neural BOLD responses to the anticipation of aversive stimuli in regions throughout the aversion-related network, with strong correlations between all measures in the motor cortex and left insula. Structural connectivity strength, measured using mean fractional anisotropy, between the mPFC and left insula correlated to aversion-related signal changes in the motor cortex. These findings highlight the impact of NCEs on multiple inter-related brain systems. In particular, they highlight the role of a prefrontal-insular-motor cortical network in the processing and responsivity to aversive stimuli and its potential adaptability by NCEs.

Original languageEnglish
Pages (from-to)4622-4637
Number of pages16
JournalHuman Brain Mapping
Volume36
Issue number11
DOIs
Publication statusPublished - Nov 1 2015

Keywords

  • Affect
  • Aversion
  • Brain networks
  • Early life stress
  • Mood disorder
  • Resting state

ASJC Scopus subject areas

  • Clinical Neurology
  • Anatomy
  • Neurology
  • Radiology Nuclear Medicine and imaging
  • Radiological and Ultrasound Technology

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  • Cite this

    Duncan, N. W., Hayes, D. J., Wiebking, C., Tiret, B., Pietruska, K., Chen, D. Q., Rainville, P., Marjańska, M., Ayad, O., Doyon, J., Hodaie, M., & Northoff, G. (2015). Negative childhood experiences alter a prefrontal-insular-motor cortical network in healthy adults: A preliminary multimodal rsfMRI-fMRI-MRS-dMRI study. Human Brain Mapping, 36(11), 4622-4637. https://doi.org/10.1002/hbm.22941