Abstract
Background
Socioeconomic factors have been consistently linked with the structure of children’s
hippocampus and anterior cingulate cortex (ACC). Chronic stress—as indexed by hair
cortisol concentration—may represent an important mechanism underlying these associations.
Here, we examined associations between hair cortisol and children’s hippocampal and
ACC structure, including across hippocampal subfields, and whether hair cortisol mediated
associations between socioeconomic background (family income-to-needs ratio, parental
education) and the structure of these brain regions.
Methods
Participants were 5- to 9-year-old children (N = 94; 61% female) from socioeconomically diverse families. Parents and children provided
hair samples that were assayed for cortisol. High-resolution, T1-weighted magnetic
resonance imaging scans were acquired, and FreeSurfer 6.0 was used to compute hippocampal
volume and rostral and caudal ACC thickness and surface area (n = 37 with both child hair cortisol and magnetic resonance imaging data; n = 41 with both parent hair cortisol and magnetic resonance imaging data).
Results
Higher hair cortisol concentration was significantly associated with smaller CA3 and
dentate gyrus hippocampal subfield volumes but not with CA1 or subiculum volume. Higher
hair cortisol was also associated with greater caudal ACC thickness. Hair cortisol
significantly mediated associations between parental education level and CA3 and dentate
gyrus volumes; lower parental education level was associated with higher hair cortisol,
which in turn was associated with smaller volume in these subfields.
Conclusions
These findings point to chronic physiologic stress as a potential mechanism through
which lower parental education level leads to reduced hippocampal volume. Hair cortisol
concentration may be an informative biomarker leading to more effective prevention
and intervention strategies aimed at childhood socioeconomic disadvantage.
Keywords
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References
- The neuroscience of socioeconomic status: Correlates, causes, and consequences.Neuron. 2017; 96: 56-71
- Childhood poverty, chronic stress, self-regulation, and coping.Child Dev Perspect. 2013; 7: 43-48
- Salivary cortisol mediates effects of poverty and parenting on executive functions in early childhood.Child Dev. 2011; 82: 1970-1984
- Socioeconomic status, hair cortisol and internalizing symptoms in parents and children.Psychoneuroendocrinology. 2017; 78: 142-150
- Hair cortisol reflects socio-economic factors and hair zinc in preschoolers.Psychoneuroendocrinology. 2013; 38: 331-340
- Determinants of hair cortisol concentration in children: A systematic review.Psychoneuroendocrinology. 2018; 87: 204-214
- Infant hair cortisol: Associations with salivary cortisol and environmental context.Dev Psychobiol. 2017; 59: 26-38
- Correspondence between hair cortisol concentrations and 30-day integrated daily salivary and weekly urinary cortisol measures.Psychoneuroendocrinology. 2016; 71: 12-18
- Time-varying effects of income on hippocampal volume trajectories in adolescent girls.Dev Cogn Neurosci. 2017; 30: 41-50
- Association of child poverty, brain development, and academic achievement.JAMA Pediatr. 2015; 169: 822-829
- Association between income and the hippocampus.PLoS One. 2011; 6e18712
- Behavior problems after early life stress: Contributions of the hippocampus and amygdala.Biol Psychiatry. 2015; 77: 314-323
- The influence of socioeconomic status on children’s brain structure.PLoS One. 2012; 7e0042486
- The effects of poverty on childhood brain development: The mediating effect of caregiving and stressful life events.JAMA Pediatr. 2013; 167: 1135-1142
- Family income, parental education and brain structure in children and adolescents.Nat Neurosci. 2015; 18: 773-778
- Neural correlates of socioeconomic status in the developing human brain.Dev Sci. 2012; 15: 516-527
- Protective prevention effects on the association of poverty with brain development.JAMA Pediatr. 2017; 171: 46-52
- Socioeconomic status and hippocampal volume in children and young adults.Dev Sci. 2018; 21e12561
- Perigenual anterior cingulate morphology covaries with perceived social standing.Soc Cogn Affect Neurosci. 2007; 2: 161-173
- Associations between children’s socioeconomic status and prefrontal cortical thickness.Dev Sci. 2013; 16: 641-652
- Regional gray matter volume mediates the relationship between family socioeconomic status and depression-related trait in a young healthy sample.Cogn Affect Behav Neurosci. 2016; 16: 51-62
- Longitudinally mapping childhood socioeconomic status associations with cortical and subcortical morphology.J Neurosci. 2019; 39: 1365-1373
- Neural changes underlying the development of episodic memory during middle childhood.Dev Cogn Neurosci. 2012; 2: 381-395
- Neuroanatomical correlates of executive functions in children and adolescents: A magnetic resonance imaging (MRI) study of cortical thickness.Neuropsychologia. 2010; 48: 2496-2508
- Cortical gray-matter thinning is associated with age-related improvements on executive function tasks.Dev Cogn Neurosci. 2013; 6: 61-71
- Early adolescent cortical thinning is related to better neuropsychological performance.J Int Neuropsychol Soc. 2013; 19: 962-970
- The human hippocampus and spatial and episodic memory.Neuron. 2002; 35: 625-641
- Neighborhood matters: Divergent patterns of stress-induced plasticity across the brain.Nat Neurosci. 2015; 18: 1364-1375
- The brain on stress: Vulnerability and plasticity of the prefrontal cortex over the life course.Neuron. 2013; 79: 16-29
- Stress effects on neuronal structure: Hippocampus, amygdala, and prefrontal cortex.Neuropsychopharmacology. 2016; 41: 3-23
- Stress and prefrontal cortical plasticity in the developing brain.Cogn Dev. 2017; 42: 15-26
- The hippocampus in depression: More than the sum of its parts? Advanced hippocampal substructure segmentation in depression.Biol Psychiatry. 2019; 85: 487-497
- Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy.Behav Neurosci. 1999; 113: 902-913
- Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus.Eur J Neurosci. 2003; 17: 879-886
- Stress-induced remodeling of hippocampal CA3 pyramidal neurons.Brain Res. 2016; 1645: 50-54
- Effects of childhood poverty and chronic stress on emotion regulatory brain function in adulthood.Proc Natl Acad Sci U S A. 2013; 110: 18442-18447
- Stress-system genes and life stress predict cortisol levels and amygdala and hippocampal volumes in children.Neuropsychopharmacology. 2014; 39: 1245-1253
- Cortisol levels and hippocampus volumes in healthy preadolescent children.Biol Psychiatry. 2006; 60: 856-861
- No association between hair cortisol or cortisone and brain morphology in children.Psychoneuroendocrinology. 2016; 74: 101-110
- Socioeconomic status and cognitive functioning: Moving from correlation to causation.Wiley Interdiscip Rev Cogn Sci. 2012; 3: 377-386
- Psychobiological mechanisms underlying the social buffering of the hypothalamic-pituitary-adrenocortical axis: A review of animal models and human studies across development.Psychol Bull. 2014; 140: 256-282
- Childhood maltreatment is associated with reduced volume in the hippocampal subfields CA3, dentate gyrus, and subiculum.Proc Natl Acad Sci U S A. 2012; 109: E563-E572
- A computational atlas of the hippocampal formation using ex vivo, ultra-high resolution MRI: Application to adaptive segmentation of in vivo MRI.Neuroimage. 2015; 115: 117-137
- Heritability and reliability of automatically segmented human hippocampal formation subregions.Neuroimage. 2016; 128: 125-137
- Cortical surface-based analysis. I. Segmentation and surface reconstruction.Neuroimage. 1999; 9: 179-194
- Measuring the thickness of the human cerebral cortex from magnetic resonance images.Proc Natl Acad Sci U S A. 2000; 97: 11050-11055
- An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest.Neuroimage. 2006; 31: 968-980
- Automatically parcellating the human cerebral cortex.Cereb Cortex. 2004; 14: 11-22
- Evaluating the validity of volume-based and surface-based brain image registration for developmental cognitive neuroscience studies in children 4-to-11 years of age.Neuroimage. 2010; 53: 85-93
- Reliability of MRI-derived measurements of human cerebral cortical thickness: The effects of field strength, scanner upgrade and manufacturer.Neuroimage. 2006; 32: 180-194
- A global measure of perceived stress.J Health Soc Behav. 1983; 24: 385-396
- Assessing the impact of life changes: Development of the Life Experiences Survey.J Consult Clin Psychol. 1978; 46: 932-946
- The Great Recession, public transfers, and material hardship.Soc Serv Rev. 2012; 86: 401-427
- Analysis of endogenous cortisol concentrations in the hair of rhesus macaques.Gen Comp Endocrinol. 2006; 147: 255-261
- Extraction and analysis of cortisol from human and monkey hair.J Vis Exp. 2014; e50882
- III. NIH Toolbox Cognition Battery (CB): Measuring episodic memory.Monogr Soc Res Child Dev. 2013; 78: 34-48
- NIH Toolbox Cognitive Function Battery (NIHTB-CFB): Measuring working memory.Monogr Soc Res Child Dev. 2013; 78: 70-87
- II. NIH Toolbox Cognition Battery (CB): Measuring executive function and attention.Monogr Soc Res Child Dev. 2013; 78: 16-33
- The NIH Toolbox Cognition Battery: Results from a large normative developmental sample (PING).Neuropsychology. 2014; 28: 1-10
- The effects of stress and stress hormones on human cognition: Implications for the field of brain and cognition.Brain Cogn. 2007; 65: 209-237
- Controlling the false discovery rate: A practical and powerful approach to multiple testing.J R Stat Soc Series B Stat Methodol. 1995; 57: 289-300
- A comparison of methods to test mediation and other intervening variable effects.Psychol Methods. 2002; 7: 83-104
- Introduction to Mediation, Moderation, and Conditional Process Analysis: A Regression-Based Approach.1st ed. Guilford Press, New York, NY2013
- Asymptotic and resampling strategies for assessing and comparing indirect effects in multiple mediator models.Behav Res Methods. 2008; 40: 879-891
- Effects of stress throughout the lifespan on the brain, behaviour and cognition.Nat Rev Neurosci. 2009; 10: 434-445
- Central role of the brain in stress and adaptation: Links to socioeconomic status, health, and disease.Ann N Y Acad Sci. 2010; 1186: 190-222
- The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress.J Neurosci. 1993; 13: 3839-3847
- Neural pathways link social support to attenuated neuroendocrine stress responses.Neuroimage. 2007; 35: 1601-1612
- Prefrontal cortical function and anxiety: Controlling attention to threat-related stimuli.Nat Neurosci. 2004; 7: 184-188
- A role for the human dorsal anterior cingulate cortex in fear expression.Biol Psychiatry. 2007; 62: 1191-1194
- Obsessive compulsive disorder: Beyond segregated cortico-striatal pathways.Trends Cogn Sci. 2012; 16: 43-51
- Methods and considerations for longitudinal structural brain imaging analysis across development.Dev Cogn Neurosci. 2014; 9: 172-190
- Positive parenting predicts the development of adolescent brain structure: a longitudinal study.Dev Cogn Neurosci. 2014; 8: 7-17
- Observed measures of negative parenting predict brain development during adolescence.PLoS One. 2016; 11e0147774
- Intellectual ability and cortical development in children and adolescents.Nature. 2006; 440: 676-679
- Thinning of the lateral prefrontal cortex during adolescence predicts emotion regulation in females.Soc Cogn Affect Neurosci. 2014; 9: 1845-1854
- Associations between cortical thickness and neurocognitive skills during childhood vary by family socioeconomic factors.Brain Cogn. 2017; 116: 54-62
- Childhood poverty is associated with altered hippocampal function and visuospatial memory in adulthood.Dev Cogn Neurosci. 2017; 23: 39-44
- Memory and the developing brain: From description to explanation with innovation in methods.Dev Cogn Neurosci. 2018; 36: 100613
- Parsing the hippocampus in depression: Chronic stress, hippocampal volume, and major depressive disorder.Biol Psychiatry. 2019; 85: 436-438
- Hair and salivary testosterone, hair cortisol, and externalizing behaviors in adolescents.Psychol Sci. 2018; 29: 688-699
- Differential effects of childhood neglect and abuse during sensitive exposure periods on male and female hippocampus.Neuroimage. 2018; 169: 443-452
- Subtle in-scanner motion biases automated measurement of brain anatomy from in vivo MRI.Hum Brain Mapp. 2016; 37: 2385-2397
- A comparison of automated segmentation and manual tracing for quantifying hippocampal and amygdala volumes.Neuroimage. 2009; 45: 855-866
- A comparison of manual tracing and FreeSurfer for estimating hippocampal volume over the adult lifespan.Hum Brain Mapp. 2018; 39: 2500-2513
Article info
Publication history
Published online: June 12, 2019
Accepted:
May 31,
2019
Received in revised form:
May 31,
2019
Received:
September 4,
2018
Identification
Copyright
© 2019 Society of Biological Psychiatry.
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- Biological Psychiatry and Socioeconomic StatusBiological PsychiatryVol. 86Issue 12
- PreviewThe basic science underlying biological psychiatry came first from animal models. For example, rodent studies established the pathways through which early-life experience and stress impact brain systems involved in anxiety and depression (1). With the advent of modern neuroimaging it became possible to study these systems as they function in healthy humans and in those with psychiatric disorders (2).
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