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Causal effects of the early caregiving environment on development of stress response systems in children.

ABSTRACT: Disruptions in stress response system functioning are thought to be a central mechanism by which exposure to adverse early-life environments influences human development. Although early-life adversity results in hyperreactivity of the sympathetic nervous system (SNS) and hypothalamic-pituitary-adrenal (HPA) axis in rodents, evidence from human studies is inconsistent. We present results from the Bucharest Early Intervention Project examining whether randomized placement into a family caregiving environment alters development of the autonomic nervous system and HPA axis in children exposed to early-life deprivation associated with institutional rearing. Electrocardiogram, impedance cardiograph, and neuroendocrine data were collected during laboratory-based challenge tasks from children (mean age = 12.9 y) raised in deprived institutional settings in Romania randomized to a high-quality foster care intervention (n = 48) or to remain in care as usual (n = 43) and a sample of typically developing Romanian children (n = 47). Children who remained in institutional care exhibited significantly blunted SNS and HPA axis responses to psychosocial stress compared with children randomized to foster care, whose stress responses approximated those of typically developing children. Intervention effects were evident for cortisol and parasympathetic nervous system reactivity only among children placed in foster care before age 24 and 18 months, respectively, providing experimental evidence of a sensitive period in humans during which the environment is particularly likely to alter stress response system development. We provide evidence for a causal link between the early caregiving environment and stress response system reactivity in humans with effects that differ markedly from those observed in rodent models.

SUBMITTER: McLaughlin KA

PROVIDER: S-EPMC4426436 | biostudies-literature | 2015 May

REPOSITORIES: biostudies-literature

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Causal effects of the early caregiving environment on development of stress response systems in children.

McLaughlin Katie A KA Sheridan Margaret A MA Tibu Florin F Fox Nathan A NA Zeanah Charles H CH Nelson Charles A CA

Proceedings of the National Academy of Sciences of the United States of America 20150420 18

Disruptions in stress response system functioning are thought to be a central mechanism by which exposure to adverse early-life environments influences human development. Although early-life adversity results in hyperreactivity of the sympathetic nervous system (SNS) and hypothalamic-pituitary-adrenal (HPA) axis in rodents, evidence from human studies is inconsistent. We present results from the Bucharest Early Intervention Project examining whether randomized placement into a family caregiving ...[more]

PMID: 25902515

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Project description:Early social experiences, particularly maternal care, shape behavioral and physiological development in primates. Thus, it is not surprising that adverse caregiving, such as child maltreatment leads to a vast array of poor developmental outcomes, including increased risk for psychopathology across the lifespan. Studies of the underlying neurobiology of this risk have identified structural and functional alterations in cortico-limbic brain circuits that seem particularly sensitive to these early adverse experiences and are associated with anxiety and affective disorders. However, it is not understood how these neurobiological alterations unfold during development as it is very difficult to study these early phases in humans, where the effects of maltreatment experience cannot be disentangled from heritable traits. The current study examined the specific effects of experience ("nurture") versus heritable factors ("nature") on the development of brain white matter (WM) tracts with putative roles in socioemotional behavior in primates from birth through the juvenile period. For this we used a randomized crossfostering experimental design in a naturalistic rhesus monkey model of infant maltreatment, where infant monkeys were randomly assigned at birth to either a mother with a history of maltreating her infants, or a competent mother. Using a longitudinal diffusion tensor imaging (DTI) atlas-based tract-profile approach we identified widespread, but also specific, maturational changes on major brain tracts, as well as alterations in a measure of WM integrity (fractional anisotropy, FA) in the middle longitudinal fasciculus (MdLF) and the inferior longitudinal fasciculus (ILF), of maltreated animals, suggesting decreased structural integrity in these tracts due to early adverse experience. Exploratory voxelwise analyses confirmed the tract-based approach, finding additional effects of early adversity, biological mother, social dominance rank, and sex in other WM tracts. These results suggest tract-specific effects of postnatal maternal care experience versus heritable or biological factors on primate WM microstructural development. Further studies are needed to determine the specific behavioral outcomes and biological mechanisms associated with these alterations in WM integrity.

Project description:Psychosocial environments impact normative behavioral development in children, increasing the risk of problem behaviors and psychiatric disorders across the life span. Converging evidence demonstrates that early normative development is affected by the gut microbiome, which itself can be altered by early psychosocial environments. However, much of our understanding of the gut microbiome's role in early development stems from nonhuman animal models and predominately focuses on the first years of life, during peri- and postnatal microbial colonization. As a first step to identify if these findings translate to humans and the extent to which these relationships are maintained after initial microbial colonization, we conducted a metagenomic investigation among a cross-sectional sample of early school-aged children with a range of adverse experiences and caregiver stressors and relationships. Our results indicate that the taxonomic and functional composition of the gut microbiome correlates with behavior during a critical period of child development. Furthermore, our analysis reveals that both socioeconomic risk exposure and child behaviors associate with the relative abundances of specific taxa (e.g., Bacteroides and Bifidobacterium species) as well as functional modules encoded in their genomes (e.g., monoamine metabolism) that have been linked to cognition and health. While we cannot infer causality within this study, these findings suggest that caregivers may moderate the gut microbiome's link to environment and behaviors beyond the first few years of life.IMPORTANCE Childhood is a formative period of behavioral and biological development that can be modified, for better or worse, by the psychosocial environment that is in part determined by caregivers. Not only do our own genes and the external environment influence such developmental trajectories, but the community of microbes living in, on, and around our bodies-the microbiome-plays an important role as well. By surveying the gut microbiomes of a cross-sectional cohort of early school-aged children with a range of psychosocial environments and subclinical mental health symptoms, we demonstrated that caregiving behaviors modified the child gut microbiome's association to socioeconomic risk and behavioral dysregulation.

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Causal effects of the early caregiving environment on development of stress response systems in children.

Publications

Causal effects of the early caregiving environment on development of stress response systems in children.

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