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Prenatal stress and stress coping style interact to predict metabolic risk in male rats.

ABSTRACT: Both prenatal stress (PNS) exposure and a passive stress-coping style have been identified as risk factors for insulin resistance in rats. In the current study, we test the hypothesis that PNS and stress-coping style may interact in predicting susceptibility for metabolic disease. To test this hypothesis, adult male control and PNS offspring were behaviorally characterized using a defensive burying test to have either a passive or proactive stress-coping style. In adulthood, all rats were fed either a standard chow or a high-fat diet for 3 weeks. After 3 weeks of diet exposure, glucose and insulin levels were assessed during an oral glucose tolerance test. Under high-fat diet conditions, PNS rats display elevated glucose and insulin responses to the oral glucose tolerance test, indicative of glucose intolerance. Interestingly, these effects of PNS were far more pronounced in rats characterized by a passive stress-coping style. Additionally, the passively coping PNS rats also gained more weight on the high-fat diet than all other rats tested. This observation suggests that a stressful prenatal environment in combination with a passive stress-coping strategy may prime an individual to be sensitive to diet-induced obesity and type 2 diabetes.

SUBMITTER: Boersma GJ

PROVIDER: S-EPMC3959611 | biostudies-literature | 2014 Apr

REPOSITORIES: biostudies-literature

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Prenatal stress and stress coping style interact to predict metabolic risk in male rats.

Boersma Gretha J GJ Moghadam Alexander A AA Cordner Zachary A ZA Tamashiro Kellie L KL

Endocrinology 20140127 4

Both prenatal stress (PNS) exposure and a passive stress-coping style have been identified as risk factors for insulin resistance in rats. In the current study, we test the hypothesis that PNS and stress-coping style may interact in predicting susceptibility for metabolic disease. To test this hypothesis, adult male control and PNS offspring were behaviorally characterized using a defensive burying test to have either a passive or proactive stress-coping style. In adulthood, all rats were fed ei ...[more]

PMID: 24467745

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Project description:Acute swim stress results in the robust production of several neuroactive steroids, which act as mediators of the stress response. These steroids include glucocorticoids, and positive GABAA receptor modulatory steroids such as allopregnanolone and tetrahydrocorticosterone (THDOC), which potentiate inhibitory GABA signalling, thereby playing a role in the negative control of the hypothalamic-pituitary-adrenal (HPA) axis. Prenatally stressed (PNS) offspring exhibit increased vulnerability to stress-related disorders and frequently display exaggerated HPA axis responses to stressors during adulthood, which may be a result of reduced neuroactive steroid production and consequently inhibitory signalling. Here, we investigated whether exposure of rats to prenatal social stress from gestational day 16-20 altered neuroactive steroid production under non-stress conditions and in response to an acute stressor (swim stress) in adulthood. Using liquid chromatography-mass spectrometry, nine neuroactive steroids were quantified (corticosterone, deoxycorticosterone [DOC], dihydrodeoxycorticosterone, THDOC, progesterone, dihydroprogesterone, allopregnanolone, pregnenolone, testosterone) in plasma and in five brain regions (frontal cortex, hypothalamus, amygdala, hippocampus, brainstem) of male and female control and PNS rats. There was no difference in the neuroactive steroid profile between control and PNS rats under basal conditions. The increase in circulating corticosterone induced by acute swim stress was similar in control and PNS offspring. However, greater stress-induced corticosterone and DOC concentrations were observed in the brainstem of male PNS offspring, whereas DOC concentrations were lower in the hippocampus of PNS females compared to controls, following acute stress. Although PNS rats did not show deficits in allopregnanolone responses to acute stress, there were modest deficits in the production of THDOC in the brainstem, amygdala, and frontal cortex of PNS males and in the frontal cortex of PNS females. The data suggest that neuroactive steroid modulation of GABAergic signalling following stress exposure may be affected in a sex- and region-specific manner in PNS offspring.

Project description:Within populations, individuals can vary in stress response, a multivariate phenomenon comprising neuroendocrine, physiological and behavioural traits.Verbal models of individual stress "coping style" have proposed that the behavioural component of this variation can be described as a single axis, with each individual's coping style being consistent across time and stress contexts.Focusing on this behavioural component of stress response and combining repeated measures of multiple traits with a novel multivariate modelling framework, we test for the existence of coping style variation and assess its stability across contexts in the Trinidadian guppy (Poecilia reticulata).Specifically, we test the following hypotheses: (1) there exists repeatable among-individual behavioural (co)variation ("personality") within a mild stress context consistent with a risk-averse-risk-prone continuum of behavioural coping style, (2) there is population-level plasticity in behaviour as a function of stressor severity, (3) there is among-individual variation in plasticity (i.e. IxE), and (4) the presence of IxE reduces cross-context stability of behavioural coping style.We found significant repeatable among-individual behavioural (co)variation in the mild stress context (open field trial), represented as an I matrix. However, I was not readily described by a simple risk-averse-risk-prone continuum as posited by the original coping style model. We also found strong evidence for population-level changes in mean behaviour with increasing stressor severity (simulated avian and piscine predation risks).Single-trait analyses did show the presence of individual-by-environment interactions (IxE), as among-individual cross-context correlations were significantly less than +1. However, multitrait analysis revealed the consequences of this plasticity variation were minimal. Specifically, we found little evidence for changes in the structure of I between mild and moderate stress contexts overall, and only minor changes between the two moderate contexts (avian vs. piscine predator).We show that a multivariate approach to assessing changes in among-individual (co)variance across contexts can prevent the over-interpretation of statistically significant, but small, individual-by-environment effects. While behavioural flexibility enables populations (and individuals) to respond rapidly to changes in the environment, multivariate personality structure can be conserved strongly across such contexts. A plain language summary is available for this article.

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Prenatal stress and stress coping style interact to predict metabolic risk in male rats.

Publications

Prenatal stress and stress coping style interact to predict metabolic risk in male rats.

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