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Diurnal cortisol amplitude and fronto-limbic activity in response to stressful stimuli.

ABSTRACT: The development and exacerbation of many psychiatric and neurologic conditions are associated with dysregulation of the hypothalamic pituitary adrenal (HPA) axis as measured by aberrant levels of cortisol secretion. Here we report on the relationship between the amplitude of diurnal cortisol secretion, measured across 3 typical days in 18 healthy individuals, and blood oxygen level dependant (BOLD) response in limbic fear/stress circuits, elicited by in-scanner presentation of emotionally negative stimuli, specifically, images of the World Trade Center (WTC) attack. Results indicate that subjects who secrete a greater amplitude of cortisol diurnally demonstrate less brain activation in limbic regions, including the amygdala and hippocampus/parahippocampus, and hypothalamus during exposure to traumatic WTC-related images. Such initial findings can begin to link our understanding, in humans, of the relationship between the diurnal amplitude of a hormone integral to the stress response, and those neuroanatomical regions that are implicated as both modulating and being modulated by that response.

SUBMITTER: Cunningham-Bussel AC

PROVIDER: S-EPMC4250041 | biostudies-literature | 2009 Jun

REPOSITORIES: biostudies-literature

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Diurnal cortisol amplitude and fronto-limbic activity in response to stressful stimuli.

Cunningham-Bussel Amy C AC Root James C JC Butler Tracy T Tuescher Oliver O Pan Hong H Epstein Jane J Weisholtz Daniel S DS Pavony Michelle M Silverman Michael E ME Goldstein Martin S MS Altemus Margaret M Cloitre Marylene M Ledoux Joseph J McEwen Bruce B Stern Emily E Silbersweig David D

Psychoneuroendocrinology 20090109 5

The development and exacerbation of many psychiatric and neurologic conditions are associated with dysregulation of the hypothalamic pituitary adrenal (HPA) axis as measured by aberrant levels of cortisol secretion. Here we report on the relationship between the amplitude of diurnal cortisol secretion, measured across 3 typical days in 18 healthy individuals, and blood oxygen level dependant (BOLD) response in limbic fear/stress circuits, elicited by in-scanner presentation of emotionally negati ...[more]

PMID: 19135805

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Project description:OBJECTIVES:Adults with bipolar disorder (BD) display aberrant activation in fronto-limbic neural circuitry during cognitive control. However, fronto-limbic response to cognitive control, and factors destabilizing this circuitry, remain under-studied during the transition from adolescence to young adulthood in BD. Sleep patterns are disturbed in BD, undergo change in adolescence, and support brain function. Among transitional age youth, BD diagnosis and sleep (duration and variability) were tested as predictors of fronto-limbic response to a stressful cognitive control task. METHODS:Two groups of youth (13-22 years old) participated: 15 with BD type I, II or not otherwise specified (NOS) [BD; age 18.1 ± 2.7 years (mean ± standard deviation, SD); 17 female] and 25 healthy controls [CTL; age 19.4 ± 2.7 years (mean ± SD); 17 female]. Sleep was monitored with actigraphy for at least 1 week prior to an adaptive multi-source interference functional magnetic resonance imaging (fMRI) paradigm (a Stroop-like cognitive interference task). Group status and sleep duration (average and intra-individual variability) were examined as predictors of activation in response to incongruent>congruent trials within the bilateral amygdala, anterior cingulate (ACC), ventrolateral prefrontal and dorsolateral prefrontal cortical regions of interest. RESULTS:The BD group displayed greater right amygdala activation than the CTL group. Average sleep duration and rostroventral ACC (rvACC) activity were negatively associated in the CTL group, but exhibited a quadratic relationship in the BD group such that short and long sleep were related to greater rvACC activation. Sleep duration variability and dorsal ACC activity were negatively associated in the BD group, and unrelated in the CTL group. Findings remained significant after controlling for age, sex, and mood symptoms. CONCLUSIONS:Subjects with BD displayed a hyper-limbic response during cognitive control, and sleep was a source of variability in ACC engagement. Stabilizing sleep may be one avenue for improving cognitive control in BD.

Project description:Inter-individual variability in metrics of hypothalamic-pituitary-adrenocortical (HPA) activity, such as the slope of the diurnal decline in cortisol, cortisol awakening response (CAR), and total cortisol output, have been found to associate inversely with trait ratings of extraversion and positive affect (E/PA) and positively with neuroticism and negative affect (N/NA) in some, but not all, investigations. These inconsistencies may partly reflect varied intensity of cortisol sampling among studies and reliance on self-rated traits, which are subject to reporting biases and limitations of introspection. Here, we further examined dispositional correlates of HPA activity in 490 healthy, employed midlife volunteers (M age=43 years; 54% Female; 86% white). Trait ratings were requested from participants and 2 participant-elected informants using the Positive and Negative Affect Schedule (PANAS) and Extraversion and Neuroticism dimensions of NEO personality inventories. CAR was assessed as percent increase in cortisol levels from awakening to 30min after awakening; and the diurnal slope and total output of cortisol [Area Under the Curve (AUC)] were determined from cortisol measurements taken at awakening, +4 and +9h later, and bedtime, across 3 workdays. Structural equation modeling was used to estimate multi-informant E/PA and N/NA factors. We used 3days of measurement as indicators to model each of the three latent cortisol factors (slope, CAR, and AUC). With the two latent emotionality and three latent cortisol indices included there was good fit to the data (?(2)(200)=278.38, p=0.0002; RMSEA=0.028, 90% CI=0.02-0.04; CFI/TLI=0.97/0.96; SRMR=0.04). After controlling for covariates (age, sex, race), results showed higher latent E/PA associated with a steeper diurnal slope (Standardized ?=-0.19, p=0.02) and smaller CAR (Standardized ?=-0.26, p=0.004), whereas N/NA did not associate with any cortisol metric (Standardized ?'s=-0.12 to 0.13, p's=0.10 to 0.53). These findings suggest that positive emotionality may be more closely associated with indices of diurnal cortisol release than negative emotionality.

Project description:Abnormal hypothalamic-pituitary-adrenal (HPA) axis function, as indexed by elevated diurnal cortisol levels and/or a blunted cortisol awakening response (CAR), has been observed among patients with first episode psychosis and associated with neurocognitive deficits in this population. However, the extent to which these features precede illness onset is unclear. The current study aimed to determine whether children who are at putatively elevated risk for psychosis because they present multiple antecedents of schizophrenia (ASz), and high-risk children with a family history of illness (FHx), are characterized by abnormal cortisol levels when compared with their typically developing (TD) peers. A further aim was to investigate the extent to which cortisol levels are associated with psychosocial stress and neurocognitive function. Thirty-three ASz children, 22 FHx children, and 40 TD children were identified at age 9-12 years using a novel community-based screening procedure or as relatives of individuals with schizophrenia. All participants were antipsychotic-naive and not currently seeking treatment for their symptoms. At age 11-14 years, participants provided salivary cortisol samples and completed psychosocial stress measures and tests of memory and executive function. Results indicated that FHx children, but not ASz children, were characterized by a blunted CAR relative to their TD peers (effect size=-0.73, p=0.01) that was not explained by psychosocial stress exposure or by distress relating to these experiences. Neither FHx nor ASz children were characterized by elevated diurnal cortisol. Among both FHx and ASz children, more pronounced HPA axis function abnormalities (i.e., higher diurnal cortisol levels and greater blunting of the CAR) were associated with poorer performance on tests of verbal memory and executive function. These findings support the notion that at least some HPA axis abnormalities described in psychosis precede illness onset, rather than being a subsequent epiphenomenon. We speculate that the blunted CAR may constitute an early (potentially genetically mediated) marker of psychosis vulnerability, whilst elevated diurnal cortisol levels may emerge only proximally to disease onset.

Dataset Information

Diurnal cortisol amplitude and fronto-limbic activity in response to stressful stimuli.

Publications

Diurnal cortisol amplitude and fronto-limbic activity in response to stressful stimuli.

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