Dataset Information

Childhood Maltreatment Alters the Neural Processing of Chemosensory Stress Signals.

ABSTRACT: Accumulating evidence suggests that childhood maltreatment (CM) confers risk for psychopathology later in life by inducing hypervigilance to social threat cues such as fearful faces. However, it remains unclear whether the modulatory impact of CM extents to the olfactory domain of social communication in humans. To address this question, we examined whether CM modulates the neural processing of chemosensory threat signals in sweat and whether CM affects the stress-reducing effects of oxytocin (OXT) in this context. In a randomized, double-blind within-subject functional MRI study design, 58 healthy participants (30 females) received intranasal OXT (40 IU) or placebo (PLC) and completed a forced-choice emotion recognition task with faces of varying emotion intensities (neutral to fearful) while exposed to sweat stimuli and a non-social control odor. Axillary sweat samples were collected from 30 healthy male donors undergoing an acute psychosocial stressor (stress) and ergometer training (sport) as control in a pre-study. CM was assessed by the 25-item Childhood Trauma Questionnaire (CTQ). The final fMRI analysis included 50 healthy participants (26 females). Regression analysis showed a stress-specific association of CTQ scores with amygdala hyperreactivity, hippocampal deactivation, and increased functional connectivity between the amygdala and the hippocampus, medial orbitofrontal cortex, and the anterior cingulate cortex (ACC) under PLC. Furthermore, we observed a positive association of CTQ scores and the dampening effects of OXT on stress-related amygdala responses. Our findings suggest that CM may induce hypervigilance to chemosensory threat cues in a healthy sample due to inefficient frontolimbic inhibition of amygdala activation. Future studies should investigate whether increased recruitment of the intralimbic amygdala-hippocampus complex reflects a compensatory mechanism that prevents the development of psychopathology in those who have experienced CM. Furthermore, the results reveal that the stress-specific effects of OXT in the olfactory domain are more pronounced in participants with increasing levels of CM exposure.

SUBMITTER: Maier A

PROVIDER: S-EPMC7425696 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Childhood Maltreatment Alters the Neural Processing of Chemosensory Stress Signals.

Maier Ayline A Heinen-Ludwig Luca L Güntürkün Onur O Hurlemann René R Scheele Dirk D

Frontiers in psychiatry 20200806

Accumulating evidence suggests that childhood maltreatment (CM) confers risk for psychopathology later in life by inducing hypervigilance to social threat cues such as fearful faces. However, it remains unclear whether the modulatory impact of CM extents to the olfactory domain of social communication in humans. To address this question, we examined whether CM modulates the neural processing of chemosensory threat signals in sweat and whether CM affects the stress-reducing effects of oxytocin (O ...[more]

PMID: 32848947

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Project description:Background:Childhood maltreatment is a strong risk factor for the development of depression in later life. However, the neurobiological mechanisms underlying this vulnerability are not well understood. As depression has been associated with dysfunction of the hypothalamic-pituitary-adrenal (HPA) axis and increased responsiveness to psychosocial stressors, we speculated that childhood maltreatment may lead to lasting alteration of the stress response system, thereby increasing the risk of depression. This study investigated the effects of childhood maltreatment on the stress response in healthy subjects while controlling for psychiatric condition. Methods:Forty-eight healthy young adults (24 females) with childhood maltreatment experience and 48 healthy controls (33 females) without such experience were administered the Montreal Imaging Stress Task during functional magnetic resonance imaging. Childhood maltreatment experience was assessed using the 28-item Childhood Trauma Questionnaire (CTQ). Between-group differences in subjective stress levels, whole brain activations and cortisol levels were assessed. Results:Relative to healthy control subjects, individuals exposed to childhood maltreatment exhibited higher subjective stress and cortisol levels. Neurofunctionally, participants with histories of childhood maltreatment displayed significantly increased activation in the dorsolateral prefrontal cortex (dlPFC), insula and precuneus, and decreased activation in ventromedial prefrontal cortex (vmPFC) relative to healthy controls during the psychosocial stress task. Activations in dlPFC and insula correlated with CTQ scores in the childhood maltreatment group. Conclusion:The results of this study show that childhood maltreatment induces lasting changes in brain function and HPA-axis responsiveness to stress. The observed abnormal activation in the dlPFC, insula and vmPFC and enhanced cortisol response are similar to those seen in individuals with depression. This dysfunction might serve as a diathesis that embeds latent vulnerability to psychiatric disorders, and this mechanism provides evidence supporting the stress sensitization model.

Project description:BackgroundCognitive models of post-traumatic stress disorder (PTSD) propose that trauma entails cognitive alterations of increased distrust and perceived threat from others. We tested whether these predictions also hold in individuals with varying levels of childhood maltreatment (CM), which is much more prevalent than traumatic events as required for a PTSD diagnosis. We hypothesized that higher levels of CM would entail greater distrust and perceived threat, and that distrust would be more change-resistant in participants with more CM.MethodsThe study was pre-registered; the pre-registration protocol, data, and code are available at https://osf.io/pufy2/ . We recruited 549 participants (M age = 29.2, 74.5% women) for an online study via websites related to CM, Borderline Personality Disorder, and via snowball method on social media. Participants self-reported their level of CM on the childhood trauma questionnaire (CTQ). Next, they played two rounds of a hypothetical distrust game, indicating the perceived trustworthiness of avatars by way of estimating expected monetary deductions from them (i.e. higher amounts indicating greater distrust). After the first round, we provided participants with the feedback that very little money was taken from them. We expected those with more CM to be less responsive to the positive feedback and to adapt their estimates less in the subsequent round. Following the distrust game, participants completed an emotion rating task in which they rated the emotional expressions of 60 faces on a scale from 'very negative' to 'very positive'. We included angry, fearful, and happy facial expressions, and expected individuals with higher CM levels to provide more negative ratings. We conducted linear mixed effects models with random intercepts for raters and stimuli (crossed), and modelled random slopes for all within-person predictors.ResultsAs hypothesized, higher levels of CM were associated with higher levels of distrust and a weaker decrease in distrust following positive feedback. Further supporting our hypotheses, individuals with higher levels of CM showed more negatively shifted emotion ratings.ConclusionsIncreased distrust and perceived interpersonal threat following trauma, as proposed in cognitive models of PTSD, likely also apply to individuals with CM, following a dose-response relationship. We discuss clinical implications of considering any level of CM as a potentially relevant treatment-factor, even when a trauma-related disorder is not the main diagnosis, and propose future research avenues.

Dataset Information

Childhood Maltreatment Alters the Neural Processing of Chemosensory Stress Signals.

Publications

Childhood Maltreatment Alters the Neural Processing of Chemosensory Stress Signals.

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