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.
Highlights
Childhood maltreatment (CM) presents a leading risk factor for the later development of psychopathology [1], with childhood maltreatment (CM) exposure accounting for over 30% of adult-onset psychiatric disorders [2]
Aberrant amygdala activations are observed across psychiatric disorders [13] and the amygdala threat detection process has been suggested to mediate the relationship between CM and psychopathology later in life [14, 15]
Human intranasal administration of OXT enhanced the stress-buffering effects of social support during the Trier Social Stress Test (TSST) [50, 51] and we recently found that the peptide reduces amygdala reactivity to social chemosensory threat signals [27]
Summary
Childhood maltreatment (CM) presents a leading risk factor for the later development of psychopathology [1], with CM exposure accounting for over 30% of adult-onset psychiatric disorders [2]. A recent line of research demonstrates that chemosensory communication of threat cues in axillary sweat modulates cross-modal emotion perception of ambiguous threatening facial stimuli and produces widespread neural threat responses in the amygdala, ACC, hippocampus, the prefrontal cortex, and fusiform face area (FFA) [27,28,29,30]. These effects are even more pronounced in individuals with heightened stress vulnerabilities such as patients with anxiety disorders [31, 32]. We assumed that CM modulates the effects of OXT on the processing of chemosensory stress cues
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