Oxytocin reduces a chemosensory-induced stress bias in social perception

Abstract

Social transmission of fear is not restricted to visual or auditory cues, but extends to the phylogenetically more ancient olfactory domain. Anxious individuals exhibit heightened sensitivity towards chemosensory stress signals in sweat; however, it is still unknown whether endogenous neuromodulators such as the peptide hormone oxytocin (OXT) influence the chemosensory communication of stress. Here, we investigated whether OXT selectively diminishes behavioral and neural responses to social chemosensory stress cues utilizing a randomized, double-blind, placebo (PLC)-controlled, within-subject functional MRI study design. Axillary sweat was obtained from 30 healthy male donors undergoing the Trier Social Stress Test (stress) and bicycle ergometer training (sport). Subsequently, 58 healthy participants (30 females) completed a forced-choice emotional face recognition task with stimuli of varying intensities (neutral to fearful) while they were exposed to both sweat stimuli and a non-social control odor following intranasal OXT or PLC administration, respectively. OXT diminished stress-induced recognition accuracy and response time biases towards fear. On the neural level, OXT reduced stress-evoked responses in the amygdala in both sexes, the anterior cingulate cortex (ACC) in females, and the hippocampus in males. Furthermore, OXT reinstated the functional connectivity between the ACC and the fusiform face area that was disrupted by stress odors under PLC. Our findings reveal a new role for OXT signaling in the modulation of chemosensory communication of stress in humans. Mechanistically, this effect appears to be rooted in a downregulation of stress-induced limbic activations and concomitant strengthening of top-down control descending from the ACC to the fusiform face area.

Behavioral and Neurobiological Convergence of Odor, Mood and Emotion: A Review

“…elevated oxytocin, via its action in the AON, can enhance recognition of social odor cues, such as those of partners or kin (Oettl et al, 2016). In humans, oxytocin also modulates responsiveness to social odors (Maier et al, 2019), though a link to receptors in AON has not been determined.…”

Chemical Fingerprints of Emotional Body Odor

“…Other assessments have focused on effects of chemical signals in relation to real-life settings such as influencing social judgment [29], and clinical performance of dental students [30]. Similarly, recordings of brain activity have been assessed with findings indicating higher event-related potentials at various time points (e.g., [31,32]), increased amygdala activity [33,34], and recruiting a wider network of brain regions in relation to empathy [35].…”

Oxytocin enhances the pain‐relieving effects of social support in romantic couples

“…A better understanding of the underlying mechanism of action is important because an increasing number of studies indicate that the potential clinical effects of OXT are person-and context-dependent (Bartz, Zaki, Bolger, & Ochsner, 2011;Olff et al, 2013) and vary as a function of attachment organization and social support. Furthermore, it has been shown that OXT not only modulates activity in the insular cortex (Striepens et al, 2012;Wigton et al, 2015) and VMPFC (Aoki et al, 2015;Labuschagne et al, 2012) but also reduces the neural response to stress-associated signals (Maier et al, 2018) and painful stimuli in the amygdala (AMY) (Paloyelis et al, 2016). Furthermore, it has been shown that OXT not only modulates activity in the insular cortex (Striepens et al, 2012;Wigton et al, 2015) and VMPFC (Aoki et al, 2015;Labuschagne et al, 2012) but also reduces the neural response to stress-associated signals (Maier et al, 2018) and painful stimuli in the amygdala (AMY) (Paloyelis et al, 2016).…”