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Abstract
Communicating threats and stress via biological signaling is common in animals. In humans, androstadienone (ANDR), a synthetic male steroid, is a socially relevant chemosignal exhibited to increase positive mood and cortisol levels specifically in (periovulatory) females in positively arousing contexts. In a negative context, we expected that such effects of ANDR could amplify social evaluative threat depending on the stress sensitivity, which differs between menstrual cycle phases. Therefore, this fMRI study aimed to examine psychosocial stress reactions on behavioral, hormonal and neural levels in 31 naturally cycling females, between 15 early follicular (EF) and 16 mid-luteal (ML) females tested with ANDR and placebo treatment in a repeated-measures design. Regardless of odor stimulation, psychosocial stress (i.e., mental arithmetic task with social evaluative threat) led to elevated negative mood and anxiety in all females. A negative association of social threat related amygdala activation and competence ratings appeared in ML-females, indicating enhanced threat processing by ANDR, particularly in ML-females who felt less competent early in the stress experience. Further, ML-females showed reduced performance and stronger stress-related hippocampus activation compared to EF-females under ANDR. Hippocampal activation in ML-females also correlated positively with post-stress subjective stress. Contrarily, such patterns were not observed in EF-females or under placebo in either group. Strikingly, unlike passive emotional processing, ANDR in a stressful context decreased cortisol concentration in all females. This points to a more complex interaction of ovarian/gonadal hormones in social threat processing and stress reactivity. Our findings suggest that ANDR enhanced initial evaluation of self-related social threat in ML-females. Female stress reactions are related to stress sensitivity through enhanced awareness and processing of social cues in a stressful context, with menstrual cycle phase being a critical factor.
Highlights
The presence of social chemosignals in nature facilitates social communication and modulates emotional behaviors between conspecifics
One might expect that presence of a male steroid should amplify female stress reactions resembling social evaluation by male experimenters
Social evaluative threat and sense of uncontrollability were increased by variable time pressure and performance monitoring on a visual scale, which was of particular interest for the effect of ANDR on social evaluative threat
Summary
The presence of social chemosignals in nature facilitates social communication and modulates emotional behaviors between conspecifics. After sniffing pure ANDR, females showed elevated cortisol and reduced negative mood ratings during a positively arousing context (Wyart et al, 2007), probably triggered by a stronger hypothalamic activation (Savic et al, 2001; Burke et al, 2012) Based on these earlier findings, it has been speculated that the properties of ANDR enhance autonomic arousal and probably act to increase sensitivity to social evaluative threat during psychosocial stress (Lübke and Pause, 2015). In a negative context, ANDR may potentiate evaluation of self-related social threat (i.e., failing to perform under expectation), which may intensify psychosocial stress. This effect may be associated with the menstrual cycle
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