Titrating the Smell of Fear: Initial Evidence for Dose-Invariant Behavioral, Physiological, and Neural Responses

Abstract

It is well accepted that emotional intensity scales with stimulus strength. Here, we used physiological and neuroimaging techniques to ask whether human body odor—which can convey salient social information—also induces dose-dependent effects on behavior, physiology, and neural responses. To test this, we first collected sweat from 36 males classified as low-, medium-, and high-fear responders. Next, in a double-blind within-subjects functional-MRI design, 31 women were exposed to three doses of fear-associated human chemosignals and neutral sweat while viewing face morphs varying between expressions of fear and disgust. Behaviorally, we found that all doses of fear-sweat volatiles biased participants toward perceiving fear in ambiguous morphs, a dose-invariant effect generally repeated across physiological and neural measures. Bayesian dose-response analysis indicated moderate evidence for the null hypothesis (except for the left amygdala), tentatively suggesting that the human olfactory system engages an all-or-none mechanism for tagging fear above a minimal threshold.

Olfaction in the Multisensory Processing of Faces: A Narrative Review of the Influence of Human Body Odors

“…These findings indicate that visual and olfactory stimuli were integrated in an emotion-congruent manner (i.e., based on the redundant fear information), resulting in a face percept biased toward fear. Similar findings were recently reported using fear-todisgust morphed faces, with "disgust" faces being perceived as more "fearful" by female participants after sniffing fear axillary sweat (de Groot et al, 2021). Fear axillary odor was also found to shorten the time interval that fear faces, but not disgust or neutral faces, took to reach visual awareness using a breaking Continuous Flash Suppression technique (i.e., b-CFS, the dichoptic presentation of dynamic noise to the dominant eye and a target stimulus to the other, which momentarily suppresses the target stimulus from visual awareness), again in a sample of female participants (Silvia et al, 2020).…”

“…Accordingly, because olfaction may be seen as a "weak sense" compared to the "dominant" visual system in adult humans, olfactionto-vision interactions are usually reported in situations where quality of visual signals is not optimal (e.g., in early development) or degraded (e.g., Zhou et al, 2010;Kuang and Zhang, 2014), thereby making the reliability of visual and olfactory estimates comparable. Overall, the findings reviewed here nonetheless indicate that human chemosensory stimuli can have a substantial influence on the visual processing of faces, impacting situations of visual ambiguity (e.g., Zhou and Chen, 2009;Zernecke et al, 2011;Kamiloglu et al, 2018;de Groot et al, 2021), though not limited to them (e.g., de Groot et al, 2015b;Wudarczyk et al, 2016). This discrete but pervasive influence of olfaction on visualsocial processing may appear surprising when considering that, in many cases, the visual perceptual estimates were not especially compromised.…”

“…These olfactory differences combined with findings reporting that women are also slightly better in processing social-emotional information (Proverbio et al, 2008;Proverbio, 2017) logically led to the observed male-female asymmetry in processing emotional chemosensory stimuli (de Groot et al, 2014a). Hence, to maximize the likelihood of finding an effect, many studies tested only female receivers exposed to body odor from male senders (e.g., de Groot et al, 2015bde Groot et al, , 2021, because men possess larger apocrine sweat glands producing more intense body odor and are not subject to menstrual fluctuations of emission (Chen and Haviland-Jones, 1999;Sergeant, 2010). The downside of such experimental setting is the questionable generalizability of the results to the male population of odor receivers on the one hand, and to the female population as odor emitters on the other hand.…”

“…Each emotional state is associated with a specific neurophysiological pattern (a definable brain circuit or affect program) producing particular expressive behaviors (e.g., facial expressions), and distinct autonomic correlates (Ekman, 1992a,b;Izard, 1993;Panksepp, 1998;Buck, 1999;Cacioppo et al, 2000;Cosmides and Tooby, 2000;LeDoux, 2000). According to this perspective, emotional chemosensory cues in senders should induce discrete emotions , which should translate in receivers displaying emotion-specificity in their response to the chemosensory stimulation (e.g., Zhou and Chen, 2009;Zernecke et al, 2011;Kamiloglu et al, 2018;de Groot et al, 2021).…”

“…Spontaneously processed as carrying social information (Pause, 2012), body odors easily bind with face-related visual cues in a multisensory percept (Cecchetto et al, 2020), and overall, social smells bear on how we look at faces. However, large discrepancies emerge across studies in the way chemosensory information is integrated with faces, ranging from the multisensory integration of what seems redundant properties (e.g., identity: Platek et al, 2004;emotion: Zhou and Chen, 2009;Kamiloglu et al, 2018;de Groot et al, 2021) to a more loosely matched correspondence with a rather unspecific influence of body odors (e.g., sex: Mutic et al, 2016;emotion: Mujica-Parodi et al, 2009;de Groot et al, 2015b;Rocha et al, 2018;health: Regenbogen et al, 2017).…”