Abstract
The communication of stress/anxiety between conspecifics through chemosensory signals has been documented in many vertebrates and invertebrates. Here, we investigate how chemosensory anxiety signals conveyed by the sweat of humans (N = 49) awaiting an academic examination are processed by the human brain, as compared to chemosensory control signals obtained from the same sweat donors in a sport condition. The chemosensory stimuli were pooled according to the donation condition and administered to 28 participants (14 males) synchronously to breathing via an olfactometer. The stimuli were perceived with a low intensity and accordingly only about half of the odor presentations were detected by the participants. The fMRI results (event-related design) show that chemosensory anxiety signals activate brain areas involved in the processing of social emotional stimuli (fusiform gyrus), and in the regulation of empathic feelings (insula, precuneus, cingulate cortex). In addition, neuronal activity within attentional (thalamus, dorsomedial prefrontal cortex) and emotional (cerebellum, vermis) control systems were observed. The chemosensory perception of human anxiety seems to automatically recruit empathy-related resources. Even though the participants could not attentively differentiate the chemosensory stimuli, emotional contagion seems to be effectively mediated by the olfactory system.
Highlights
Chemosensory alarm signals are supposed to have evolved independently within all major taxa, probably including plants [1] and are hypothesized to support evolutionary fitness [2]
Chemosensory signals of anxiety activate brain areas involved in the processing of social anxiety signals, and structures which mediate the internal representation of the emotional state of others
Insula activations are commonly observed during odor perception [33], in the present study these activations are very likely not caused by an olfactory component of the chemosensory anxiety signals
Summary
Chemosensory alarm signals are supposed to have evolved independently within all major taxa, probably including plants [1] and are hypothesized to support evolutionary fitness [2]. The release of chemosensory alarm signals is associated with activity of the pituitary-adrenal axis [3]. Different sensory systems are discussed to process stress-related social chemosignals in rodents (grueneberg ganglion cells [4], the vomeronasal organ [5], olfactory receptors [6], and trace-amine-associated receptors [7]). The processing of chemosensory anxiety signals affect perceptional performances by enhancing cognitive alertness [13], and reducing the perceptual acuity for social safety cues [14]. Chemosensory stress signals of conspecifics augment defensive reflexes (startle) in humans [15] and rats [16]. The attentional capacities for the identification of chemosensory anxiety signals appear to be limited [17,18]
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