Induction of empathy by the smell of anxiety

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.

Figure 1. Cortisol (top) and testosterone (bottom) change-scores (difference values compared to the baseline measurement: means, SDs) for male (left) and female (right) donors at the three time points (t1, t2, and t3, separated by 30 min each).

Figure 2. Trial time course.

In the beginning of each trial, participants were requested to exhale (a ball decreased in diameter for 3 s) and then to inhale (a ball increased in diameter for 3 s). After a variable interval (range = 2.6–8.5 s) a question mark appeared on the screen and the participants were asked to indicate whether they perceived an odor or not. By pressing one of the two response buttons the questions mark disappeared. If no response was given within 2.75 s, an exclamation mark appeared for 0.5 s. The trial duration was 22.75 s.

Figure 3. Brain activations of the contrast Anxiety minus Sport in 28 participants (threshold, p<0.001).

A: Insula and OFC. B: Precuneus. C: Cingulate gyrus. D: Fusiform gyurs. OFC = orbitofrontal cortex.

Figure 4. Time course of mean activations with respect to the anxiety and the sport control condition across all trials and participants [insula (x = 45 y = 12 z = 0), precuneus (x = 3 y = −54 z = 57), anterior cingulate gyrus (x = 6 y = 21 z = 21), fusiformis gyrus (x = −45 y = −60 z = −21)].