A behavioral defense against disease

Abstract

Animals, including humans, have evolved under the continuous selection pressure posed by pathogens. As a result, we have developed a set of physiological mechanisms to combat pathogens – the immune system. However, engaging the immune system in this battle can be costly, unnecessarily so in cases when pathogens can be avoided. Recent studies have focused on the behavioral defense against disease, which helps us to avoid pathogens before they enter the body by detecting and avoiding sources of contagion. A behavioral defense can also be argued to promote recovery if infected, through so-called sickness behavior. Both aspects are related to motivational states that help the organism reorganize its priorities to promote disease avoidance and recovery. In this thesis, we investigated by which perceptual cues, facial and/or olfactory, humans are able to dissociate between sick and healthy individuals as well as how these cues can affect social liking of other people. We also investigated whether sick individuals would exhibit sickness behavior that includes relevant shifts in chemosensory perception of food and social odors.

In Study I, we investigated whether facial expressions of emotion change during sickness. Twenty-two healthy volunteers were injected with either an endotoxin (lipopolysaccharide, LPS; 2ng/kg body weight) or saline. Facial photographs of the volunteers were taken 2 hours after the injections. At a later stage, 49 naïve participants were asked to rate the emotional expressions and the perceived health of both the sick and healthy faces. The results showed that sickness had a negative effect on facial expressions of emotion. Sick faces looked significantly more sad and disgusted, as well as less happy, compared to the healthy faces. Moreover, the emotional expressions mediated 59.1% of the treatment-dependent changes in ratings of the perceived health of the faces.

In Study II, using the sick and healthy facial photographs from Study I and body odors from the same volunteers, we investigated the effects of olfactory and facial (visual) disease cues on social liking. We also assessed whether individual traits such as perceived vulnerability to disease, disgust sensitivity, and health anxiety could influence participants’ liking ratings. Seventy-seven participants were presented with sick and healthy facial photographs and body odors in a 2 x 2 factorial design. During the presentation of the stimuli, facial electromyographic activity was recorded as an objective measure of participants’ own facial expressions of emotion. The results revealed a negative main effect of both facial and body odor sickness cues on liking ratings, indicating that sick individuals are liked less than their healthy counterparts. No significant effect of sickness cues on facial electromyographic activity was found. Finally, we showed that participants who perceived themselves as more vulnerable to disease liked the presented volunteers less [than other participants did], regardless of health status.

In Study III, we sought to examine if, apart from experimentally induced inflammation, naturally occurring inflammation can result in an altered body odor. As in Study II, the effect of individual traits – perceived vulnerability to disease, disgust sensitivity, and health anxiety – on sickness perception was also assessed. Body odors were collected from 23 volunteers who were experiencing respiratory infections. Three weeks later, body odors from the same individuals were collected again, after they had recovered. In a later stage, 46 participants rated the body odors in terms of intensity, disgust, pleasantness, and health. Our results showed that the sick body odors, in line with hypotheses, smelled nominally more intense, more disgusting, and less healthy compared to the healthy body odors, though these results did not reach statistical significance. Moreover, there was no association between the individual traits and body odor perception.

In Study IV, we assessed the effect of sickness on odor and taste perception. Relevant to this study is the fact that sickness behavior entails both a loss of appetite and social withdrawal. Using an experimental disease model, 40 participants received LPS (between 0.51 and 0.80 ng/kg body weight) or saline injections. They were then presented with eight different odors (two food odors, three social odors, and three control odors) and four different basic tastes (plus a control) and asked to rate the intensity and pleasantness of these stimuli. In line with the hypothesis, participants perceived food odors as significantly less pleasant when they were sick. No significant effect of sickness on ratings of social odors, control odors, or tastes was found.

In conclusion, the present thesis reveals a number of perceptual sickness cues with the potential to trigger avoidance or limit approach behavior. These cues are available as early as a few hours after the induction of systemic inflammation. Once sick, an individual demonstrates less motivation to consume food, as indicated by a dampened perception of food odor pleasantness, likely in favor of allocating resources to recovery. Avoiding the sickness cues and engaging in the sickness behaviors identified in this thesis may be important in a behavioral defense against disease that helps us stay alive and healthy.