Behavioral and neural correlates to multisensory detection of sick humans

Abstract

Throughout human evolution, infectious diseases have been a primary cause of death. Detection of subtle cues indicating sickness and avoidance of sick conspecifics would therefore be an adaptive way of coping with an environment fraught with pathogens. This study determines how humans perceive and integrate early cues of sickness in conspecifics sampled just hours after the induction of immune system activation, and the underlying neural mechanisms for this detection. In a double-blind placebo-controlled crossover design, the immune system in 22 sample donors was transiently activated with an endotoxin injection [lipopolysaccharide (LPS)]. Facial photographs and body odor samples were taken from the same donors when "sick" (LPS-injected) and when "healthy" (saline-injected) and subsequently were presented to a separate group of participants (n = 30) who rated their liking of the presented person during fMRI scanning. Faces were less socially desirable when sick, and sick body odors tended to lower liking of the faces. Sickness status presented by odor and facial photograph resulted in increased neural activation of odor-and faceperception networks, respectively. A superadditive effect of olfactory-visual integration of sickness cues was found in the intraparietal sulcus, which was functionally connected to core areas of multisensory integration in the superior temporal sulcus and orbitofrontal cortex. Taken together, the results outline a disease-avoidance model in which neural mechanisms involved in the detection of disease cues and multisensory integration are vital parts.body odor | lipopolysaccharide | endotoxin | sickness cues | disease avoidance

Disease avoidance, and breeding group age and size condition the dispersal patterns of western lowland gorilla females

“…An abnormal aspect of the face can be used to appraise the health status of other individuals (Regenbogen et al. ). We suppose that in gorillas, behavioral signals, comparable to disgust in humans, can function as a disease‐avoidance mechanism that could be acquired throughout individual development and into adulthood (Oaten et al.…”

Social neuroscience of disgust

“…In humans the axillary odors of men administered LPS were rated as less pleasant and healthy than either placebo treated individuals or prior to treatments . Likewise the faces of individuals given LPS were rated as less desirable, with a further reduction with the presentation of LPS treated odor . In this regard there is suggestive evidence that heightened olfactory sensitivity is associated with the augmented expression of disgust and enhanced perceptual vigilance .…”

“…There is evidence that odor cues are also used to recognize and socially avoid infected same‐ and opposite‐sex conspecifics in humans and non‐human primates . In both humans and rodents stimulation of the immune system by systemic administration of LPS, results in a coordinated set of adaptive behavioral responses termed “sickness behavior”.…”

“…The threats to territory, resources and, importantly risk of pathogen exposure posed by individuals from out‐groups (unfamiliar individuals, strangers, foreigners, outsiders) are important determinants of social interactions in humans . There is evidence that in humans disgust is associated with a heightened sensory awareness, including that of odors and a greater salience of the negative sensory cues posed by out groups . These threats may bias social preferences and interactions eliciting disgust and promote affiliation, interactions and cooperation with in‐group individuals.…”

Exogenous attention and memory for faces following contextual behavioral immune system activation

“…Importantly, the face provides valuable information about the health state of individuals, which is essential to the elicitation/activation of avoidance behaviors (Kouznetsova, et al ., ). Consistent with this notion, two recent studies showed that participants were able to identify (above chance level) sickness cues in faces of individuals who were previously injected with a bacterial stimulus that elicited an immune response (Axelsson, Sundelin, Olsson et al ., ; Regenbogen, Axelsson, Lasselin et al ., ). Thus, even though some studies have already investigated cognitive processes associated with face processing, more studies are needed to further corroborate and explore different aspects of attention and memory associated with this type of processing, such as exogenous attention and recognition memory, particularly when a priming effect is at stake.…”