Social factors and the neurobiology of pathogen avoidance

Abstract

Although the evolutionary causes and consequences of pathogen avoidance have been gaining increasing interest, there has been less attention paid to the proximate neurobiological mechanisms. Animals gauge the infection status of conspecifics and the threat they represent on the basis of various sensory and social cues. Here, we consider the neurobiology of pathogen detection and avoidance from a cognitive, motivational and affective state (disgust) perspective, focusing on the mechanisms associated with activating and directing parasite/pathogen avoidance. Drawing upon studies with laboratory rodents, we briefly discuss aspects of (i) olfactory-mediated recognition and avoidance of infected conspecifics; (ii) relationships between pathogen avoidance and various social factors (e.g. social vigilance, social distancing (approach/avoidance), social salience and social reward); (iii) the roles of various brain regions (in particular the amygdala and insular cortex) and neuromodulators (neurotransmitters, neuropeptides, steroidal hormones and immune components) in the regulation of pathogen avoidance. We propose that understanding the proximate neurobiological mechanisms can provide insights into the ecological and evolutionary consequences of the non-consumptive effects of pathogens and how, when and why females and males engage in pathogen avoidance.

Hearing, touching, and multisensory integration during mate choice

“…A recent mice study described that 24% of agranular insular neurons encode social exploration and distinguish between anogenital, nose-to-nose, or body exploration (Miura et al, 2020 ). Insula-amygdala interconnectivity (Shi and Cassell, 1999 ; Gehrlach et al, 2020 ) for instance has to be shown to be crucially involved in positive and negative valence coding during social interactions (Ferretti et al, 2019 ; Nicolas et al, 2021 ) such as pathogen avoidance (Kavaliers et al, 2022 ). Intriguingly insula function may be decisive to discriminate between sick and healthy rats (Rieger et al, 2022 ) whereas the amygdala seems to have a preventive but not a causal role (Kwon et al, 2021 ) in signaling sickness and overall sociability.…”

Of Germs and Culture; Parasite Stress as the Origin of Individualism-Collectivism

“…A detailed description of how genes and gene expression, probably through interaction with environmental factors like early exposure to diseases, impact the tendency toward a particular cultural system and how such tendency might be reflected in neural networks is still unknown. Considering the role of OXTR rs53576 in relation to parasites and cultures, and the importance of oxytocin in facilitating various aspects of social cognition and interaction (Kavaliers et al, 2022 ), researchers need to consider the possible role of oxytocin as a neurotransmitter that can chain infectious diseases and cultures. Research on disgust, the emotion that fuels pathogen avoidance, can also shed light on the origin of individualism-collectivism.…”

Infectious disease and cognition in wild populations

“…Moreover, little is known about the fitness, population, and community consequences of infection-linked cognitive impairment in wild animals, which could be profound for species that rely heavily on cognitive abilities However, a changing pathogen community could also place selection pressure on aspects of perception (B) that enable individuals to identify infected individuals (e.g., detection of visual and olfactory cues in birds [5] and primates [90], respectively). Selection could also act on the neurobiological response (sensitivity) to these cues after perception (C), which can vary with internal state and external environment and contribute to differences in behavioral responses, as reviewed for rodents [7] and bees [85]. Responses to perceived infection risk (D) can range from avoidance to caregiving, as documented in human and non-human primates [6,84], flies [8], and rodents [7].…”

“…Selection could also act on the neurobiological response (sensitivity) to these cues after perception (C), which can vary with internal state and external environment and contribute to differences in behavioral responses, as reviewed for rodents [7] and bees [85]. Responses to perceived infection risk (D) can range from avoidance to caregiving, as documented in human and non-human primates [6,84], flies [8], and rodents [7]. The consequences of these responses (positive or negative) can lead to changes in behavior based on experience (E), such as learned taste or odor aversions in bats and flies [87,91] and learned aversion of high-risk habitats in fish [9], and ultimately select for an increased capacity to learn.…”

“…In particular, parasite pressure may select for cognitive abilities that reduce the likelihood of infection (Figure 2). These include the ability to perceive infection cues and activate the neuroendocrine and cognitive responses (e.g., working memory) that elicit appropriate behavioral responses (behavioral immunity) [7,83]. The ability to perceive disease can be based on visual, olfactory, or other cues, and is posited to be one driver of social cognition, enabling animals to identify and respond appropriately to infected conspecifics by subtle differences in appearance, voice, movement [84], or chemical stimuli [85].…”