Skip to main content

Pathogen and Toxin Disgust in Rodents

  • Chapter
  • First Online:
The Handbook of Disgust Research

Abstract

From an evolutionary perspective disgust can be considered as an affective/emotional system that functions to detect signs of pathogens, toxins, and contaminants, as well as to stimulate behaviours that reduce the risk of their acquisition. Here, we briefly review the origins, expression, and regulation of disgust-like behaviour in rodents. We briefly discuss: (1) evidence for the evolutionarily conserved expression of affective states and emotions, and in particular disgust (or analogues of disgust), in rodents; (2) pathogen disgust and olfactory mediated recognition and avoidance of actual and potentially infected conspecifics; (3) toxin elicited disgust and anticipatory disgust (anticipatory nausea); (4) trade-offs with other fitness costs; (5) the neurobiological mechanisms associated with the expression and modulation of avoidance/aversive behaviours and disgust; and (6) sex differences in the expression and regulation of disgust. Unravelling the mechanisms underlying the expression and regulation of disgust and disgust-like responses is critical for understanding how both humans and non-humans respond to pathogen, toxin, and contaminant threat.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adachi, A., & Kobashi, M. (1988). Electrophysiological analysis of chemosensitive neurons within the area postrema of the rat. Prog. Brain Res. 74, 77-83.

    Article  Google Scholar 

  • Adamo, S. A., & Spiteri, R. J. (2009). He’s healthy, but will he survive the plague? Possible constraints on mate choice for disease resistance. Anim. Behav., 77, 67-78.

    Article  Google Scholar 

  • Aguilar-Rivera, M., Kin, S., Coleman, T. P., Maldonado, P. E., & Torrealba, F. (2020). Interoceptive insular cortex participates in sensory processing of gastrointestinal malaise and associated behaviors. Sci. Rep., 20, 21642.

    Article  Google Scholar 

  • Altizier, S., Nunn, C. L., Thrall, P. H., Gittleman, J. L., Antonovics, J., Cunningham, A. A., Dobson, A. P., Ezenwa, V., Jones, K. E., Pedersen, A. B., Poss, M., & Pulliam, J. R. C. (2003). Social organization and parasite risk in mammals. Integrating theory and empirical studies. Ann. Rev. Ecol. Sys., 34, 517-547.

    Article  Google Scholar 

  • Al-Shawaf, L., Lewis, D. M. G., & Buss, D. M. (2017). Sex differences in disgust: Why are women more easily disgusted than men. Emot. Rev. 10, 1-12.

    Google Scholar 

  • Anderson, D. J., & Adolphs, R. (2014). A framework for studying emotions across species. Cell, 157, 187-200.

    Article  PubMed  PubMed Central  Google Scholar 

  • Arakawa, H., Arakawa, K., & Deak, T. (2010). Oxytocin and vasopressin in the medial amygdala differentially modulate approach and avoidance behaviour towards illness-related social odour. Neuroscience, 171, 1141-1151.

    Article  PubMed  Google Scholar 

  • Arakawa, H., Cruz, S., & Deak, T. (2011). From models to mechanisms: odorant communication as a key determinant of social behavior in rodents during illness associated states. Neurosci. Biobehav. Rev., 35, 1916-1922.

    Google Scholar 

  • Batres, C., & Perrett, D. I. (2020). Pathogen disgust sensitivity changes according to the perceived harshness of the environment. Cogn. Emo. 34, 377-383.

    Article  Google Scholar 

  • Baum, M. J., & Bakker, J. (2013). Roles of sex and gonadal steroids in mammalian pheromonal communication. Front. Neuroendocrinol., 34, 268-284.

    Article  PubMed  Google Scholar 

  • Beltran-Bech, S. & Richard, F.-J. (2014). Impact of infection on mate choice. Anim. Behav., 90, 159-170.

    Article  Google Scholar 

  • Berridge, K. C. (2000). Measuring hedonic impact in animals and infants: microstructure of affective taste reactivity patterns. Neurosci. Biobehav. Rev., 24, 173-198.

    Google Scholar 

  • Berridge, K. C. (2018). Evolving concepts of emotion and motivation. Front. Psychol., 9, 1-20.

    Article  Google Scholar 

  • Boillat, N., Challet, L., Rossier, D., Kan, C., Carelton, A., & Rodriguez, I. (2015). The vomeronasal system mediates sick conspecific avoidance. Curr. Biol., 25, 251-255.

    Article  PubMed  Google Scholar 

  • Borison, H. L. (1988). Area postrema: Chemoreceptor circumventricular organ of the medulla oblongata. Prog. Neurobiol., 32, 351-390.

    Article  Google Scholar 

  • Boulet, N. P., Cloutier, C. J., Ossenkopp, K.-P., & Kavaliers, M. (2016). Oxytocin, social factors and the expression of conditioned disgust (anticipatory nausea) in male rats. Behav. Pharm., 27, 718-725.

    Article  Google Scholar 

  • Brechbuhl, J., de Valliere, A., Wood, D., Tosato, M. N., & Broillet, M.-C. (2020). The grueneberg ganglion controls odor-driven food choices in mice under threat. Comm. Biol, 3, 533.

    Article  Google Scholar 

  • Bressan, P., & Kramer, P. (2021). Progesterone does raise disgust. Horm. Behav. Advance online publication. https://doi.org/10.1016/j.yhbeh.2021.104937

  • Brizzee, K. R., & Klara, P. M. (1984). The structure of the mammalian area postrema. Fedn. Proc., 43, 2944-2948.

    Google Scholar 

  • Buck, J. C., Weinstein, S. B., & Young, H. S. (2018). Ecological and evolutionary consequences of parasite avoidance. Trends Ecol. Evol., 33, 619-632.

    Article  PubMed  Google Scholar 

  • Bufe, B., Teuchert, Y., Schmid, A., Pyrski, M., Perez-Gomez, A., Eisenbeis, J., Timm, T., Ishis, T., Lochnit, G., Bischoff, M., Mombaerts, P., Leinders-Zufall, T., & Zufall, F. (2019). Bacterial MgrB peptide activates chemoreceptor Fpr3 in mouse accessory olfactory system and drives avoidance behavior. Nature Neurosci., 10, 4889.

    Google Scholar 

  • Case, T. I., Stevenson, R. J., Byrne, R. W., & Hobaiter, C. (2020). The animal origins of disgust: reports of basic disgust in nonhuman great apes. Evol. Behav. Sci., 14, 231-260.

    Article  Google Scholar 

  • Chambers, K. C. (2015). Conditioned taste aversions. In: R.L. Doty (Ed.) Handbook of olfaction and gustation (3rd ed., pp. 865-886). John Wiley & Sons.

    Google Scholar 

  • Choleris, E., Clipperton-Allen, A. E., Phan, A., & Kavaliers, M. (2009). Neuroendocrinology of social information processing in rats and mice. Front. Neuroendocrinol., 30, 442-458.

    Article  PubMed  Google Scholar 

  • Choleris, E., Gustafsson, J.-A., Korach, K. S., Mugila, L. J., Pfaff, D. W., & Ogawa, S. (2003). An estrogen dependent 4-gene micronent regulating social recognition: a study with oxytocin and estrogen receptor –α and –β knockout mice. Proc. Natl. Acad. Sci. USA, 100, 6192-6197.

    Article  PubMed  PubMed Central  Google Scholar 

  • Choleris, E., Phan, A., Clipperton-Allen, A. E., Valsecchi, P., & Kavaliers, M. (2012). Estrogenic involvement in social learning, social recognition and pathogen avoidance. Front. Neuroendocrinol., 33, 140-159.

    Article  PubMed  Google Scholar 

  • Cloutier, C. J., Kavaliers, M., & Ossenkkopp, K.-P. (2017). Sex differences in LiCl-induced context related conditioned disgust behaviors in rats and inhibition following immune system stimulation. Pharmacol. Biochem. Behav., 152, 4-12.

    Article  PubMed  Google Scholar 

  • Cloutier, C. J., Zevy, D., Kavaliers, M., & Ossenkopp, K.-P. (2018). Conditioned disgust in rats (anticipatory nausea) to a context paired with the effects of the toxin LICl: Influences of sex and the estrous cycle. Pharmacol. Biochem. Behav., 173, 51-57.

    Article  PubMed  Google Scholar 

  • Cross-Mellor, S. K., Foley, K. A., Parker, L. A., & Ossenkopp, K.-P. (2009). Lipopolysaccharide dose-dependently impairs the rapid toxin-induced gustatory conditioning in rats consuming a sucrose-lithium chlorides solution. Brain Behav. Immun., 23, 204-216.

    Article  PubMed  Google Scholar 

  • Curtis, V. A. (2014). Infection-avoidance behaviors in humans and other animals. Trends Immunol., 35, 457-464.

    Article  PubMed  Google Scholar 

  • Debiec, J., & Olsson, A. (2017). Social fear learning: from animal models to human function. Trends Cogn. Sci., 21, 546-555.

    Article  PubMed  PubMed Central  Google Scholar 

  • De Dreu, C. K. W., & Kret, M. E. (2016). Oxytocin conditions intergroup relations through upregulated in-group empathy, cooperation, conformity, and defense. Biol. Psych., 79, 165-171.

    Article  Google Scholar 

  • Divgi, A. B. (1989). Oncologist-induced vomiting: the IGVID syndrome? New Engl. J. Med., 320, 189-190.

    Google Scholar 

  • Dolensek, N., Gehrlach, D. A., Klein, A. S., & Gogolla, N. (2020). Facial expressions of emotion states and their neuronal correlates in mice. Science, 368. 89-94.

    Article  PubMed  Google Scholar 

  • Duque-Wilckens, N., Steinman, M. Q., Busnelli, M., Chini, B., Yokoyama, S., Pham, M., Laredo, S. A., Hao, R., Perkeybile, A. M., Minie, V. A., Tan, P. R., Bales, K. L., & Trainor, B. C. (2018). Oxytocin receptors in the anteriomedial bed nucleus of the stria terminalis promote stress-induced social avoidance in females. Biol. Psych., 83, 203-213.

    Article  Google Scholar 

  • Eckel, L. A., & Ossenkopp, K.-P. (1996). Area postrema mediates the formation of rapid, conditioned palatability shifts in lithium treated rats. Behav. Neurosci. 110, 202-212.

    Article  PubMed  Google Scholar 

  • Ervin, K. S. J., Lymer, J. M., Matta, R., Clipperton-Allen, A. E., Kavaliers, M., & Choleris, E. (2015). Estrogen involvement in social behavior in rodents: rapid and long-term actions. Horm. Behav., 74, 53-76.

    Article  PubMed  Google Scholar 

  • Evans, J. C., Silk, M. J., Boogert, M. J., Hodgdon, D. J. (2020). Infected or informed? Social structure and the simultaneous transmission of information and infectious disease? Oikos, 129, 1271-1288.

    Article  Google Scholar 

  • Ezenwa, V., Ghai, R. R., McKay, A. F., & Williams, A. E. (2016). Group living and pathogen infection revisited. Curr. Op. Behav. Sci., 12, 66-72.

    Article  Google Scholar 

  • Faulkner, J., Schaller, M., Park, J. H., & Duncan, L. A. (2004). Evolved disease avoidance mechanisms and contemporary xenophobic attitudes. Group Proc. Intgr. Rel., 7, 33-53.

    Google Scholar 

  • Ferguson, J. N., Aldag, J. M., Insel, T. R., & Young, L. J. (2001). Oxytocin in the medial amygdala is essential for social recognition in the mouse. J. Neurosci., 21, 8278-8285.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ferretti, V., Maltese, F., Contarini, G., Nigro, M., Bonavia, A., Huang, H., Gigliucci, V., Morelli, G., Scheggia, D., Manago, F., Castellani, G., Lefevre, A., Cancedda, L., Chini, B., Grinevich, V., & Papaleo, F. (2019). Oxytocin signaling in the central amygdala modulates emotion discrimination in mice. Curr. Biol., 29, 1-16.

    Article  Google Scholar 

  • Fleischman, D. S., & Fessler, D. M. T. (2011). Progesterone’s effects on the psychology of disease avoidance: Support for the compensatory behavioral prophylaxis hypothesis. Horm. Behav., 59, 271-275.

    Article  PubMed  Google Scholar 

  • Freeland, W. J. (1976). Pathogens and the evolution of primate sociality. Biotropica, 8, 12-24.

    Article  Google Scholar 

  • Gabor, C. S., Phan, A., Clipperton-Allen, A. E., Kavaliers, M., & Choleris, E. (2012). Interplay of oxytocin, vasopressin, and sex hormones in the regulation of social recognition. Behav. Neurosci., 126, 97-109.

    Article  PubMed  Google Scholar 

  • Galef, B. G., Lim, T. C. W., & Gilbert, G. S. (2008). Evidence of mate choice copying in Norway rats, Rattus norvegicus. Anim. Behav., 75, 117-1123.

    Article  Google Scholar 

  • Garcia, J., Hankins, W. G., & Rusiniak, K. W. (1974). Behavioral regulation of the milieu interne in man and rat. Science, 185, 824-831.

    Article  PubMed  Google Scholar 

  • Garcia, J., Laister, P. S., Bermudez-Rattoni, F., & Deems, D. A. (1985). A general theory of aversion learning. Ann. NY Acad. Sci., 443, 8-21.

    Article  PubMed  Google Scholar 

  • Gehrlach, D. A., Dolensek, N., Klein, A. S., Chowdhury, R. R., Matthys, A., Junghanel, M., Gaitanos, T. N., Podgornik, A., Black, T. D., Vaka, R. N., Conzelmann, K.-K., & Gogolla, N. (2019). Aversive state processing in the posterior insular cortex. Nat. Neurosci., 22, 1424-1437.

    Article  PubMed  Google Scholar 

  • Goodson, J. L. (2013). Deconstructing sociality, social evolution and relevant nonapeptide functions. Psychoneuroendocrinology, 38, 465-478.

    Article  PubMed  Google Scholar 

  • Grill, H. J., & Berridge, K. C. (1985). Taste reactivity as a measure of the neural control of palatability. Prog. Psychobiol. Physiol. Psychol., 11, 1-61.

    Google Scholar 

  • Grill, H. J., & Norgen, R. (1978). The taste reactivity test I. Mimetic responses to gustatory stimuli in neurologically intact rats. Brain Res. 143, 263-279.

    Google Scholar 

  • Guitton, M. J., Klin, Y., & Dudai, Y. (2008). Taste-dependent sociophobia: When food and company do not mix. Behav. Brain Res., 191, 148-152.

    Article  PubMed  Google Scholar 

  • Hamasato, E. K., Lovelock, D., Palermo-Neo, J., & Deak, T. (2017). Assessment of social behaviour directed toward sick partners and its relation to central cytokine expression in rats. Physiol. Behav., 182, 128-136.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hamilton, W. D., & Zuk, M. (1982). Heritable true fitness and bright birds: a role for parasites. Science, 218, 384-387.

    Article  PubMed  Google Scholar 

  • Hart, B. L. (2011). Behavioural defence in animals against pathogens and parasites: parallels with the pillars of medicine in humans. Phil. Trans. R. Soc B, 366, 3406.

    Article  PubMed  PubMed Central  Google Scholar 

  • Horn, C. C., Kimball, B. A., Wang, H., Kaus, J., Dienel, S., Nagy, A., Gaithright, G. R., Yates, B. J., & Andrews, P. L. R. (2013). Why can’t rodents vomit? A comparative behavioural, anatomical, and physiological study. PLOS One, 8, e60537.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hornby, P. J. (2001). Central neurocircuitry associated with emesis. Amer Jour.Med., 111, 106-112, 2001.

    Google Scholar 

  • Hurst, J. L. (2009). Female recognition and assessment of males through scent. Behav. Brain. Res., 22, 295-303.

    Article  Google Scholar 

  • Johnson, Z. V., Walum, J. H., Xiao, Y., Riefkohl, P. C., & Young, L. J. (2017). Oxytocin receptors modulate a social salience network in male prairie voles. Horm. Behav., 87, 16-24.

    Article  PubMed  Google Scholar 

  • Jones, R. C., Hahn, A. C., Fisher, C. I., Wang, H., Kandrik, M., Lee, A. J., Tybur, J. M., & DeBruine, L. M. (2018). Hormonal correlates of pathogen disgust: testing the compensatory prophylaxis hypothesis. Evol. Hum. Behav. 39, 166-169.

    Article  Google Scholar 

  • Joye, P., & Kawecki, T. J. (2019). Sexual selection favours good or bad genes for pathogen resistance depending on males’ pathogen exposure. Proc. R. Soc. B, 286, 20190226.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jurek, B., & Neumann, I. D. (2018). The oxytocin receptor: from intracellular signaling to behavior. Physiol. Rev., 98, 1805-1908.

    Google Scholar 

  • Kappeler, P. M., Cremer, S., & Nunn, C. L. (2015). Sociality and health: impacts of sociality on disease susceptibility and transmission in animal and human societies. Phil. Trans. Roy. Soc. B, 370, 20140116.

    Article  Google Scholar 

  • Kavaliers, M., Bishnoi, I. R., Ossenkopp, K.-P., & Choleris, E. (2021). Differential effects of progesterone on social recognition and the avoidance of pathogen threat by female mice. Horm. Behav. 127, 104873.

    Article  PubMed  Google Scholar 

  • Kavaliers, M., & Choleris, E. (2018). The role of social cognition in parasite and pathogen avoidance. Phil. Trans. Roc. Soc. B, 373, 20170206.

    Article  Google Scholar 

  • Kavaliers, M., Choleris, E., Ǻgmo, A., Braun, W. J., Colwell, D. D., Muglia, L. J., Ogawa, S., & Pfaff, D.W. (2006). Inadvertent social information and the avoidance of parasitized male mice: a role for oxytocin. Proc. Natl. Acad. Sci. USA, 103, 4293-4298.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kavaliers, M., Choleris, E., & Colwell, D. D. (2001). Learning from others to cope with biting flies: social learning of fear-induced conditioned analgesia and active avoidance. Behav. Neurosci., 115, 661-674.

    Article  PubMed  Google Scholar 

  • Kavaliers, M., Colwell, D. D., & Choleris, E. (2005). Kinship, familiarity and social status modulate social learning about “micropredators” (biting flies) in deer mice. Behav. Ecol. Sociobiol., 58, 60-71.

    Article  Google Scholar 

  • Kavaliers, M., Colwell, D. D., Choleris, E., Agmo, A., Mugila, L. J., Ogawa, S., & Pfaff, D. W. (2003). Impaired discrimination of and aversion to parasitized male odors by female oxytocin knockout mice. Genes. Brain. Behav., 2, 220-230.

    Article  PubMed  Google Scholar 

  • Kavaliers, M., Colwell, D. D., Cloutier, C. J., Ossenkopp, K.-P., & Choleris, E. (2014). Pathogen threat and unfamiliar males rapidly bias the social responses of female mice. Anim. Behav., 97, 105-111.

    Article  Google Scholar 

  • Kavaliers, M., Colwell, D. D., Ossenkopp, K.-P., & Perrot-Sinal, T. S. (1997). Altered responses to female odors in parasitized male mice: neuromodulatory mechanisms and relations to female choice. Behav. Ecol. Sociobiol., 40, 373-384.

    Article  Google Scholar 

  • Kavaliers, M., Colwell, D. D., Wah, D. T. O., Bishnoi, I. R., Ossenkopp, K.-P., & Choleris, E. (2019a). Conspecific infection threat rapidly biases the social responses of female mice: involvement of oxytocin. Horm. Behav., 113, 67-75.

    Article  PubMed  Google Scholar 

  • Kavaliers, M., Matta, R., & Choleris, E. (2017). Mate-choice copying, social information processing, and the roles of oxytocin. Neurosci. Biobehav. Rev., 72, 232-242.

    Article  PubMed  Google Scholar 

  • Kavaliers, M., Ossenkopp, K. P., & Choleris, E. (2019b). Social neuroscience of disgust. Genes Brain Behav., 18, e12508.

    Article  PubMed  Google Scholar 

  • Kayyal, H., Yiannakas, A., Chandran, S. K., Khamaisy, M., Sharma, V., & Rosenblum, K. (2019). Activity of insula to basolateral amygdala projecting neurons is necessary and sufficient for taste valence representation. J. Neurosci. 89, 9369-9382.

    Article  Google Scholar 

  • Keiser, C. N., Rudolf, V. H. W., Luksik, M. C., & Saltz, J. B. (2019). Sex differences in disease avoidance behaviour vary across modes of pathogen exposure. Ethology, 126, 304-312.

    Article  Google Scholar 

  • Kiefer, S. W., & Orr, M. R. (1992). Taste avoidance, but not aversion, learning in rats lacking gustatory cortex. Behav. Neurosci. 106, 140-146.

    Article  PubMed  Google Scholar 

  • Klein, S. L., & Flanagan, K. L. (2016). Sex differences in immune response. Nat. Rev. Immunol. 16, 626-638.

    Article  Google Scholar 

  • Koprivnikar, J., & Penalva, I. (2015). Lesser of two evils? Foraging choices in response to threats of predation and parasitism. PLOS One, 19, 0116589.

    Google Scholar 

  • Kwon, J.-K., Ryu, C., Lee, H., Sheffield, A., Fan, J., Cho, D. H., Bigler, S., Sullivan, H. A., Choe, H. K., Wickersham, I. R., Heiman, M., & Choi, G. B. (2021). An amygdala circuit that suppresses social engagement. Nature. Advance online publication. https://doi.org/10.1038/s41586-021-03413-6

  • Limebeer, C. L., Hall, G., & Parker, L. A. (2006). Exposure to a lithium-paired context elicits gaping in rats: a model of anticipatory nausea. Physiol. Behav., 88, 398-403.

    Article  PubMed  Google Scholar 

  • Limebeer, C. L., Krohn, J. P., Cross-Mellor, S. K., Litt, D. E., Ossenkopp, K.-P., & Parker, L. A. (2008). Exposure to a context previously associated with nausea elicits conditioned gaping in rats: A model of anticipatory nausea, Behav. Brain Res. 187, 33-40.

    Article  PubMed  Google Scholar 

  • Limebeer, C. L., Rock, E. M., Sharkey, K. A., & Parker, L. A. (2018). Nausea-induced 5-HT release in the interoceptive insular cortex and regulation by monoacylglycerol lipase (MAGL) inhibition and cannabidiol. eNeuro, 5, 0256-18

    Article  Google Scholar 

  • Lin, S. F., Tsai, Y. F., Tai, M. Y., & Yeh, K. Y. (2015). Estradiol enhances the acquisition of lithium chloride-induced conditioned taste aversion in castrated male rats. Sci. Nat., 102, 5.

    Google Scholar 

  • Lister, K. C., Bouchard, S. M., Markova, T., Aternail, A., Denecli, P., Pimentel, S. D., Majeed, M., Austin, J.-S., Williams, A. C., & Mogil, J. S. (2020). Chronic pain produces hypervigilance to predator odor in mice. Curr. Biol. 15, R866-R867.

    Article  Google Scholar 

  • Lockhart, A. B., Thrall, P. H., & Antonovics, J. (1996). Sexually transmitted diseases in animals; Ecological and evolutionary implications. Biol. Rev., 71, 415-471.

    Article  PubMed  Google Scholar 

  • Lopes, P. C., Block, P., & Konig, B. (2016). Infection-induced behavioural changes reduce connectivity and the potential for disease spread in wild mice contact networks. Sci. Rep., 6, 31790

    Article  PubMed  PubMed Central  Google Scholar 

  • Lymer, J. M., Shepard, P. A. S., Kuun, T., Blackman, A., Jani, N., Mahbub, S., & Choleris E. (2018). Estrogens and their receptors in the medial amygdala rapidly promote social recognition in female mice. Psychoneuroendocrinology, 89, 30-38.

    Article  PubMed  Google Scholar 

  • Marlin, B. J., & Froemke, R. C. (2017). Oxytocin modulation of neural circuits for social behavior. Dev. Neurobiol., 77, 169-182.

    Article  PubMed  Google Scholar 

  • McCabe, C. M., Reader, S. M., & Nunn, C. L. (2015). Infectious disease, behavioral flexibility and the evolution of culture in primates. Proc. R. Soc. B, 282, 20140862.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mitre, M., Marlin, B. J., Schiavo, J. K., Morina, E., Norden, S. E., Hackett, T. A., Aoiki, C. J., Chao, M. V., & Froemke, R. C. (2016). A distributed network for social cognition enriched for oxytocin receptors. J. Neurosci., 36, 2517-2535.

    Article  PubMed  PubMed Central  Google Scholar 

  • Moller, A. P., Dufva, R., & Allander, K. (1993). Parasites and the evolution of host social behavior. Adv. Stud. Behav., 22, 65-102.

    Article  Google Scholar 

  • Newman, S. W. (1999). The medial extended amygdala in male reproductive behavior. A node in the mammalian social behavior network. Ann. N. Y. Acad. Sci., 877, 242-257.

    Google Scholar 

  • Oaten, M. J., Stevenson, R. J., & Case, T. I. (2011). Disease avoidance as a functional basis for stigmatization. Phil. Trans. R. Soc. B, 366, 3433-3452.

    Article  PubMed  PubMed Central  Google Scholar 

  • Oaten, M. J., Stevenson, R. J., & Case, T. I. (2015). The effect of disgust on pain sensitivity. Physiol. Behav., 138, 107-112.

    Article  PubMed  Google Scholar 

  • O’Connell, L. A., & Hofmann, H. A. (2011). The vertebrate mesolimbic reward system and social behavior network: a comparative synthesis. J. Comp. Neurol., 519, 3599-3639.

    Article  PubMed  Google Scholar 

  • Olatunji, B. O., Taylor, A., & Zald, D. (2019). Sex differences in the etiology of disgust sensitivity: A preliminary behavioral genetic analysis. J. Anx. Disord., 65, 41-46.

    Article  Google Scholar 

  • Olsson, M. J., Lundstrom, J. N., Kimball, B. A., Gorden, A. R., Karshikoff, B., Hosseini, N., Sorjonen, K., Hoglund, O., Solares, C., Soop, A., Axellson, J. B., & Lekander, M. (2014). The scent of disease: human body odor contains an early chemosensory cue of sickness. Psychol. Sci., 25, 617-823.

    Article  Google Scholar 

  • Ossenkopp, K.-P., & Eckel, L. A. (1994) Area postrema as a brainstem chemosensor in defense against ingested toxins. Adv. Biosci., 93. 485-490.

    Google Scholar 

  • Ossenkopp, K.-P., & Eckel, L. A. (1995) Toxin-induced changes in taste reactivity responses and the role of the chemosensitive area postrema. Neurosci. Biobehav. Rev. 19, 99-108.

    Article  PubMed  Google Scholar 

  • Ossenkopp, K.-P., Rabi, Y. J., & Eckel, L. A. (1996). Oestradiol-induced taste avoidance is the result of a conditioned palatability shift. NeuroReport, 7, 2777-27.

    Article  PubMed  Google Scholar 

  • Ossenkopp, K.-P., Sutherland, C., & Ladowsky, R. L. (1986). Motor activity changes and conditioned taste aversions induced by administration of scopolamine in rats: Role of the area postrema. Pharmacol. Biochem. Behav. 25, 269-276.

    Article  PubMed  Google Scholar 

  • Paletta, P., Sheppard, P. A. S., Matta, R., Ervin, K. S. J., & Choleris, E. (2019). Rapid effects of estrogens on short term memeory: possible mechanisms. Horm. Behav., 104, 88-99.

    Article  Google Scholar 

  • Panksepp, J. B., & Lahvis, G. P. (2011). Rodent empathy and affective neuroscience. Neurosci. Biobehav. Rev., 35, 1864-1875.

    Article  PubMed  PubMed Central  Google Scholar 

  • Parker, L. A. (2003). Taste avoidance and taste aversion: evidence for two different processes. Anim. Learn. Behav., 31, 165-172.

    Article  Google Scholar 

  • Parker, L. A. (2014). Conditioned flavour avoidance and conditioned gaping: rat models of conditioned nausea. Eur. J. Pharmacol. 722, 122-133.

    Article  PubMed  Google Scholar 

  • Parker, L. A., & Limbeer, C. L. (2006). Conditioned gaping in rats: a selective measure of nausea. Auton. Neurosci. Basic Clin., 129, 36-41.

    Article  Google Scholar 

  • Poirotte, C., & Kappeler, P. M. (2019). Hygenic personalities in wild grey mouse lemurs vary adaptively with sex. Proc. R. Soc. B, 286, 20190863.

    Article  PubMed  PubMed Central  Google Scholar 

  • Poirotte, C., Massol, F., Herbert, A., Willaume, E., Borno, P. M., Kappeler, P. M., & Charpentier, G. (2017). Mandrills use olfaction to socially avoid parasitized conspecifics. Sci. Adv., 3, e160172.

    Article  Google Scholar 

  • Regenbogen, C., Axelsson, J., Lasselin, J., Porada, D. K., Sundelin, T., Peter, M. G., Lekander, M., Lundstrom, J. N., & Olsson, M. J. (2011). Behavioral and neural correlates to multisensory detection of sick humans. Proc. Natl. Acad. Sci. USA, 114, 6499-6405.

    Google Scholar 

  • Rogers-Carter, M. M., & Christianson, J. P. (2019). An insular view of the social decision-making network. Neurosci. Biobehav. Rev., 103, 119-132.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rogers-Carter, M. M., Varela, J. A., Gribbons, K.-B., Pierce, A. F., McGoey, M. T., Ritchey, M., & Christianson, J. B. (2018). Insular cortex mediates approach and avoidance responses to social affective stimuli. Nat. Neurosci., 21, 404-414.

    Article  PubMed  PubMed Central  Google Scholar 

  • Romano, V., MacIntosh, A. J. J., & Sueur, C. (2020). Stemming the flow: information, infection and social evolution. Trends Ecol. Evol., 39, 849-845.

    Article  Google Scholar 

  • Sarabian, C., & MacIntosh, A. J. J. (2015). Hygenic tendencies correlate with low geohelminth infections in free-ranging macaques. Biol. Lett., 11, 20150757

    Article  PubMed  PubMed Central  Google Scholar 

  • Sarabian, C., Ngoubangoye, B,, & MacIntosh, A. J. J. (2017). Avoidance of biological contaminants through sight, smell and touch in chimpanzees. R. Soc. Open Sci., 4, 170968.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sarkar, A., Harty, S., Johnson, K. V.-A., Moeller, A. H., Archie, E.A., Schell, L. D., Carmody, R. N., Clutton-Brock, T. H., Dungar, R. I. M., & Burnet, P. W. J. (2020). Microbial transmission in animal social networks and the social microbiome. Nat Ecol. Evol.,, 4, 1020-1035.

    Article  PubMed  Google Scholar 

  • Schaller, M., & Park, J. H. (2011). The behavioral immune system (and why it matters). Curr. Dir. Psychol. Sci., 20, 99-103.

    Article  Google Scholar 

  • Schier, L. A., & Spector, A. C. (2019). The functional and neurobiological properties of bad taste. Physiol. Rev., 99, 605-663.

    Article  PubMed  Google Scholar 

  • Shamay-Tsoory, S. G., & Abu-Akel, A. (2016). The social salience hypothesis of oxytocin. Biol. Psych., 79, 194-202.

    Article  Google Scholar 

  • Smith, C., & Bilbo, S. D. (2021). Sickness and the social brain: Love in the time of COVID. Front. Psycht., 12, 633664.

    Article  Google Scholar 

  • Spector, A. C., Breslin, P., & Grill, H. J., (1988). Taste reactivity as a dependent measure of the rapid formation of a conditioned taste aversion: A tool for the analysis of taste-visceral associations. Behav. Neurosci., 102, 942-952.

    Article  PubMed  Google Scholar 

  • Steinman, M. Q., Duque-Wilckens, N., & Trainor, B. C. (2019). Complementary neural circuits for divergent effects of oxytocin: social approach versus social anxiety. Biol. Psych., 85, 792-801.

    Article  Google Scholar 

  • Stephenson, J. F., Perkins, S. E., & Cable, J. (2018). Transmission risk predicts avoidance of infected conspecifics in Trinidadian guppies. J. Anim. Ecol., 87, 1525-1533.

    Article  PubMed  Google Scholar 

  • Stevenson, R. J., Case, T. I., Oaten, M. J., Stafford, L., & Saluja, S. (2019). A proximal perspective on disgust. Emot. Rev., 11, 209-225.

    Article  Google Scholar 

  • Stockmaier, S., Bolnick, D. L., Page, R. A., & Carter, G. G. (2020). Sickness effects depend on the type of behaviour and relationship. J. Anim. Ecol., 6, 1387-1394.

    Article  Google Scholar 

  • Stockmaier, S., Stroeymeyt, N., Shattuck, E. C., Hawley, D. M., Meyers, L.A., & Bolnick, D. I. (2021) Infectious diseases and social distancing in nature. Science, 371, eabc8881.

    Google Scholar 

  • Stowers, L., & Tsuang-Han, K. (2015). Mammalian pheromones: emerging properties and mechanisms of detection. Curr. Op. Neurobiol., 34, 103-109.

    Article  PubMed  Google Scholar 

  • Tenk, C. M., Kavaliers, M., & Ossenkopp, K.-P. (2005). Dose response effects of lithium chloride on conditioned place aversions and locomotor activity. Eur. J. Pharmacol., 515, 117-127.

    Article  PubMed  Google Scholar 

  • Theodoridou, A., Penton-Voak, I. S., & Rowe, A. C. (2013). A direct examination of the effect of intranasal administration of oxytocin on approach-avoidance motor responses to emotional stimuli. PLOS One, 8, e58113.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tuerke, K. J., Limebeer, C. L., Fletcher, P. J., & Parker, L. A. (2012). Double dissociation between the regulation of conditioned disgust and taste avoidance by serotonin availability at the 5-HT3 receptor in the posterior and anterior insular cortex. J. Neurosci., 32, 13709-13717.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wicker, B., Keysers, C., Plailly, J., Royet, J. P., Gallese, V., & Rizzolatti, G. (2003). Both of us disgusted in my insula: the common neural basis of seeing and feeling disgust. Neuron, 40, 655-664.

    Article  PubMed  Google Scholar 

  • Williams, A. V., Duque-Wilckens, N., Ramos-Maciel, S., Campi, K.L., Bhela, S., Xu, K., Jackson, K., Chini, B., Pesavento, P. A., & Trainor, B. V. (2020). Social approach and social vigilance are differentially regulated by oxytocin receptors in the nucleus accumbens. Neuropsychopharmacology, 45, 1423-1430.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The studies described here were supported by Natural Sciences and Engineering Research Council of Canada (NSERC) discovery grants to E.C. and. M.K and K-P.O.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Martin Kavaliers .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2021 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Kavaliers, M., Ossenkopp, KP., Choleris, E. (2021). Pathogen and Toxin Disgust in Rodents. In: Powell, P.A., Consedine, N.S. (eds) The Handbook of Disgust Research. Springer, Cham. https://doi.org/10.1007/978-3-030-84486-8_4

Download citation

Publish with us

Policies and ethics