Retrieval of conditioned immune response in male mice is mediated by an anterior–posterior insula circuit

Willyard, C. How gut microbes could drive brain disorders. Nature 590, 22–25 (2021).

Article  PubMed  CAS  Google Scholar 

Mohajeri, M. H. et al. The role of the microbiome for human health: from basic science to clinical applications. Eur. J. Nutr. 57, 1–14 (2018).

Article  PubMed  PubMed Central  Google Scholar 

Osterhout, J. A. et al. A preoptic neuronal population controls fever and appetite during sickness. Nature 606, 937–944 (2022).

Article  PubMed  PubMed Central  CAS  Google Scholar 

Pavlov, I. Conditioned Reflexes: An Investigation of the Physiological Activity of the Cerebral Cortex (Oxford University Press, 1927).

Schedlowski, M. & Pacheco-López, G. The learned immune response: Pavlov and beyond. Brain Behav. Immun. 24, 176–185 (2010).

Article  PubMed  Google Scholar 

Cohen, N., Moynihan, J. A. & Ader, R. Pavlovian conditioning of the immune system. Int. Arch. Allergy Immunol. 105, 101–106 (1994).

Article  PubMed  CAS  Google Scholar 

Janz, L. J. et al. Pavlovian conditioning of LPS-induced responses: effects on corticosterone, splenic NE, and IL-2 production. Physiol. Behav. 59, 1103–1109 (1996).

Article  PubMed  CAS  Google Scholar 

Oberbeck, R., Kromm, A., Exton, M. S., Schade, U. & Schedlowski, M. Pavlovian conditioning of endotoxin-tolerance in rats. Brain Behav. Immun. 17, 20–27 (2003).

Article  PubMed  CAS  Google Scholar 

Ader, R. & Cohen, N. Behaviorally conditioned immunosuppression. Psychosom. Med. 37, 333–340 (1975).

Article  PubMed  CAS  Google Scholar 

Hadamitzky, M., Lückemann, L., Pacheco-López, G. & Schedlowski, M. Pavlovian conditioning of immunological and neuroendocrine functions. Physiol. Rev. 100, 357–405 (2020).

Article  PubMed  CAS  Google Scholar 

Pacheco-López, G. & Bermúdez-Rattoni, F. Brain–immune interactions and the neural basis of disease-avoidant ingestive behaviour. Philos. Trans. R. Soc. Lond. B Biol. Sci. 366, 3389–3405 (2011).

Article  PubMed  PubMed Central  Google Scholar 

Barnéoud, P., Neveu, P. J., Vitiello, S., Mormède, P. & Le Moal, M. Brain neocortex immunomodulation in rats. Brain Res. 474, 394–398 (1988).

Article  PubMed  Google Scholar 

Dantzer, R. Neuroimmune interactions: from the brain to the immune system and vice versa. Physiol. Rev. 98, 477–504 (2018).

Article  PubMed  CAS  Google Scholar 

Sergeeva, M., Rech, J., Schett, G. & Hess, A. Response to peripheral immune stimulation within the brain: magnetic resonance imaging perspective of treatment success. Arthritis Res. Ther. 17, 268 (2015).

Article  PubMed  PubMed Central  Google Scholar 

Gehrlach, D. A. et al. A whole-brain connectivity map of mouse insular cortex. eLife 9, e55585 (2020).

Article  PubMed  PubMed Central  CAS  Google Scholar 

Yiannakas, A. et al. Parvalbumin interneuron inhibition onto anterior insula neurons projecting to the basolateral amygdala drives aversive taste memory retrieval. Curr. Biol. 31, 2770–2784 (2021).

Article  PubMed  CAS  Google Scholar 

Koren, T. et al. Insular cortex neurons encode and retrieve specific immune responses. Cell 184, 5902–5915 (2021).

Levitan, D. et al. Single and population coding of taste in the gustatory cortex of awake mice. J. Neurophysiol. 122, 1342–1356 (2019).

Article  PubMed  PubMed Central  CAS  Google Scholar 

Bergeron, D., Obaid, S., Fournier-Gosselin, M. P., Bouthillier, A. & Nguyen, D. K. Deep brain stimulation of the posterior insula in chronic pain: a theoretical framework. Brain Sci. 11, 639 (2021).

Article  PubMed  PubMed Central  Google Scholar 

Chen, K., Kogan, J. F. & Fontanini, A. Spatially distributed representation of taste quality in the gustatory insular cortex of behaving mice. Curr. Biol. 31, 247–256 (2021).

Article  PubMed  Google Scholar 

Pritchard, T. C., Macaluso, D. A. & Eslinger, P. J. Taste perception in patients with insular cortex lesions. Behav. Neurosci. 113, 663–671 (1999).

Article  PubMed  CAS  Google Scholar 

Exton, M. S., Bull, D. F., King, M. G. & Husband, A. J. Behavioral conditioning of endotoxin-induced plasma iron alterations. Pharmacol. Biochem. Behav. 50, 675–679 (1995).

Article  PubMed  CAS  Google Scholar 

Raduolovic, K., Mak’Anyengo, R., Kaya, B., Steinert, A. & Niess, J. H. Injections of lipopolysaccharide into mice to mimic entrance of microbial-derived products after intestinal barrier breach. J. Vis. Exp. 2018, 57610 (2018).

Tateda, K., Matsumoto, T., Miyazaki, S. & Yamaguchi, K. Lipopolysaccharide-induced lethality and cytokine production in aged mice. Infect. Immun. 64, 769–774 (1996).

Article  PubMed  PubMed Central  CAS  Google Scholar 

Sun, W. et al. Ilexgenin A, a novel pentacyclic triterpenoid extracted from Aquifoliaceae shows reduction of LPS-induced peritonitis in mice. Eur. J. Pharmacol. 797, 94–105 (2017).

Article  PubMed  CAS  Google Scholar 

Víctor, V. M. & de la Fuente, M. Comparative study of peritoneal macrophage functions in mice receiving lethal and non-lethal doses of LPS. J. Endotoxin Res. 6, 235–241 (2000).

Article  PubMed  Google Scholar 

Auger, M. J. & Ross, J. A. in The Macrophage (eds Lewis, C. E., & McGee, J.O.D.) 1–74 (Oxford University Press, 1993).

Bosurgi, L. et al. Macrophage function in tissue repair and remodeling requires IL-4 or IL-13 with apoptotic cells. Science 356, 1072–1076 (2017).

Ginhoux, F. & Jung, S. Monocytes and macrophages: developmental pathways and tissue homeostasis. Nat. Rev. Immunol. 14, 392–404 (2014).

Article  PubMed  CAS  Google Scholar 

Meng, F. & Lowell, C. A. Lipopolysaccharide (LPS)-induced macrophage activation and signal transduction in the absence of Src-family kinases Hck, Fgr, and Lyn. J. Exp. Med. 185, 1661–1670 (1997).

Article  PubMed  PubMed Central  CAS  Google Scholar 

Liao, C. T. et al. Peritoneal macrophage heterogeneity is associated with different peritoneal dialysis outcomes. Kidney Int. 91, 1088–1103 (2017).

Article  PubMed  PubMed Central  CAS  Google Scholar 

Soskic, B., Qureshi, O. S., Hou, T. & Sansom, D. M. A transendocytosis perspective on the CD28/CTLA-4 pathway. Adv. Immunol. 124, 95–136 (2014).

Subauste, C. S., de Waal Malefyt, R. & Fuh, F. Role of CD80 (B7.1) and CD86 (B7.2) in the immune response to an intracellular pathogen. J. Immunol. 160, 1831–1840 (1998).

Article  PubMed  CAS  Google Scholar 

Akdis, M. et al. Interleukins, from 1 to 37, and interferon-γ: receptors, functions, and roles in diseases. J. Allergy Clin. Immunol. 127, 701–721 (2011).

Article  PubMed  CAS  Google Scholar 

Ramírez-Amaya, V. et al. Insular cortex lesions impair the acquisition of conditioned immunosuppression. Brain Behav. Immun. 10, 103–114 (1996).

Article  PubMed  Google Scholar 

Kayyal, H. et al. Insula to mPFC reciprocal connectivity differentially underlies novel taste neophobic response and learning in mice. eLife 10, e66686 (2021).

Article  PubMed  PubMed Central  CAS  Google Scholar 

Kayyal, H. et al. Activity of insula to basolateral amygdala projecting neurons is necessary and sufficient for taste valence representation. J. Neurosci. 39, 9369–9382 (2019).

Comments (0)

No login
gif