Reflex control of immunity
Open accessAbstract
Inflammation can cause damage and even death. What controls this primitive and potentially lethal innate immune response to injury and infection? Molecular and neurophysiological studies during the past decade have revealed a pivotal answer: immunity is coordinated by neural circuits that operate reflexively. The afferent arc of the reflex consists of nerves that sense injury and infection. This activates efferent neural circuits, including the cholinergic anti-inflammatory pathway, that modulate immune responses and the progression of inflammatory diseases. It might be possible to develop therapeutics that target neural networks for the treatment of inflammatory disorders.
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Activation of the parasympathetic nervous system can modulate the activity of the immune system via alterations in vagal release of acetylcholine from T cells.
“Interestingly, evidence suggests that activation of the parasympathetic nervous system also can modulate the activity of the immune system via alterations in vagal release of acetylcholine from T cells (Tracey, 2009).”
From Inflammation in Fear- and Anxiety-Based Disorders: PTSD, GAD, and Beyond (2017) · cites this paper as Tracey, 2009
The ‘Anatomy of the cholinergic anti-inflammatory pathway’ section says the pathway is functionally neither parasympathetic nor sympathetic, contrary to the claim’s classification. It also describes a hypothesis in which vagus nerve signals prompt splenic nerve endings to release noradrenaline near T cells that produce acetylcholine—not vagal release of acetylcholine from T cells. The paper does support vagal modulation of immune activity, but not the mechanism stated here. (LLM, conf=0.86)
Checked by a reasoning model — may be wrong.
Experimental — accuracy not yet measuredThe parasympathetic nervous system modulates immune responses at a regional level through efferent and afferent fibers of the vagus nerve, enabling it to prevent excessive inflammation.
“Additional evidence suggests that the parasympathetic nervous system modulates immune responses at a regional level through both the efferent and afferent fibers of the vagus nerve, enabling it to prevent excessive inflammation”
From From stress to inflammation and major depressive disorder: A social signal transduction theory of depression. (2014) · cites this paper as Tracey, 2009
The afferent-arc and efferent-arc sections describe vagal signals sensing inflammation and suppressing cytokine production in innervated tissues, supporting the reflex and its prevention of excessive inflammation. But the anatomy section explicitly says the cholinergic anti-inflammatory pathway is functionally neither parasympathetic nor sympathetic, so attributing this control specifically to the parasympathetic nervous system overstates the source. (LLM, conf=0.90)
Experimental — accuracy not yet measuredMotor vagus nerve stimulation attenuates the activation of NFκB following an immune challenge.
“For example, motor vagus nerve stimulation attenuates the activation of NFκB following an immune challenge (Tracey, 2009).”
From Inflammation in Fear- and Anxiety-Based Disorders: PTSD, GAD, and Beyond (2017) · cites this paper as Tracey, 2009
ACh binds to α-7-nicotinic ACh receptors of macrophages to inhibit TNF-α.
“ACh binds to α-7-nicotinic ACh receptors of those macrophages to inhibit the TNF-α (69).”
From Vagus Nerve as Modulator of the Brain–Gut Axis in Psychiatric and Inflammatory Disorders (2018) · cites this paper as [69]
Vagal activity can modulate immune responses regionally through efferent and afferent fibers to prevent excessive inflammation.
“with evidence that vagal activity can modulate immune responses at a regional level through both the efferent and afferent fibers of the vagus nerve, to prevent excessive inflammation”
From Sleep health: Reciprocal regulation of sleep and innate immunity (2017) · cites this paper as Tracey, 2009
Multiple non-exclusive pathways activate the HPA axis upon cerebral or peripheral immune challenges, including local inflammatory mediators, circulating factors accessing the PVN via circumventricular organs or a disrupted blood-brain barrier, endothelial signaling, and vagus nerve afferents.
“Multiple non-exclusive pathways participate in the activation of the HPA axis upon cerebral or peripheral immune challenges. When an immunogenic insult takes place in the brain, various inflammatory mediators produced locally may trigger the HPA axis.”
From The HPA – Immune Axis and the Immunomodulatory Actions of Glucocorticoids in the Brain (2014) · cites this paper as [21]
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The protective effect of the vagus nerve in a murine model of chronic relapsing colitis
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“This complex associates with myeloid differentiation primary response protein 88 (MYD88; a cytoplasmic Toll–IL-1R (TIR) domain-containing adaptor protein) and recruits signalling proteins that activate mitogen-activated protein kinases (MAPKs) and nuclear factor-κB ( NF-κB”
BackgroundVagus nerve integrity and experimental colitis
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Vagus nerve stimulation therapy in depression and epilepsy: therapeutic parameter settings
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“Vagus nerve stimulators are currently in clinical use and have been safely implanted in tens of thousands of patients as a treatment for seizure disorders that are refractory to medicatio”
BackgroundCardiac Autonomic Changes Associated With Fish Oil vs Soy Oil Supplementation in the Elderly
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“By contrast, activation of 5-hydroxytryptamine receptors or β-adrenergic receptors inhibits pro-inflammatory cytokine release and suppresses inflammatio”
BackgroundFunctional significance of coactivation of vagal and sympathetic cardiac nerves.
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“This occurs because parasympathetic stimulation slows the heart rate, which improves the efficiency by which the heart is filled with bloo”
BackgroundAcetylcholine and the sympathetic innervation of the spleen
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BackgroundTHE CHOLINERGIC COMPONENT IN THE SYMPATHETIC INNERVATION TO THE SPLEEN
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“These neurotransmitters cause depolarization of nearby sensory fibres travelling in the vagus nerve, which propagate to the brain stem, where a motor arc is activated to mediate compensatory responses to increase oxygen deliver”
BackgroundHeart Rate Variability in Patients with Systemic Sarcoidosis
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“How can there be a requirement for α7nAChR-dependent signalling to control cytokine production in the spleen if the splenic neurons release catecholamines , not acetylcholine? It has been known for decades that the spleen is a rich source of acetylcholine (indeed, this molecule was originally identified in spleen tiss…”
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Slavich, G. M., & Irwin, M. R. (2014) · Psychological Bulletin · doi:10.1037/a0035302 · Cited by 2,206 · see citing works
Air pollution: mechanisms of neuroinflammation and CNS disease
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The interplay between the intestinal microbiota and the brain
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HMGB1 is a therapeutic target for sterile inflammation and infection
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Visceral influences on brain and behavior
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“CNS sensing of inflammation, particularly within NTS, also plays a critical role in regulating the magnitude of innate immune response to infection, injury or ischemia (Tracey, 2009).”
Vagus Nerve as Modulator of the Brain–Gut Axis in Psychiatric and Inflammatory Disorders
Breit, S., Kupferberg, A., Rogler, G., & Hasler, G. (2018) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2018.00044 · Cited by 1,189 · see citing works
“As stated earlier, ACh released at the distal end of VN efferents decreases the production of proinflammatory cytokines, such as TNF-α (188).”
BackgroundInfluentialNeuroinflammation and depression: A review
Troubat, R., Barone, P., Leman, S., Desmidt, T., Cressant, A., Atanasova, B., Brizard, B., El Hage, W., Surget, A., Belzung, C., et al. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.14720 · Cited by 1,107 · see citing works
“Peripheral, circulating inflammatory mediators also affect HPA axis activity, reaching the hypothalamus directly through the endothelium of the circumventricular organs or an altered BBB (Bellavance & Rivest, 2014) or indirectly through afferent fibres from the vagus nerve conveying information about peripheral inflam…”
BackgroundThe vagus nerve and the inflammatory reflex – linking immunity and metabolism
Pavlov, V. A., & Tracey, K. J. (2012) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2012.189 · Cited by 1,040 · see citing works
Self-citationDopamine controls systemic inflammation through inhibition of NLRP3 inflammasome
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“Increasing evidence has shown that the immune system can be influenced by the nervous system and neurotransmitters (Olofsson et al., 2012; Tracey, 2009).”
Haroon, E., Raison, C. L., & Miller, A. H. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2011.205 · Cited by 1,000 · see citing works
“For example, treatment of mouse midbrain and striatal synaptosomes with IL-1b and TNF-a was shown to lead to a dose- and time-dependent increase in serotonin reuptake, which was reversed by the p38 antagonist, SB203580 (Zhu et al, 2006).”
BackgroundInfluentialThe immune system’s role in sepsis progression, resolution, and long-term outcome
Delano, M. J., & Ward, P. A. (2016) · Immunological Reviews · doi:10.1111/imr.12499 · Cited by 880 · see citing works
Inflammation in Fear- and Anxiety-Based Disorders: PTSD, GAD, and Beyond
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“Interestingly, evidence suggests that activation of the parasympathetic nervous system also can modulate the activity of the immune system via alterations in vagal release of acetylcholine from T cells (Tracey, 2009).”
BackgroundMicroglia and neurodegeneration: The role of systemic inflammation
Cunningham, C. (2013) · Glia · doi:10.1002/glia.22350 · Cited by 769 · see citing works
Neuropathogenesis of Delirium: Review of Current Etiologic Theories and Common Pathways
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The Adverse Effects of Air Pollution on the Nervous System
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“In addition, circulating cytokines that are released by inflamed peripheral organs or endothelial cells could stimulate peripheral innate immune cells, activate peripheral neuronal afferents, or enter the brain by diffusion and active transport thereby worsening the condition synergistically [27, 28].”
BackgroundStress, Inflammation, and Defense of Homeostasis
Chovatiya, R., & Medzhitov, R. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.03.030 · Cited by 704 · see citing works
“…nociceptors may monitor and control tissue homeostasis not only at the extremes of infection and injury, but also duringmore common and less dramatic alterations of normal tissue states (Ahern, 2013; Basbaum et al., 2009;Mosser and Edwards, 2008; Nguyen et al., 2011; Pollard, 2009; Tracey, 2009).”
BackgroundSepsis: Current Dogma and New Perspectives
Deutschman, C. S., & Tracey, K. J. (2014) · Immunity · doi:10.1016/j.immuni.2014.04.001 · Cited by 676 · see citing works
“The inflammatory reflex is a prototypical, major efferent neural pathway that modulates TNF release in response to LPS (Figure 2) (Tracey, 2002, 2009; Borovikova et al., 2000).”
BackgroundSelf-citationPrisco, G. D., Cavaliere, V., Annoscia, D., Varricchio, P., Caprio, E., Nazzi, F., Gargiulo, G., & Pennacchio, F. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1314923110 · Cited by 674 · see citing works
“The inflammatory reflex circuit described in mammals is essential to ensure a neural coordination of the defense response to have a sufficient protection while preventing damages deriving from an overzealous reaction (44, 45).”
BackgroundNeuro-immune Interactions Drive Tissue Programming in Intestinal Macrophages
Gabanyi, I., Muller, P. A., Feighery, L. M., Oliveira, T. Y., Costa‐Pinto, F. A., & Mucida, D. (2016) · Cell · doi:10.1016/j.cell.2015.12.023 · Cited by 658 · see citing works
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Sleep health: Reciprocal regulation of sleep and innate immunity
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“In relation to inflammation, the parasympathetic nervous system is also involved, with evidence that vagal activity can modulate immune responses at a regional level through both the efferent and afferent fibers of the vagus nerve, to prevent excessive inflammation (Sternberg, 2006; Tracey, 2009).”
BackgroundNeuroimmune mechanisms of depression
Hodes, G. E., Kana, V., Menard, C., Merad, M., & Russo, S. J. (2015) · Nature Neuroscience · doi:10.1038/nn.4113 · Cited by 585 · see citing works
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Resolving postoperative neuroinflammation and cognitive decline
Terrando, N., Eriksson, L. I., Ryu, J. K., Yang, T., Monaco, C. G., Feldmann, M., Fagerlund, M. J., Charo, I. F., Akassoglou, K., & Maze, M. (2011) · Annals of Neurology · doi:10.1002/ana.22664 · Cited by 582 · see citing works
“Stimulation of the cholinergic anti-inflammatory pathway via activation of the a7 nAChR subtype is a pivotal regulator of NF-jB activity.(21,22) We tested whether pharmacologic activation of this receptor could prevent surgery-induced neuroinflammation.”
BackgroundAre bee diseases linked to pesticides? — A brief review
Sánchez‐Bayo, F., Goulson, D., Pennacchio, F., Nazzi, F., Goka, K., & Desneux, N. (2016) · Environment International · doi:10.1016/j.envint.2016.01.009 · Cited by 488 · see citing works
“on immunity (Di Prisco et al., 2013; Tracey, 2009; Tracey, 2011), one could expect a general undermining of the body defences in other”
BackgroundThe Meningeal Lymphatic System: A New Player in Neurophysiology
Da Mesquita, S., Fu, Z., & Kipnis, J. (2018) · Neuron · doi:10.1016/j.neuron.2018.09.022 · Cited by 479 · see citing works
Biology and Genetics of Prions Causing Neurodegeneration
Prusiner, S. B. (2013) · Annual Review of Genetics · doi:10.1146/annurev-genet-110711-155524 · Cited by 455 · see citing works
The neurobiology of interoception in health and disease
Quadt, L., Critchley, H., & Garfinkel, S. N. (2018) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.13915 · Cited by 447 · see citing works
Neural circuits of interoception
Berntson, G. G., & Khalsa, S. S. (2021) · Trends in Neurosciences · doi:10.1016/j.tins.2020.09.011 · Cited by 419 · see citing works
“Future research should be addressed at (i) further elaborating the multisynaptic pathways and circuits connecting the CNS with the internal organs of the body, (ii) clarifying the ascending interoceptive pathways linking the NTS and spinal afferents with higher order regions of the CNS, (iii) understanding how interac…”
BackgroundInfluentialMatteoli, G., Gomez-Pinilla, P. J., Némethová, A., Giovangiulio, M. D., Cailotto, C., van Bree, S. V., Michel, K., Tracey, K., Schemann, M., Boesmans, W., et al. (2013) · Gut · doi:10.1136/gutjnl-2013-304676 · Cited by 412 · see citing works
Self-citationFunctional Innervation of Hepatic iNKT Cells Is Immunosuppressive Following Stroke
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The HPA – Immune Axis and the Immunomodulatory Actions of Glucocorticoids in the Brain
Bellavance, M.-A., & Rivest, S. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00136 · Cited by 419 · see citing works
“Finally, afferent fibers of the vagus nerve may also signal peripheral inflammation to the brain and thereby activate the HPA response (20, 21).”
BackgroundSignalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis
Rusch, J. A., Layden, B. T., & Dugas, L. R. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1130689 · Cited by 415 · see citing works
Rheumatoid arthritis and depression: an inflammatory perspective
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Biological mechanisms underlying the role of physical fitness in health and resilience
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“The most important mechanisms relate to modulation of the body’s main stress responsive systems—the HPA axis, the autonomic nervous system and immune system—and interactions among these systems [36–40].”
BackgroundRethinking inflammation: neural circuits in the regulation of immunity
Olofsson, P. S., Rosas‐Ballina, M., Levine, Y. A., & Tracey, K. J. (2012) · Immunological Reviews · doi:10.1111/j.1600-065x.2012.01138.x · Cited by 393 · see citing works
“A prototypical neural reflex circuit of this kind is the ‘inflammatory reflex’ which includes a sensory arm in the afferent vagus and a motor arm in the efferent vagus nerve (3) (Fig.”
BackgroundSelf-citationMind–body therapies and control of inflammatory biology: A descriptive review
Bower, J. E., & Irwin, M. R. (2016) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2015.06.012 · Cited by 388 · see citing works
“Increases in parasympathetic nervous system activity may also reduce inflammation via the anti-inflammatory cholinergic pathway (Tracey, 2009).”
BackgroundA genetically encoded fluorescent acetylcholine indicator for in vitro and in vivo studies
Jing, M., Zhang, P., Wang, G., Feng, J., Mesik, L., Zeng, J., Jiang, H., Wang, S., Looby, J. C., Guagliardo, N. A., et al. (2018) · Nature Biotechnology · doi:10.1038/nbt.4184 · Cited by 378 · see citing works
Autonomic Nervous System and Immune System Interactions
Kenney, M., & Ganta, C. K. (2014) · Comprehensive physiology · doi:10.1002/cphy.c130051 · Cited by 383 · see citing works
Vagus Nerve and Vagus Nerve Stimulation, a Comprehensive Review: Part III
Yuan, H., & Silberstein, S. D. (2015) · Headache The Journal of Head and Face Pain · doi:10.1111/head.12649 · Cited by 381 · see citing works
“VN senses inflammation and dampens the inflammatory response by influencing the hypothalamicpituitary-adrenal axis and modulating the autonomic system that controls key immune organs, such as the spleen, adrenal glands, and possibly bone marrow.(27,28) The spleen is the central organ in the inflammatory reflex and the…”
BackgroundInfluentialZannad, F. M., Ferrari, G. M. D., Tuinenburg, A. E., Wright, D. J., Brugada, J., Butter, C., Klein, H., Stolen, C., Meyer, S., Steín, K. M., et al. (2014) · European Heart Journal · doi:10.1093/eurheartj/ehu345 · Cited by 380 · see citing works
Depression in cancer: The many biobehavioral pathways driving tumor progression
Bortolato, B., Hyphantis, T. N., Valpione, S., Perini, G., Maes, M. H. J., Morris, G., Kubera, M., Köhler, C. A., Fernandes, B. S., Stubbs, B., et al. (2016) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2016.11.004 · Cited by 378 · see citing works
“kappa B (NF-jB), an effect referred to as the ‘‘cholinergic antiinflammatory pathway” [36].”
BackgroundStressful early life experiences and immune dysregulation across the lifespan
Fagundes, C. P., Glaser, R., & Kiecolt-Glaser, J. K. (2013) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2012.06.014 · Cited by 371 · see citing works
“On the other hand, higher parasympathetic activity results in lower levels of inflammation via the cholinergic anti-inflammatory pathway that facilitates acetylcholine release (Tracey, 2009).”
BackgroundDiabetic cardiac autonomic neuropathy, inflammation and cardiovascular disease
Vinik, A. I., Erbas, T. A., & CASELLINI, C. M. (2013) · Journal of Diabetes Investigation · doi:10.1111/jdi.12042 · Cited by 376 · see citing works
Targeting Tumor Necrosis Factor Alpha for Alzheimer’s Disease
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“Peripheral inflammation is also translated to the brain through the vagus nerve by neural reflex (Tracey, 2009).”
BackgroundOverview and introduction: The blood–brain barrier in health and disease
Abbott, N. J., & Friedman, A. (2012) · Epilepsia · doi:10.1111/j.1528-1167.2012.03696.x · Cited by 362 · see citing works
“Evidence suggests tight direct interactions between the cholinergic and immune systems in both the peripheral and the central nervous systems (Tracey, 2009; Gnatek et al., 2012).”
BackgroundA Path Toward Precision Medicine for Neuroinflammatory Mechanisms in Alzheimer's Disease
Hampel, H., Caraci, F., Cuello, A. C., Caruso, G., Nisticò, R., Corbo, M., Baldacci, F., Toschi, N., Garaci, F., Chiesa, P. A., et al. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00456 · Cited by 360 · see citing works
Targeting HMGB1 in inflammation
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Self-citationExercise, inflammation and aging.
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Septic-Associated Encephalopathy: a Comprehensive Review
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“Four broad functions are controlled by the brainstem: brainstem reflexes, sleep–wake cycle, control of vital functions, and modulation of the immune response [88].”
BackgroundCurrent Directions in the Auricular Vagus Nerve Stimulation I – A Physiological Perspective
Kaniušas, E., Kampusch, S., Tittgemeyer, M., Panetsos, F., Gines, R. F., Papa, M., Kiss, A., Podesser, B. K., Cassara, A. M., Tanghe, E., et al. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00854 · Cited by 331 · see citing works
“In particular, VNS was shown to rebalance the working point of autonomic regulation of the immune system into a protective range avoiding pro-inflammatory responses and, on the other hand, avoiding immunosuppression (Tracey, 2009).”
BackgroundPathophysiological and cognitive mechanisms of fatigue in multiple sclerosis
Manjaly, Z., Harrison, N. A., Critchley, H., Tri, C., Stefanics, G., Wenderoth, N., Lutterotti, A., Müller, A. E., & Stephan, K. E. (2019) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp-2018-320050 · Cited by 324 · see citing works
“84 Additionally, several indirect pathways exist how peripheral inflammation can affect the CNS.”
BackgroundSchedlowski, M., Enck, P., Rief, W., & Bingel, U. (2015) · Pharmacological Reviews · doi:10.1124/pr.114.009423 · Cited by 323 · see citing works
“…there are few studies reporting these effects in humans, and those that do mainly employed insulin as a US measuring blood glucose or insulin levels as a conditioned response (Fehm-Wolfsdorf et al., 1993; Stockhorst et al., 1999, 2004, 2011; Klosterhalfen et al., 2000; reviewed in Wendt et al.,…”
BackgroundTrauma of major surgery: A global problem that is not going away
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Anti-inflammatory effect of vagus nerve stimulation in a rat model of inflammatory bowel disease
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“Tracey's group reported an anti-inflammatory role of vagal efferents through the cholinergic anti-inflammatory pathway: acetylcholine (Ach) released at the distal end of the vagus nerve, interacts with α-7 nicotinic Ach receptor (α7nAChR) of human macrophages to inhibit the release of proinflammatory cytokines such as…”
BackgroundPsychosocial stress in pregnancy and preterm birth: associations and mechanisms
Shapiro, G. D., Fraser, W., Frasch, M. G., & Séguin, J. (2013) · Journal of Perinatal Medicine · doi:10.1515/jpm-2012-0295 · Cited by 278 · see citing works
“Evidence in support of this pathway comes from suppression of inflammation (decreased production of proinflammatory cytokines with no change in production of anti-inflammatory cytokines) in response to stimulation of the vagus nerve in adult animal models [88].”
BackgroundYang, I. H., Corwin, E. J., Brennan, P. A., Jordan, S., Murphy, J. R., & Dunlop, A. L. (2015) · Nursing Research · doi:10.1097/nnr.0000000000000133 · Cited by 283 · see citing works
“All rights reserved. reducing the production of proinflammatory cytokines, including tumor necrosis factor-alpha (Pavlov, Wang, Czura, Friedman, & Tracey, 2003; Tracey, 2009; Vijayaraghavan et al., 2013).”
BackgroundSepsis-associated encephalopathy: A vicious cycle of immunosuppression
Ren, C., Yao, R.-Q., Zhang, H., Feng, Y.-W., & Yao, Y.-M. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-1701-3 · Cited by 259 · see citing works
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Inflammatory mediators in human epilepsy: A systematic review and meta-analysis
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Inflammatory Response in Dry Eye
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Self-citationα7-Cholinergic Receptor Mediates Vagal Induction of Splenic Norepinephrine
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Inhibitors of Acetylcholinesterase and Butyrylcholinesterase Meet Immunity
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“CNS is involved in the regulation of innate immunity [15–24].”
BackgroundPro-cognitive properties of T cells
Kipnis, J., Gadani, S., & Derecki, N. C. (2012) · Nature Reviews Immunology · doi:10.1038/nri3280 · Cited by 246 · see citing works
Peripheral gating of pain signals by endogenous lipid mediators
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Neuroimmune cardiovascular interfaces control atherosclerosis
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The self in context: brain systems linking mental and physical health
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The Pathophysiology of Sepsis-Associated AKI
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“Fourth, brain stem derived innervation of the vagus nerve, which also attributes to immune modulatory effects (Tracey, 2009), remains unaffected.”
BackgroundFood for thought: The role of nutrition in the microbiota-gut–brain axis
Oriach, C. S., Robertson, R. C., Stanton, C., Cryan, J. F., & Dinan, T. G. (2016) · Clinical Nutrition Experimental · doi:10.1016/j.yclnex.2016.01.003 · Cited by 227 · see citing works
“Through this complex network the gut can influence the brain via visceral messages, and conversely, the brain is able to influence gastrointestinal functions (like motility, secretion and mucin production) and immune functions, such as the modulation of cytokine production by cells of the mucosal immune system [40].”
The Neurology of the Immune System: Neural Reflexes Regulate Immunity
Rosas‐Ballina, M., & Tracey, K. J. (2009) · Neuron · doi:10.1016/j.neuron.2009.09.039 · Cited by 226 · see citing works
“The answer stems from studies addressing the role of neural networks, which revealed that signals originating in the brain, and conveyed as action potentials transmitted in the vagus nerve, regulate cytokine production by the innate immune system (Tracey, 2009).”
BackgroundSelf-citationImpact of ICU-acquired weakness on post-ICU physical functioning: a follow-up study
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“Alternatively, an increased risk of developing infections may be the result of immune dysfunction secondary to autonomic dysfunction that may accompany ICU-AW [28,29].”
Neuroimmune crosstalk in the central nervous system and its significance for neurological diseases
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“Membrane proteins TLRs, RAGE, LFA-1, MAC-1, CRs, FcRβ [16-19,21,25,45-47] CD45, CD91, CD200R, CD172a [18,48]; CX3CR1 [49]; TREM-2 [50]; FasL, Fas [38,39]”
BackgroundInfluentialAutonomic regulation of cellular immune function
Bellinger, D. L., & Lorton, D. (2014) · Autonomic Neuroscience · doi:10.1016/j.autneu.2014.01.006 · Cited by 217 · see citing works
Noninvasive sub-organ ultrasound stimulation for targeted neuromodulation
Cotero, V. E., Fan, Y., Tsaava, T., Kressel, A. M., Hancu, I., Fitzgerald, P. B., Wallace, K. D., Kaanumalle, S., Graf, J. F., Rigby, W., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-08750-9 · Cited by 217 · see citing works
Self-citationVIP and PACAP : neuropeptide modulators of CNS inflammation, injury, and repair
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“NA then acts on MF in these organs to release ACh, which in turn acts in an autocrine or paracrine manner on immune cells that express a7 nicotinic receptors to alter their function (Rosas-Ballina and Tracey, 2009; Tracey, 2009; Thayer and Sternberg, 2010).”
BackgroundHao, J., Liu, R., Piao, W., Zhou, Q., Vollmer, T. L., Campagnolo, D. I., Xiang, R., Cava, A. L., Kaer, L. V., & Shi, F. (2010) · The Journal of Experimental Medicine · doi:10.1084/jem.20092749 · Cited by 214 · see citing works
“These factors might include CNS Ags, signals generated from neuronal cells (Tracey, 2009), and CNSderived APCs.”
BackgroundThe immunology of neurodegeneration
Czirr, E., & Wyss‐Coray, T. (2012) · Journal of Clinical Investigation · doi:10.1172/jci58656 · Cited by 211 · see citing works
“…tissues may signal to the brain through at least four different routes: active transport across the BBB, signaling at the luminal side of the BBB and propagation of secondary factors into the CNS, diffusion via circumventricular organs, and signaling via peripheral nerves such as the vagus (64–66).”
Antidepressant therapies inhibit inflammation and microglial M1-polarization
Kalkman, H. O., & Feuerbach, D. (2016) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2016.04.001 · Cited by 212 · see citing works
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The Cholinergic System and Inflammation: Common Pathways in Delirium Pathophysiology
Cerejeira, J., Nogueira, V., Luís, P., Vaz‐Serra, A., & Mukaetova‐Ladinska, E. B. (2012) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2011.03883.x · Cited by 207 · see citing works
“In addition, the CNS modulates the innate immune response through the cholinergic output of the vagus nerve.(3) It has recently been reported that individuals with delirium had lower plasma levels of cholinesterase activity than controls even before surgery, suggesting that lower plasma levels of cholinesterase activi…”
BackgroundInfluentialBrain Ischemia Suppresses Immunity in the Periphery and Brain via Different Neurogenic Innervations
Liu, Q., Jin, W.-N., Liu, Y., Shi, K., Sun, H., Zhang, F., Zhang, C., Gonzales, R. J., Sheth, K. N., Cava, A. L., et al. (2017) · Immunity · doi:10.1016/j.immuni.2017.02.015 · Cited by 207 · see citing works
“Acute ischemic brain injury swiftly activates the sympathetic, parasympathetic, and HPA axis pathways, leading to the release of norepinephrine (NE), ACh, and glucocorticoids (GCs) (Meisel et al., 2005; Prass et al., 2003; Rosas-Ballina and Tracey, 2009; Wong et al., 2011).”
Loneliness Promotes Inflammation During Acute Stress
Jaremka, L. M., Fagundes, C. P., Peng, J., Bennett, J. M., Glaser, R., Malarkey, W. B., & Kiecolt-Glaser, J. K. (2013) · Psychological Science · doi:10.1177/0956797612464059 · Cited by 255 · see citing works
“Furthermore, parasympathetic activity can reduce inflammation via the cholinergic anti-inflammatory pathway that induces acetylcholine release (Tracey, 2009).”
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“Neural anatomy has shown that the auricular branch of the vagus nerve (ABVN) projects to the nucleus tractus solitari (NTS), which is further connected with other brain regions, such as the locus coeruleus, parabrachial nucleus, hypothalamus, thalamus, amygdala, hippocampus, anterior cingulate cortex (ACC), anterior i…”
BackgroundInfluentialNeural aspects of immunomodulation: Focus on the vagus nerve
Thayer, J. F., & Sternberg, E. M. (2010) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2010.07.247 · Cited by 200 · see citing works
“N IH -PA Author M anuscript N IH -PA Author M anuscript N IH -PA Author M anuscript alpha 7 nicotinic receptors that inhibit NF kappa B and thus cytokine synthesis and release (Rosas-Ballina and Tracey, 2009).”
BackgroundThe crosstalk between autonomic nervous system and blood vessels.
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Crosstalk between the nociceptive and immune systems in host defence and disease
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The neuroinflammatory response of postoperative cognitive decline
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Midgut microbiota and host immunocompetence underlie Bacillus thuringiensis killing mechanism
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Beyond neurotransmission: acetylcholine in immunity and inflammation
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Modulatory effects of α7 nAChRs on the immune system and its relevance for CNS disorders
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“Vagus nerve stimulation, which reduces inflammation [23, 66, 69, 122], has been approved for treatment of drugresistant depression in humans [123].”
BackgroundInfluentialCholinergic System and Its Therapeutic Importance in Inflammation and Autoimmunity
Halder, N., & Lal, G. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.660342 · Cited by 186 · see citing works
- Authors
- Tracey, K. J.
- Affiliations
- Feinstein Institute for Medical Research (US)
- Corresponding author
- Tracey, Kevin J.
- ORCID
- Tracey, Kevin J.
- Venue
- Nature Reviews Immunology
- Published
- 2009-06
- Volume
- 9
- Issue
- 6
- Pages
- 418-428
- ISSN
- 1474-1733 (ISSN-L)
- 1474-1741
- PMC
- PMC4535331
- OpenAlex
- W2029051866
- Cited by
- 1,154
- References
- 102
- Citations by year
- 2026: 55 · 2025: 61 · 2024: 49 · 2023: 66 · 2022: 71 · 2021: 77 · 2020: 73 · 2019: 71 · 2018: 66 · 2017: 71 · 2016: 80 · 2015: 75 · 2014: 70 · 2013: 81 · 2012: 68
- FWCI
- 4.87
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature reviews. Immunology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- Feinstein Institutes for Medical Research
- National Institute of General Medical Sciences (R01GM057226)
- Topics
- Life Sciences › Neuroscience › Neurology › Vagus Nerve Stimulation Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Heart Rate Variability and Autonomic Control
- Keywords
- cholinergic anti-inflammatory pathway, acetylcholine, inflammatory cytokines, neural circuits, innate immunity, neuroimmune regulation, inflammatory diseases
- MeSH terms
- Animals, Cardiovascular Physiological Phenomena, Catecholamines, Efferent Pathways, Homeostasis, Humans, Hypertension, Immunity, Innate, Inflammation, Receptors, Cholinergic, Reflex, Neuroimmunomodulation
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