Abstract
Immune activation modulates sleep by influencing brain neurons involved in the regulation and maintenance of sleep-wake cycles and arousal states. The precise mechanisms by which this occurs are not completely established, but seem to follow from direct influences of immune-derived mediators, such as cytokines, on sleep/wake neurons (Opp 2005), and/or via activation of peripheral viscerosensory neurons driving brain neural circuits that modulate arousal states in response to internal and external challenges. In this chapter we will review the organization of visceral sensory pathways that carry immune-related information to the brain, and recent findings regarding the brain neurocircuitry connecting immune-brain interfaces with arousal network nuclei that influence sleep-wake states.
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References
Adriaensen, D., Timmermans, J.-P., Brouns, I., Berthoud H.-R., Neuhuber, W.L., and Scheuermann D.W. (1998) Pulmonary intraepithelial vagal nodose afferent nerve terminals are confined to neuroepithelial bodies: An anterograde tracing and confocal microscopy study in adult rats. Cell Tiss Res 293, 395–405.
Banks, W.A. (2005) Blood—brain barrier transport of cytokines: A mechanism for neuropathology. Curr Pharm Des 11, 973–84.
Beckstead, R.M., and Norgren, R. (1979) An autoradiographic examination of the central distribution of the trigeminal, facial, glossopharyngeal, and vagal nerves in the monkey. J Comp Neurol 184, 455–472.
Berthoud, H.-R., Kressel, M., and Neuhuber, W.L. (1995) Vagal afferent innervation of the rat abdominal paraganglia as revealed by anterograde DiI-tracing and confocal microscopy. Acta Anat 152, 127–132.
Berthoud, H.-R., and Neuhuber, W.L. (2000) Functional and chemical anatomy of the afferent vagal system. Auton Neurosci 85, 1–17.
Bluthe, R.-M., Michaud, B., Kelly, K.W., and Dantzer, R. (1996) Vagotomy blocks behavioral effects of interleukin-1 injected via the intraperitoneal route but not by other systemic routes. Neuroreport 7, 2823–2827.
Bronzino, J.D., Stern, W.C., Leahy, J.P., and Morgane, P.J. (1976) Power spectral analysis of EEG activity obtained from cortical and subcortical sites during vigilance states in the cat. Brain Res Bull 1, 285–294.
Buller, K., Xu, Y., Dayas, C., and Day, T. (2001) Dorsal and ventral medullary catecholamine cell groups contribute differentially to systemic interleukin-1beta-induced hypothalamic pituitary adrenal axis responses. Neuroendocrinology 73, 129–138.
Cano, G., Sved, A.F., Rinaman, L., Rabin, B.S., and Card, J.P. (2001) Characterization of the central nervous system innervation of the rat spleen using viral transneuronal tracing. J Comp Neurol 439, 1–18.
Carpenter, M.B., and Sutin J (1983) Human Neuroanatomy. 8th Edn. Williams & Wilkins, Baltimore.
Chernicky, C.L., Barnes, K.L., Ferrario, C.M., and Conomy, J.P. (1984) Afferent projections of the cervical vagus and nodose ganglion in the dog. Brain Res Bull 13, 401–411.
Chou, T.C., Bjorkum, A.A., Gaus, S.E., Lu, J., Scammell, T.E., and Saper, C.B. (2002) Afferents to the ventrolateral preoptic nucleus. J Neurosci 22, 977–990.
Ek, M., Kurosawa, M., Lundeberg, T., and Ericsson, A. (1998) Activation of vagal afferents after intravenous injection of interleukin-1 : Role of endogenous prostaglandins. J Neurosci 18, 9471–9479.
Elmquist, J.K., Scammell, T.E., Jacobson, C.D., and Saper, C.B. (1996) Distribution of Foslike immunoreactivity in the rat brain following intravenous lipopolysaccharide administration. J Comp Neurol 371, 85–103.
Ericsson A., Arias, C., and Sawchenko, P.E. (1997) Evidence for an intramedullary prostaglandin-dependent mechanism in the activation of stress-related neuroendocrine circuitry by intravenous interleukin-1. J Neurosci 17, 7166–7179.
Ericsson, A., Kovacs, K.J., and Sawchenko, P.E. (1994) A functional anatomical analysis of central pathways subserving the effects of interleukin-1 on stress-related neuroendocrine neurons. J Neurosci 14, 897–913.
Ericsson, A., Liu, C., Hart, R.P., and Sawchenko, P.E. (1995) Type 1 interleukin-1 receptor in the rat brain: Distribution, regulation, and relationship to sites of IL-1-induced cellular activation. J Comp Neurol 361, 681–698.
Felton, D.L., Livnat, S., Felton, S.Y., Carlson, S.L., Bellinger, D.L., and Yeh, P. (1984) Sympathetic innervation of lymph nodes in mice. Brain Res Bull 13, 693–696.
Gaykema, R.P.A., Goehler, L.E., Tilders, F.J.H., Bol, J.G.M., McGorry, M.M., Maier, S.F., and Watkins, L.R. (1998) Bacterial endotoxin induces Fos immunoreactivity in primary afferent neurons of the vagus nerve. Neuroimmunomodulation 5, 234–240.
Goehler, L.E. (2003) Immunsensory signaling: Role of cytokines. In: Z. Kronfol (Ed.), Cytokines and Mental Health. Kluwer Academic, Boston, pp. 15–38.
Goehler, L.E., Erisir, A., and Gaykema, R.P.A. (2006) Neural-immune interface in the rat area postrema. Neuroscience 140, 1415–1434.
Goehler, L.E., Gaykema, R.P.A., Hammack, S.E., Maier, S.F., and Watkins L.R. (1998) Interleukin-1 induces c-Fos immunoreactivity in primary afferent neurons of the vagus nerve. Brain Res 804, 306–310.
Goehler, L.E., Gaykema, R.P.A., Nguyen, K.T., Lee, J.L, Tilders, F.J.H., Maier, S.F., and Watkins L.R. (1999) Interleukin-1β in immune cells of the abdominal vagus nerve: An immune to nervous system link? J Neurosci 17, 2799–2806.
Goehler, L.E., Gaykema, R.P.A., Hansen, M.K., Maier, S.F., and Watkins, L.R. (2000) Vagally mediated fever: A visceral chemosensory modality. Auton Neurosci 85, 49–59.
Goehler, L.E., Gaykema, R.P.A., Opitz, N., Reddaway, R., Badr, N.A., and Lyte, M. (2005) Activation in vagal afferents and central autonomic pathways: Early responses to intestinal infection with Campylobacter jejuni. Brain Behav Immun 19, 334–344.
Goehler, L.E., Relton, J.K., Dripps, D., Keichle, R., Tartaglia, N., Maier, S.F., and Watkins, L.R. (1997) Vagal paraganglia bind biotinylated interleukin-1 receptor antagonist: A possible mechanism for immune-to-brain communication. Brain Res Bull 43, 357–364.
Golanov, E.V., and Reis, D.J. (2001) Neurons of the nucleus of the solitary tract synchronize EEG and elevate cerebral blood flow via a novel medullary area. Brain Res 892, 1–12.
Hansen, M.K., and Krueger, J.M. (1997) Subdiaphragmatic vagotomy blocks the sleep- and fever-promoting effects of interleukin-1 . Am J Physiol 273, R1246–R1253.
Hansen, M.K., O'Conner, K.A., Goehler, L.E., Watkins, L.R., and Maier, S.F. (2001) The role of the vagus nerve in interleukin-1 -induced fever is dependent on dose. Am J Physiol 280, R929–R934.
Hosoi, T., Okuma, Y., Matsuda, T., and Nomura, Y. (2005) Novel pathway for LPS-induced afferent vagus nerve activation: Possible role of nodose ganglion. Auton Neurosci 120, 104–107.
Ishizuka, Y., Ishida, Y., Kunitake, T., Kato, K., Hanamori, T., Mitsuyama, Y., and Kannan, H. (1997) Effects of area postrema lesion and abdominal vagotomy on interleukin-1β-induced norepinephrine release in the hypothalamic paraventricular nucleus region in the rat. Neurosci Lett 223, 57–60.
Kobierski, L.A., Srivastava, S., and Borsook, D. (2000) Systemic lipopolysaccharide and interleukin-1β activate the interleukin 6: STAT intracellular signaling pathway in neurons of mouse trigeminal ganglion. Neurosci Lett 281, 61–64.
Konsman, J.P., Tridon, V., and Dantzer, R. (2000) Diffusion and action of intracerebroventricularly injected interleukin-1 in the CNS. Neuroscience 101, 957–967.
Lee, H.Y., Whiteside, M.B., and Herkenham M. (1998) Area postrema removal abolishes stimulatory effects of intravenous interleukin-1β on hypothalamic-pituitary-adrenal axis activity and c-fos mRNA in the hypothalamic paraventricular nucleus. Brain Res Bull 46, 495–503.
Marvel, F.A., Chen, C.-C., Badr, N.A., Gaykema, R.P.A., and Goehler L.E. (2004) Reversible inactivation of the dorsal vagal complex blocks lipopolysaccharide-induced social withdrawal and c-Fos expression in central autonomic nuclei. Brain Behav Immun 18, 123–143.
Mascarucci, P., Perego, C., Terrazzino, S., and DeSimoni, M.G. (1998) Glutamate release in the nucleus tractus solitarius induced by peripheral lipopolysaccharide and interleukin-1 β . Neuroscience 86, 1285–1290.
McMenamin, P.G. (1999) Distribution and phenotype of dendritic cells and resident tissue macrophages in the dura mater, leptomeninges and choroid plexus of the rat brain as demonstrated in wholemount preparations. J Comp Neurol 405, 553–562.
Nagura, H., Ohtani, H., Masuda, T., Kimura, M., and Nakamura, S. (1991) HLA-DR expression on M cells overlaying Peyer's patches is a common feature of human small intestine. Acta Pathol Jpn 41, 818–823.
Nance, D.M., and Burns, J. (1989) Innervation of the spleen in the rat: Evidence for absence of afferent innervation. Brain Behav Immun 3, 281–290.
Niijima A. (1996) The afferent discharges from sensors for interleukin-1 β in the hepatoportal system in the anesthetized rat. J Auton Nerv Syst 61, 287–291.
Opp, M.R. (2005) Cytokines and sleep. Sleep Med Rev 9, 355–364.
Opp, M.R., and Toth, L.A. (1998) Somnogenic and pyrogenic effects of interleukin-1 beta and lipopolysaccharide in intact and vagotomized rats. Life Sci 62, 923–936.
Popper, P., Mantyh, C.R., Vigna, S.R., Maggio, J.E., and Mantyh, P.W. (1988) The localization of sensory nerve fibers and receptor binding sites for sensory neuropeptides in canine lymph nodes. Peptides 9, 257–267.
Quan, N., Whiteside, M., and Herkenham, M. (1998) Time course and localization patterns of interleukin-1 messenger RNA expression in brain and pituitary after peripheral administration of lipopolysaccharide. Neuroscience 83, 281–293.
Riche, D., De Pommery, J., and Menetrey, D. (1990) Neuropeptides and catecholamines in efferent projections of the nuclei of the solitary tract in the rat. J Comp Neurol 293, 399–424.
Romeo, H., Tio, D.L., Rahman, S.U., Chiappelli, F., and Taylor, A.N. (2001) The glossopharyngeal nerve as a novel pathway in immune-to-brain communication: Relevance to neuroimmune surveillance of the oral cavity. J Neuroimmunol 115, 91–100.
Saper, C.B., Scammell, T.E., and Lu, J. (2005) Hypothalamic regulation of sleep and circadian rhythms. Nature 437, 1257–1263.
Scafers, M., Svensson, C., Sommer, C., and Sorkin, L.S. (2003) Tumor necrosis factor-a induces mechanical allodynia after spinal nerve ligation by activation of p38 MAPK in primary sensory neurons. J Neurosci 23, 2517–2521.
Sykes, R.M., Spyer, K.M., and Izzo, P.N. (1997) Demonstration of glutamate immunoreactivity in vagal sensory afferents in the nucleus tractus solitarius of the rat. Brain Res 762, 1–11.
Vernet-der Garabedian, B., Lemaigre-Dubreuil, Y., and Mariani, J. (2000) Central origin of IL-1 β produced during peripheral inflammation: Role of meninges. Mol Brain Res 75, 259–263.
Wan, W., Janz, L., Vriend, C.Y., Sorensen, C.M., Greenberg, A.H., and Nance, D.M., (1993) Differential induction of c-Fos immunoreactivity in hypothalamus and brainstem nuclei following central and peripheral administration of endotoxin. Brain Res Bull 32, 581–587.
Wang, X., Wang, B.-R., Duan, W.-L., Liu, H.L., and Ju, G. (2000) The expression of IL-1 receptor type 1 in nodose ganglion and vagal paraganglia in the rat. Chin J Neurosci 16, 90–93.
Wang, X., Wang, B.-R., Duan, X.-L., Zhang, P., Ding, Y.-Q., Jia, Y., Jiao, X.-Y., and Ju, G. (2002) Strong expression of interleukin-1 receptor type 1 in the rat carotid body. J Histochem Cytochem 50, 1677–1684.
Zhang, J.-M., Li, H., Liu, B., and Brull, S.J. (2002) Acute topical application of tumor necrosis factor a evokes protein kinase A-dependent responses in rat sensory neurons. J Neurophysiol 88, 1387–1392.
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Goehler, L., Gaykema, R. (2007). Immune Signaling to Brain: Mechanisms and Potential Pathways Influencing Sleep. In: Pandi-Perumal, S., Cardinali, D.P., Chrousos, G.P. (eds) Neuroimmunology of Sleep. Springer, Boston, MA. https://doi.org/10.1007/978-0-387-69146-6_6
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DOI: https://doi.org/10.1007/978-0-387-69146-6_6
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