Interleukin-1β modulates state-dependent discharge activity of preoptic area and basal forebrain neurons: role in sleep regulation
dc.contributor.author | Alam, Md. Noor | en_US |
dc.contributor.author | McGinty, Dennis | en_US |
dc.contributor.author | Bashir, Tariq | en_US |
dc.contributor.author | Kumar, Sunil | en_US |
dc.contributor.author | Imeri, Luca | en_US |
dc.contributor.author | Opp, Mark R. | en_US |
dc.contributor.author | Szymusiak, Ronald | en_US |
dc.date.accessioned | 2010-06-01T22:24:23Z | |
dc.date.available | 2010-06-01T22:24:23Z | |
dc.date.issued | 2004-07 | en_US |
dc.identifier.citation | Alam, Md. Noor; McGinty, Dennis; Bashir, Tariq; Kumar, Sunil; Imeri, Luca; Opp, Mark R.; Szymusiak, Ronald (2004). "Interleukin-1β modulates state-dependent discharge activity of preoptic area and basal forebrain neurons: role in sleep regulation." European Journal of Neuroscience 20(1): 207-216. <http://hdl.handle.net/2027.42/75399> | en_US |
dc.identifier.issn | 0953-816X | en_US |
dc.identifier.issn | 1460-9568 | en_US |
dc.identifier.uri | https://hdl.handle.net/2027.42/75399 | |
dc.identifier.uri | http://www.ncbi.nlm.nih.gov/sites/entrez?cmd=retrieve&db=pubmed&list_uids=15245493&dopt=citation | en_US |
dc.description.abstract | Interleukin-1β (IL-1) is a pro-inflammatory cytokine that has been implicated in the regulation of nonrapid eye movement (nonREM) sleep. IL-1, IL-1 receptors and the IL-1 receptor antagonist (ra) are present normally in discrete brain regions, including the preoptic area (POA) of the hypothalamus and the adjoining magnocellular basal forebrain (BF). The POA/BF have been implicated in the regulation of sleep–wakefulness. We hypothesized that IL-1 promotes nonREM sleep, in part by altering the state-dependent discharge activity of POA/BF neurons. We recorded the sleep–wake discharge profiles of 83 neurons in the lateral POA/BF and assessed the effects of IL-1, IL-1ra, and IL-ra + IL-1 delivered through a microdialysis probe on state-dependent neuronal discharge activity. IL-1 decreased the discharge rate of POA/BF neurons as a group ( n = 55) but wake-related and sleep-related neurons responded differently. IL-1 significantly decreased the discharge rate of wake-related neurons. Of 24 wake-related neurons studied, 19 (79%) neurons exhibited a greater than 20% change in their discharge in the presence of IL-1 during waking. IL-1 suppressed the discharge activity of 18 of 19 responsive neurons. Of 13 sleep-related neurons studied, IL-1 increased the discharge activity of five and suppressed the discharge activity of four neurons. IL-1ra increased the discharge activity of four of nine neurons and significantly attenuated IL-1-induced effects on neuronal activity of POA/BF neurons ( n = 19). These results suggest that the sleep-promoting effects of IL-1 may be mediated, in part, via the suppression of wake-related neurons and the activation of a subpopulation of sleep-related neurons in the POA/BF. | en_US |
dc.format.extent | 687787 bytes | |
dc.format.extent | 3109 bytes | |
dc.format.mimetype | application/pdf | |
dc.format.mimetype | text/plain | |
dc.publisher | Blackwell Science Ltd | en_US |
dc.rights | 2004 Federation of European Neuroscience Societies | en_US |
dc.subject.other | Cytokine | en_US |
dc.subject.other | Extracellular Unit Recording | en_US |
dc.subject.other | Interleukin-1 Receptor Antagonist | en_US |
dc.subject.other | Microdialysis | en_US |
dc.subject.other | Rat | en_US |
dc.title | Interleukin-1β modulates state-dependent discharge activity of preoptic area and basal forebrain neurons: role in sleep regulation | en_US |
dc.type | Article | en_US |
dc.subject.hlbsecondlevel | Neurosciences | en_US |
dc.subject.hlbtoplevel | Health Sciences | en_US |
dc.description.peerreviewed | Peer Reviewed | en_US |
dc.contributor.affiliationum | Departments of Anesthesiology and Molecular & Integrative Physiology, University of Michigan, Ann Arbor, MI 48109, USA | en_US |
dc.contributor.affiliationother | Veteran Affairs Greater Los Angeles Health Care System, 16111 Plummer Street, North Hills, CA 91343, USA | en_US |
dc.contributor.affiliationother | Department of Psychology | en_US |
dc.contributor.affiliationother | Department of Medicine, University of California, Los Angeles, CA 90033, USA | en_US |
dc.contributor.affiliationother | Institute of Human Physiology II, University of Milan, Milan, Italy | en_US |
dc.identifier.pmid | 15245493 | en_US |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/75399/1/j.1460-9568.2004.03469.x.pdf | |
dc.identifier.doi | 10.1111/j.1460-9568.2004.03469.x | en_US |
dc.identifier.source | European Journal of Neuroscience | en_US |
dc.identifier.citedreference | Alam, M. N. & Mallick, B. N. ( 1990 ) Differential acute influence of medial and lateral preoptic areas on sleep-wakefulness in freely moving rats. Brain Res., 525, 242 – 248. | en_US |
dc.identifier.citedreference | Alam, M. N., McGinty, D. & Szymusiak, R. ( 1995 ) Neuronal discharge of preoptic/anterior hypothalamic thermosensitive neurons: relation to NREM sleep. Am. J. Physiol., 269, R1240 – R1249. | en_US |
dc.identifier.citedreference | Alam, M. N., Szymusiak, R., Gong, H., King, J. & McGinty, D. ( 1999 ) Adenosinergic modulation of rat basal forebrain neurons during sleep and waking: neuronal recording with microdialysis. J. Physiol., 521, 679 – 690. | en_US |
dc.identifier.citedreference | Baker, S. S., Stewart, D. R., Xu, F., Szymusiak, R., Opp, M. R. & McGinty, D. F. ( 2003 ) Interleukin-1b treatment increases c-Fos protein expression in sleep – active regions of the preoptic hypothalamus in rats. Neurosci. Abstract, 617.614. | en_US |
dc.identifier.citedreference | Borsody, M. K. & Weiss, J. M. ( 2002 ) Alteration of locus coeruleus neuronal activity by interleukin-1 and the involvement of endogenous corticotropin-releasing hormone. Neuroimmunomodulation, 10, 101 – 121. | en_US |
dc.identifier.citedreference | Cunningham, E. T. Jr, Wada, E., Carter, D. B., Tracey, D. E., Battey, J. F. & De Souza, E. B. ( 1992 ) Distribution of type I interleukin-1 receptor messenger RNA in testis: an in situ histochemical study in the mouse. Neuroendocrinology, 56, 94 – 99. | en_US |
dc.identifier.citedreference | De, A., Churchill, L., Obal, F. Jr, Simasko, S. M. & Krueger, J. M. ( 2002 ) GHRH and IL1beta increase cytoplasmic Ca(2+) levels in cultured hypothalamic GABAergic neurons. Brain Res., 949, 209 – 212. | en_US |
dc.identifier.citedreference | Detari, L., Rasmusson, D. D. & Semba, K. ( 1999 ) The role of basal forebrain neurons in tonic and phasic activation of the cerebral cortex. Prog. Neurobiol., 58, 249 – 277. | en_US |
dc.identifier.citedreference | Dinarello, C. A. ( 1991 ) Interleukin-1 and interleukin-1 antagonism. Blood, 77, 1627 – 1652. | en_US |
dc.identifier.citedreference | Dinarello, C. A. ( 1996 ) Biologic basis for interleukin-1 in disease. Blood, 87, 2095 – 2147. | en_US |
dc.identifier.citedreference | Dripps, D. J., Verderber, E., Ng, R. K., Thompson, R. C. & Eisenberg, S. P. ( 1991 ) Interleukin-1 receptor antagonist binds to the type II interleukin-1 receptor on B cells and neutrophils. J. Biol. Chem., 266, 20311 – 20315. | en_US |
dc.identifier.citedreference | Ericsson, A., Liu, C., Hart, R. P. & 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. | en_US |
dc.identifier.citedreference | Fang, J., Wang, Y. & Krueger, J. M. ( 1998 ) Effects of interleukin-1 beta on sleep are mediated by the type I receptor. Am. J. Physiol., 274, R655 – R660. | en_US |
dc.identifier.citedreference | Gallis, B., Prickett, K. S., Jackson, J., Slack, J., Schooley, K., Sims, J. E. & Dower, S. K. ( 1989 ) IL-1 induces rapid phosphorylation of the IL-1 receptor. J. Immunol., 143, 3235 – 3240. | en_US |
dc.identifier.citedreference | Gaus, S. E., Strecker, R. E., Tate, B. A., Parker, R. A. & Saper, C. B. ( 2002 ) Ventrolateral preoptic nucleus contains sleep-active, galaninergic neurons in multiple mammalian species. Neuroscience, 115, 285 – 294. | en_US |
dc.identifier.citedreference | Gemma, C., Imeri, L., de Simoni, M. G. & Mancia, M. ( 1997 ) Interleukin-1 induces changes in sleep, brain temperature, and serotonergic metabolism. Am. J. Physiol., 272, R601 – R606. | en_US |
dc.identifier.citedreference | Gong, H., McGinty, D., Guzman-Marin, R., Chew, K. T., Stewart, D. & Szymusiak, R. ( 2004 ) Activation of c-fos in GABAergic neurons in the preoptic area during sleep and in response to sleep deprivation. J. Physiol. (Lond.), 556, 935 – 946. | en_US |
dc.identifier.citedreference | Hohagen, F., Timmer, J., Weyerbrock, A., Fritsch-Montero, R., Ganter, U., Krieger, S., Berger, M. & Bauer, J. ( 1993 ) Cytokine production during sleep and wakefulness and its relationship to cortisol in healthy humans. Neuropsychobiology, 28, 9 – 16. | en_US |
dc.identifier.citedreference | Hori, T. & Katafuchi, T. ( 1998 ) Cell biology and the functions of thermosensitive neurons in the brain. Prog. Brain Res., 115, 9 – 23. | en_US |
dc.identifier.citedreference | Imeri, L., Gemma, C., De Simoni, M. G., Opp, M. R. & Mancia, M. ( 1999 ) Hypothalamic serotonergic activity correlates better with brain temperature than with sleep–wake cycle and muscle tone in rats. Neuroscience, 89, 1241 – 1246. | en_US |
dc.identifier.citedreference | Jones, B. E. ( 2004 ) Activity, modulation and role of basal forebrain cholinergic neurons innervating the cerebral cortex. Prog. Brain Res., 145, 157 – 169. | en_US |
dc.identifier.citedreference | Konsman, J. P., Parnet, P. & Dantzer, R. ( 2002 ) Cytokine-induced sickness behaviour: mechanisms and implications. Trends Neurosci., 25, 154 – 159. | en_US |
dc.identifier.citedreference | Krueger, J. M., Walter, J., Dinarello, C. A., Wolff, S. M. & Chedid, L. ( 1984 ) Sleep-promoting effects of endogenous pyrogen (interleukin-1). Am. J. Physiol., 246, R994 – R999. | en_US |
dc.identifier.citedreference | Lu, J., Greco, M. A., Shiromani, P. & Saper, C. B. ( 2000 ) Effect of lesions of the ventrolateral preoptic nucleus on NREM and REM sleep. J. Neurosci., 20, 3830 – 3842. | en_US |
dc.identifier.citedreference | Lue, F. A., Bail, M., Jephthah-Ochola, J., Carayanniotis, K., Gorczynski, R. & Moldofsky, H. ( 1988 ) Sleep and cerebrospinal fluid interleukin-1-like activity in the cat. Int. J. Neurosci., 42, 179 – 183. | en_US |
dc.identifier.citedreference | Luk, W. P., Zhang, Y., White, T. D., Lue, F. A., Wu, C., Jiang, C. G., Zhang, L. & Moldofsky, H. ( 1999 ) Adenosine: a mediator of interleukin-1beta-induced hippocampal synaptic inhibition. J. Neurosci., 19, 4238 – 4244. | en_US |
dc.identifier.citedreference | Manfridi, A., Brambilla, D., Bianchi, S., Mariotti, M., Opp, M. R. & Imeri, L. ( 2003 ) Interleukin-1beta enhances non-rapid eye movement sleep when microinjected into the dorsal raphe nucleus and inhibits serotonergic neurons in vitro. Eur. J. Neurosci., 18, 1041 – 1049. | en_US |
dc.identifier.citedreference | McGinty, D. & Szymusiak, R. ( 2003 ) Hypothalamic regulation of sleep and arousal. Front. Biosci., 8, 1074 – 1083. | en_US |
dc.identifier.citedreference | McGinty, D., Szymusiak, R. & Thomson, D. ( 1994 ) Preoptic/anterior hypothalamic warming increases EEG delta frequency activity within non-rapid eye movement sleep. Brain Res., 667, 273 – 277. | en_US |
dc.identifier.citedreference | Muller, C. E. ( 2001 ) A1 adenosine receptors and their ligands: overview and recent developments. Farmaco, 56, 77 – 80. | en_US |
dc.identifier.citedreference | Nakashima, T., Hori, T., Mori, T., Kuriyama, K. & Mizuno, K. ( 1989 ) Recombinant human interleukin-1 beta alters the activity of preoptic thermosensitive neurons in vitro. Brain Res. Bull., 23, 209 – 213. | en_US |
dc.identifier.citedreference | Obal, F. Jr & Krueger, J. M. ( 2003 ) Biochemical regulation of non-rapid-eye-movement sleep. Front. Biosci., 8, 520 – 550. | en_US |
dc.identifier.citedreference | Obal, F. Jr, Opp, M., Cady, A. B., Johannsen, L., Postlethwaite, A. E., Poppleton, H. M., Seyer, J. M. & Krueger, J. M. ( 1990 ) Interleukin 1 alpha and an interleukin 1 beta fragment are somnogenic. Am. J. Physiol., 259, R439 – R446. | en_US |
dc.identifier.citedreference | Oka, T., Oka, K., Hosoi, M., Aou, S. & Hori, T. ( 1995 ) The opposing effects of interleukin-1 beta microinjected into the preoptic hypothalamus and the ventromedial hypothalamus on nociceptive behavior in rats. Brain Res., 700, 271 – 278. | en_US |
dc.identifier.citedreference | Opp, M. R. & Krueger, J. M. ( 1991 ) Interleukin 1-receptor antagonist blocks interleukin 1-induced sleep and fever. Am. J. Physiol., 260, R453 – R457. | en_US |
dc.identifier.citedreference | Opp, M. R. & Krueger, J. M. ( 1994 ) Anti-interleukin-1 beta reduces sleep and sleep rebound after sleep deprivation in rats. Am. J. Physiol., 266, R688 – R695. | en_US |
dc.identifier.citedreference | Opp, M. R., Obal, F. Jr & Krueger, J. M. ( 1988 ) Effects of alpha-MSH on sleep, behavior, and brain temperature: interactions with IL 1. Am. J. Physiol., 255, R914 – R922. | en_US |
dc.identifier.citedreference | Opp, M., Obal, F. Jr & Krueger, J. M. ( 1989 ) Corticotropin-releasing factor attenuates interleukin 1-induced sleep and fever in rabbits. Am. J. Physiol., 257, R528 – R535. | en_US |
dc.identifier.citedreference | Opp, M. R., Obal, F. Jr & Krueger, J. M. ( 1991 ) Interleukin 1 alters rat sleep: temporal and dose-related effects. Am. J. Physiol., 260, R52 – R58. | en_US |
dc.identifier.citedreference | Paxinos, G. & Watson, C. ( 1998 ) The Rat Brain: in Stereotaxic Coordinates. Academic Press, New York. | en_US |
dc.identifier.citedreference | Porkka-Heiskanen, T., Alanko, L., Kalinchuk, A. & Stenberg, D. ( 2002 ) Adenosine and sleep. Sleep Med. Rev., 6, 321 – 332. | en_US |
dc.identifier.citedreference | Rasmusson, D. D., Clow, K. & Szerb, J. C. ( 1994 ) Modification of neocortical acetylcholine release and electroencephalogram desynchronization due to brainstem stimulation by drugs applied to the basal forebrain. Neuroscience, 60, 665 – 677. | en_US |
dc.identifier.citedreference | Ribeiro, J. A. ( 1999 ) Adenosine A2A receptor interactions with receptors for other neurotransmitters and neuromodulators. Eur. J. Pharmacol., 375, 101 – 113. | en_US |
dc.identifier.citedreference | Rosenwasser, L. J. ( 1998 ) Biologic activities of IL-1 and its role in human disease. J. Allergy. Clin. Immunol., 102, 344 – 350. | en_US |
dc.identifier.citedreference | Rothwell, N. J. & Luheshi, G. N. ( 2000 ) Interleukin 1 in the brain: biology, pathology and therapeutic target. Trends Neurosci., 23, 618 – 625. | en_US |
dc.identifier.citedreference | Saper, C. B., Chou, T. C. & Scammell, T. E. ( 2001 ) The sleep switch: hypothalamic control of sleep and wakefulness. Trends Neurosci., 24, 726 – 731. | en_US |
dc.identifier.citedreference | Schobitz, B., De Kloet, E. R. & Holsboer, F. ( 1994 ) Gene expression and function of interleukin 1, interleukin 6 and tumor necrosis factor in the brain. Prog. Neurobiol., 44, 397 – 432. | en_US |
dc.identifier.citedreference | Semba, K. ( 2004 ) Phylogenetic and ontogenetic aspects of the basal forebrain cholinergic neurons and their innervation of the cerebral cortex. Prog. Brain Res., 145, 3 – 43. | en_US |
dc.identifier.citedreference | Sherin, J. E., Shiromani, P. J., McCarley, R. W. & Saper, C. B. ( 1996 ) Activation of ventrolateral preoptic neurons during sleep. Science, 271, 216 – 219. | en_US |
dc.identifier.citedreference | Shirakawa, F., Chedid, M., Suttles, J., Pollok, B. A. & Mizel, S. B. ( 1989 ) Interleukin 1 and cyclic AMP induce kappa immunoglobulin light-chain expression via activation of an NF-kappa B-like DNA-binding protein. Mol. Cell. Biol., 9, 959 – 964. | en_US |
dc.identifier.citedreference | Stylianou, E., O'Neill, L. A., Rawlinson, L., Edbrooke, M. R., Woo, P. & Saklatvala, J. ( 1992 ) Interleukin 1 induces NF-kappa B through its type I but not its type II receptor in lymphocytes. J. Biol. Chem., 267, 15836 – 15841. | en_US |
dc.identifier.citedreference | Szymusiak, R., Alam, N. & McGinty, D. ( 2000 ) Discharge patterns of neurons in cholinergic regions of the basal forebrain during waking and sleep. Behav. Brain. Res., 115, 171 – 182. | en_US |
dc.identifier.citedreference | Szymusiak, R., Alam, N., Steininger, T. L. & McGinty, D. ( 1998 ) Sleep–waking discharge patterns of ventrolateral preoptic/anterior hypothalamic neurons in rats. Brain Res., 803, 178 – 188. | en_US |
dc.identifier.citedreference | Takahashi, S., Kapas, L., Fang, J., Seyer, J. M., Wang, Y. & Krueger, J. M. ( 1996 ) An interleukin-1 receptor fragment inhibits spontaneous sleep and muramyl dipeptide-induced sleep in rabbits. Am. J. Physiol., 271, R101 – R108. | en_US |
dc.identifier.citedreference | Toth, L. A. & Krueger, J. M. ( 1988 ) Alteration of sleep in rabbits by Staphylococcus aureus infection. Infect. Immunol., 56, 1785 – 1791. | en_US |
dc.identifier.citedreference | Toth, L. A. & Krueger, J. M. ( 1989 ) Effects of microbial challenge on sleep in rabbits. FASEB J., 3, 2062 – 2066. | en_US |
dc.identifier.citedreference | Xi, X. & Toth, L. A. ( 2000 ) Lipopolysaccharide effects on neuronal activity in rat basal forebrain and hypothalamus during sleep and waking. Am. J. Physiol., 278, R620 – R627. | en_US |
dc.identifier.citedreference | Xin, L. & Blatteis, C. M. ( 1992 ) Blockade by interleukin-1 receptor antagonist of IL-1 beta-induced neuronal activity in guinea pig preoptic area slices. Brain Res., 569, 348 – 352. | en_US |
dc.identifier.citedreference | Yabuuchi, K., Minami, M., Katsumata, S. & Satoh, M. ( 1994 ) Localization of type I interleukin-1 receptor mRNA in the rat brain. Mol. Brain Res., 27, 27 – 36. | en_US |
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