Interleukin-1 inhibits putative cholinergic neurons in vitro and REM sleep when microinjected into the rat laterodorsal tegmental nucleus

Sleep

Volumn 33, Issue 7, 2010, Pages 919-929

  Brambilla, Dario ^a   Barajon, Isabella ^a   Bianchi, Susanna ^a   Opp, Mark R ^b   Imeri, Luca ^a,b  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Acetylcholine; Adenosine; Cytokines; GABA; Glutamate; Patch clamp

Indexed keywords

INTERLEUKIN 1;

ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; BRAIN STEM; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EVOKED RESPONSE; IN VITRO STUDY; INFECTION; MALE; MICROINJECTION; NONHUMAN; PRIORITY JOURNAL; RAT; REM SLEEP; TEGMENTUM;

EID: 77954366479     PISSN: 01618105     EISSN: 15509109     Source Type: Journal    
DOI: 10.1093/sleep/33.7.919     Document Type: Article

References (65)

1. Imeri L, Opp MR. How (and why) the immune system makes us sleep. Nat Rev Neurosci 2009;10:199-210.
2. Kluger MJ, Kozak W, Conn CA, Leon LR, Soszynski D. The adaptive value of fever. Infect Dis Clin North Am 1996;10:1-20.
3. Opp MR. Cytokines and sleep. Sleep Med Rev 2005; 9:355-64.
4. Vitkovic L, Bockaert J, Jacque C. "Inflammatory" cytokines: neuromodulators in normal brain? J Neurochem 2000;74:457-71.
5. Gemma C, Imeri L, De Simoni MG, Mancia M. Interleukin-1 induces changes in sleep, brain temperature, and serotonergic metabolism. Am J Physiol 1997;272:R601-6.
6. Opp MR, Obal F Jr, Krueger JM. Interleukin 1 alters rat sleep: temporal and dose-related effects. Am J Physiol 1991;260:R52-8.
7. Olivadoti MD, Opp MR. Effects of i.c.v. administration of interleukin-1 on sleep and body temperature of interleukin-6-deficient mice. Neuroscience 2008;153:338-48.
8. Obal F Jr, Krueger JM. Biochemical regulation of non-rapid-eye-movement sleep. Front Biosci 2003;8:d520-50.
9. McCarley RW. Neurobiology of REM and NREM sleep. Sleep Med 2007;8:302-30.
10. Thakkar M, Portas C, McCarley RW. Chronic low-amplitude electrical stimulation of the laterodorsal tegmental nucleus of freely moving cats increases REM sleep. Brain Res 1996;723:223-7.
11. Webster HH, Jones BE. Neurotoxic lesions of the dorsolateral pontomesencephalic tegmentum-cholinergic cell area in the cat. II. Effects upon sleep-waking states. Brain Res 1988;458:285-302.
12. El Mansari M, Sakai K, Jouvet M. Unitary characteristics of presumptive cholinergic tegmental neurons during the sleep-waking cycle in freely moving cats. Exp Brain Res 1989;76:519-29. (Pubitemid 19203604)
13. Steriade M, Pare D, Datta S, Oakson G, Curro DR. Different cellular types in mesopontine cholinergic nuclei related to ponto-geniculo-occipital waves. J Neurosci 1990;10:2560-79.
14. Mitani A, Ito K, Mitani Y, McCarley RW. Morphological and electrophysiological identification of gigantocellular tegmental field neurons with descending projections in the cat: I. Pons. J Comp Neurol 1988;268:527-45. (Pubitemid 18065915)
15. Semba K, Reiner PB, Fibiger HC. Single cholinergic mesopontine tegmental neurons project to both the pontine reticular formation and the thalamus in the rat. Neuroscience 1990;38:643-54.
16. Semba K. The mesopontine cholinergic system: a dual role in REM sleep and wakefulness. In: Lydic R, Baghdoyan HA, eds. Handbook of behavioral state control: cellular and molecular mechanisms. Boca Raton: CRC Press, 1999: 161-80.
17. Baghdoyan HA. Cholinergic mechanisms regulating REM sleep. In: Schwarz WJ, editor. Sleep science: integrating basic research and clinical practice. Basel: Karger, 2002: 88-116.
18. Imeri L, Bianchi S, Angeli P, Mancia M. Selective blockade of different brain stem muscarinic receptor subtypes: effects on the sleep-wake cycle. Brain Res 1994;636:68-72.
19. Maloney KJ, Mainville L, Jones BE. Differential c-Fos expression in cholinergic, monoaminergic, and GABAergic cell groups of the pontomesencephalic tegmentum after paradoxical sleep deprivation and recovery. J Neurosci 1999;19:3057-72.
20. Rada P, Mark GP, Vitek MP, et al. Interleukin-1 beta decreases acetylcholine measured by microdialysis in the hippocampus of freely moving rats. Brain Res 1991;550:287-90.
21. Carmeliet P, Van DJ, Denef C. Interleukin-1 beta inhibits acetylcholine synthesis in the pituitary corticotropic cell line AtT20. Brain Res 1989;491:199-203.
22. Li Y, Liu L, Kang J, et al. Neuronal-glial interactions mediated by inter- interleukin- 1 enhance neuronal acetylcholinesterase activity and mRNA expression. J Neurosci 2000;20:149-55.
23. Arrigoni E, Rainnie DG, McCarley RW, Greene RW. Adenosine-mediated presynaptic modulation of glutamatergic transmission in the laterodorsal tegmentum. J Neurosci 2001;21:1076-85. (Pubitemid 32163149)
24. Ford B, Holmes CJ, Mainville L, Jones BE. GABAergic neurons in the rat pontomesencephalic tegmentum: codistribution with cholinergic and other tegmental neurons projecting to the posterior lateral hypothalamus. J Comp Neurol 1995;363:177-96.
25. Greene RW, Rainnie DG. Mechanisms affecting neuronal excitability in brainstem cholinergic centers and their impact on behavioral state. In: Lydic R, Baghdoyan HA, eds. Handbook of behavioral state control: cellular and molecular mechanisms. Boca Raton: CRC Press, 1999:277-96.
26. Williams JA, Reiner PB. Noradrenaline hyperpolarizes identified rat mesopontine cholinergic neurons in vitro. J Neurosci 1993;13:3878-83.
27. Paxinos G, Watson C. The rat brain in stereotaxic coordinates - fifth edition. Burlington, MA: Elsevier Academic Press, Inc., 2005.
28. Opp MR. Rat strain differences suggest a role for corticotropin-releasing hormone in modulating sleep. Physiol Behav 1997;63:67-74.
29. Manfridi A, Brambilla D, Bianchi S, Mariotti M, Opp MR, Imeri L. Interleukin-1beta enhances non-rapid eye movement sleep when microinjected into the dorsal raphe nucleus and inhibits serotonergic neurons in vitro. Eur J Neurosci 2003;18:1041-9.
30. Kamondi A, Williams JA, Hutcheon B, Reiner PB. Membrane properties of mesopontine cholinergic neurons studied with the whole-cell patchclamp technique: implications for behavioral state control. J Neurophysiol 1992;68:1359-72.
31. Kang Y, Kitai ST. Electrophysiological properties of pedunculopontine neurons and their postsynaptic responses following stimulation of substantia nigra reticulata. Brain Res 1990;535:79-95.
32. Leonard CS, Llinas R. Electrophysiology of mammalian peduncolopontine and laterodorsal tegmental neurons in vitro: implications for the control of REM sleep. In: Steriade M, Biesold D, eds. Brain cholinergic system. New York: Oxford University Press, 1990: 205-23.
33. Luebke JI, Greene RW, Semba K, Kamondi A, McCarley RW, Reiner PB. Serotonin hyperpolarizes cholinergic low-threshold burst neurons in the rat laterodorsal tegmental nucleus in vitro. Proc Natl Acad Sci U S A 1992;89:743-7.
34. Brambilla D, Chapman D, Greene R. Adenosine mediation of presynaptic feedback inhibition of glutamate release. Neuron 2005;46:275-83.
35. Brambilla D, Franciosi S, Opp MR, Imeri L. Interleukin-1 inhibits firing of serotonergic neurons in the dorsal raphe nucleus and enhances GABAergic inhibitory post-synaptic potentials. Eur J Neurosci 2007;26:1862-9.
36. Luk WP, Zhang Y, White TD, et al. Adenosine: a mediator of interleukin-1beta-induced hippocampal synaptic inhibition. J Neurosci 1999;19:4238-44.
37. Sperlagh B, Baranyi M, Hasko G, Vizi ES. Potent effect of interleukin-1 beta to evoke ATP and adenosine release from rat hippocampal slices. J Neuroimmunol 2004;151:33-39.
38. Zhu G, Okada M, Yoshida S, et al. Involvement of Ca(2+)-induced Ca2+ releasing system in interleukin-1beta-associated adenosine release. Eur J Pharmacol 2006;532:246-52.
39. Rainnie DG, Grunze HC, McCarley RW, Greene RW. Adenosine inhibition of mesopontine cholinergic neurons: implications for EEG arousal. Science 1994; 263:689-92.
40. Imeri L, Bianchi S, Mancia M. Muramyl dipeptide and IL-1 effects on sleep and brain temperature after inhibition of serotonin synthesis. Am J Physiol 1997;273:R1663-8.
41. Imeri L, Ceccarelli P, Mariotti M, Manfridi A, Opp MR, Mancia M. Sleep, but not febrile responses of Fisher 344 rats to immune challenge are affected by aging. Brain Behav Immun 2004;18:399-404.
42. Opp MR, Imeri L. Rat strains that differ in corticotropin-releasing hormone production exhibit different sleep-wake responses to interleukin 1. Neuroendocrinology 2001;73:272-84.
43. 14C]inulin in rat. Neuroscience 2000;95:577-92.
44. Schobitz B, De Kloet ER, Holsboer F. Gene expression and function of interleukin 1, interleukin 6 and tumor necrosis factor in the brain. Prog Neurobiol 1994;44:397-432.
45. Dinarello CA, Ikejima T, Warner SJ, et al. Interleukin 1 induces interleu- interleukin 1. I. Induction of circulating interleukin 1 in rabbits in vivo and in human mononuclear cells in vitro. J Immunol 1987;139:1902-10.
46. Taishi P, Churchill L, De A, Obal F Jr, Krueger JM. Cytokine mRNA induction by interleukin-1beta or tumor necrosis factor alfa in vitro and in vivo. Brain Res 2008;1226:89-98.
47. Lu J, Sherman D, Devor M, Saper CB. A putative flip-flop switch for control of REM sleep. Nature 2006;441:589-94.
48. De A, Churchill L, Obal F Jr, Simasko SM, Krueger JM. GHRH and IL- 1beta increase cytoplasmic Ca(2+) levels in cultured hypothalamic GABAergic neurons. Brain Res 2002;949:209-12.
49. Feleder C, Arias P, Refojo D, Nacht S, Moguilevsky J. Interleukin-1 inhibits NMDA-stimulated GnRH secretion: associated effects on the release of hypothalamic inhibitory amino acid neurotransmitters. Neuroimmunomodulation 2000;7:46-50. (Pubitemid 30012578)
50. Miller LG, Galpern WR, Dunlap K, Dinarello CA, Turner TJ. Interleukin-1 augments gamma-aminobutyric acidA receptor function in brain. Mol Pharmacol 1991;39:105-8.
51. Tabarean IV, Korn H, Bartfai T. Interleukin-1beta induces hyperpolarization and modulates synaptic inhibition in preoptic and anterior hypothalamic neurons. Neuroscience 2006;141:1685-95.
52. Zeise ML, Madamba S, Siggins GR. Interleukin-1 beta increases synaptic inhibition in rat hippocampal pyramidal neurons in vitro. Regul Pept 1992;39:1-7.
53. McGinty D, Szymusiak R, Thomson D. Preoptic/anterior hypothalamic warming increases EEG delta frequency activity within non-rapid eye movement sleep. Brain Res 1994; 667:273-7.
54. Szymusiak R, Satinoff E. Maximal REM sleep time defines a narrower thermoneutral zone than does minimal metabolic rate. Physiol Behav 1981;26:687-90.
55. Lin MT, Wang HC, Chandra A. The effects on thermoregulation of intracerebroventricular injections of acetylcholine, pilocarpine, physostigmine, atropine and hemicholinium in the rat. Neuropharmacology 1980;19:561-5.
56. Rodrigues AG, Lima NR, Coimbra CC, Marubayashi U. Intracerebroventricular physostigmine facilitates heat loss mechanisms in running rats. J Appl Physiol 2004;97:333-8.
57. Imeri L, Bianchi S, Angeli P, Mancia M. Stimulation of cholinergic receptors in the medial preoptic area affects sleep and cortical temperature. Am J Physiol 1995;269:R294-9.
58. Kirkpatrick WE, Lomax P. Temperature changes following iontophoretic injection of acetylcholine into the rostral hypothalamus of the rat. Neuropharmacology 1970;9:195-202.
59. Mallick BN, Joseph MM. Role of cholinergic inputs to the medial preoptic area in regulation of sleep-wakefulness and body temperature in freely moving rats. Brain Res 1997;750:311-7.
60. Poole S, Stephenson JD. Effects of noradrenaline and carbachol on temperature regulation of rats. Br J Pharmacol 1979;65:43-51. (Pubitemid 9080695)
61. Takahashi A, Kishi E, Ishimaru H, Ikarashi Y, Maruyama Y. Role of preoptic and anterior hypothalamic cholinergic input on water intake and body temperature. Brain Res 2001;889:191-9.
62. Imeri L, Bianchi S, Angeli P, Mancia M. Muscarinic receptor subtypes in the medial preoptic area and sleep-wake cycles. Neuroreport 1996;7:417-20. (Pubitemid 126830277)
63. Chiba T, Murata Y. Afferent and efferent connections of the medial preoptic area in the rat: a WGA-HRP study. Brain Res Bull 1985;14:261-72.
64. Parmeggiani PL. Thermoregulation and sleep. Front Biosci 2003;8:s557-67.
65. Dinarello CA. Blocking IL-1 in systemic inflammation. J Exp Med 2005;201:1355-9.