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. 1990 Mar-Apr;63(2):157–172.

Somnogenic cytokines and models concerning their effects on sleep.

J M Krueger 1, F Obal Jr 1, M Opp 1, L Toth 1, L Johannsen 1, A B Cady 1
PMCID: PMC2589298  PMID: 2205056

Abstract

All the sleep-promoting substances currently identified also have other biological activities. Despite years of effort, a single specific central nervous system sleep center has not been described. These observations led us to propose a biochemical model of a sleep activational system in which the effects of several sleep factors are integrated into a regulatory scheme. These sleep factors interact by altering the metabolism, production, or activity of each other and thereby result in multiple feedback loops. This web of interactions leads to sleep stability in that minor challenges to the system will not greatly alter sleep. The system, however, is responsive to strong perturbations, such as sleep deprivation and infectious disease. The sleep-promoting effects of cytokines and their interactions with prostaglandins and the neuroendocrine system are used to illustrate the functioning of a part of the sleep activational system under normal conditions and during infectious disease. Although the actions of individuals sleep factors are not specific to sleep, their interactions at various levels of the neuraxis can mediate a specific sleep response. Such a system would also be responsive to the autonomic and environmental parameters that alter sleep.

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Selected References

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  1. Berkenbosch F., van Oers J., del Rey A., Tilders F., Besedovsky H. Corticotropin-releasing factor-producing neurons in the rat activated by interleukin-1. Science. 1987 Oct 23;238(4826):524–526. doi: 10.1126/science.2443979. [DOI] [PubMed] [Google Scholar]
  2. Bernton E. W., Beach J. E., Holaday J. W., Smallridge R. C., Fein H. G. Release of multiple hormones by a direct action of interleukin-1 on pituitary cells. Science. 1987 Oct 23;238(4826):519–521. doi: 10.1126/science.2821620. [DOI] [PubMed] [Google Scholar]
  3. Borbély A. A. A two process model of sleep regulation. Hum Neurobiol. 1982;1(3):195–204. [PubMed] [Google Scholar]
  4. Breder C. D., Dinarello C. A., Saper C. B. Interleukin-1 immunoreactive innervation of the human hypothalamus. Science. 1988 Apr 15;240(4850):321–324. doi: 10.1126/science.3258444. [DOI] [PubMed] [Google Scholar]
  5. Cady A. B., Kotani S., Shiba T., Kusumoto S., Krueger J. M. Somnogenic activities of synthetic lipid A. Infect Immun. 1989 Feb;57(2):396–403. doi: 10.1128/iai.57.2.396-403.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chastrette N., Cespuglio R. Influence of proopiomelanocortin-derived peptides on the sleep-waking cycle of the rat. Neurosci Lett. 1985 Dec 18;62(3):365–370. doi: 10.1016/0304-3940(85)90576-2. [DOI] [PubMed] [Google Scholar]
  7. Danguir J. Intracerebroventricular infusion of somatostatin selectively increases paradoxical sleep in rats. Brain Res. 1986 Mar 5;367(1-2):26–30. doi: 10.1016/0006-8993(86)91574-x. [DOI] [PubMed] [Google Scholar]
  8. Danguir J., Nicolaidis S. Chronic intracerebroventricular infusion of insulin causes selective increase of slow wave sleep in rats. Brain Res. 1984 Jul 23;306(1-2):97–103. doi: 10.1016/0006-8993(84)90359-7. [DOI] [PubMed] [Google Scholar]
  9. Dinarello C. A. An update on human interleukin-1: from molecular biology to clinical relevance. J Clin Immunol. 1985 Sep;5(5):287–297. doi: 10.1007/BF00918247. [DOI] [PubMed] [Google Scholar]
  10. Dinarello C. A., Bernheim H. A. Ability of human leukocytic pyrogen to stimulate brain prostaglandin synthesis in vitro. J Neurochem. 1981 Sep;37(3):702–708. doi: 10.1111/j.1471-4159.1982.tb12544.x. [DOI] [PubMed] [Google Scholar]
  11. Dinarello C. A., Bernheim H. A., Duff G. W., Le H. V., Nagabhushan T. L., Hamilton N. C., Coceani F. Mechanisms of fever induced by recombinant human interferon. J Clin Invest. 1984 Sep;74(3):906–913. doi: 10.1172/JCI111508. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dinarello C. A. Biology of interleukin 1. FASEB J. 1988 Feb;2(2):108–115. [PubMed] [Google Scholar]
  13. Dinarello C. A., Cannon J. G., Wolff S. M., Bernheim H. A., Beutler B., Cerami A., Figari I. S., Palladino M. A., Jr, O'Connor J. V. Tumor necrosis factor (cachectin) is an endogenous pyrogen and induces production of interleukin 1. J Exp Med. 1986 Jun 1;163(6):1433–1450. doi: 10.1084/jem.163.6.1433. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dinarello C. A. Interleukin-1. Rev Infect Dis. 1984 Jan-Feb;6(1):51–95. doi: 10.1093/clinids/6.1.51. [DOI] [PubMed] [Google Scholar]
  15. Dinarello C. A. Interleukin-1: amino acid sequences, multiple biological activities and comparison with tumor necrosis factor (cachectin). Year Immunol. 1986;2:68–89. [PubMed] [Google Scholar]
  16. Drucker-Colín R. R., Spanis C. W., Hunyadi J., Sassin J. F., McGaugh J. L. Growth hormone effects on sleep and wakefulness in the rat. Neuroendocrinology. 1975;18(1):1–8. doi: 10.1159/000122377. [DOI] [PubMed] [Google Scholar]
  17. Drucker-Colín R., Bernal-Pedraza J., Fernández-Cancino F., Oksenberg A. Is vasoactive intestinal polypeptide (VIP) a sleep factor? Peptides. 1984 Jul-Aug;5(4):837–840. doi: 10.1016/0196-9781(84)90032-9. [DOI] [PubMed] [Google Scholar]
  18. Ehlers C. L., Reed T. K., Henriksen S. J. Effects of corticotropin-releasing factor and growth hormone-releasing factor on sleep and activity in rats. Neuroendocrinology. 1986;42(6):467–474. doi: 10.1159/000124489. [DOI] [PubMed] [Google Scholar]
  19. Endres S., Ghorbani R., Lonnemann G., van der Meer J. W., Dinarello C. A. Measurement of immunoreactive interleukin-1 beta from human mononuclear cells: optimization of recovery, intrasubject consistency, and comparison with interleukin-1 alpha and tumor necrosis factor. Clin Immunol Immunopathol. 1988 Dec;49(3):424–438. doi: 10.1016/0090-1229(88)90130-4. [DOI] [PubMed] [Google Scholar]
  20. Farrar W. L., Hill J. M., Harel-Bellan A., Vinocour M. The immune logical brain. Immunol Rev. 1987 Dec;100:361–378. doi: 10.1111/j.1600-065x.1987.tb00539.x. [DOI] [PubMed] [Google Scholar]
  21. Farrar W. L., Kilian P. L., Ruff M. R., Hill J. M., Pert C. B. Visualization and characterization of interleukin 1 receptors in brain. J Immunol. 1987 Jul 15;139(2):459–463. [PubMed] [Google Scholar]
  22. Fontana A., Kristensen F., Dubs R., Gemsa D., Weber E. Production of prostaglandin E and an interleukin-1 like factor by cultured astrocytes and C6 glioma cells. J Immunol. 1982 Dec;129(6):2413–2419. [PubMed] [Google Scholar]
  23. Gauldie J., Lamontagne L., Stadnyk A. Acute phase response in infectious disease. Surv Synth Pathol Res. 1985;4(2):126–151. doi: 10.1159/000156970. [DOI] [PubMed] [Google Scholar]
  24. Gillin J. C., Jacobs L. S., Fram D. H., Snyder F. Acute effect of a glucocorticoid on normal human sleep. Nature. 1972 Jun 16;237(5355):398–399. doi: 10.1038/237398a0. [DOI] [PubMed] [Google Scholar]
  25. Golstein J., Van Cauter E., Désir D., Noël P., Spire J. P., Refetoff S., Copinschi G. Effects of "jet lag" on hormonal patterns. IV. Time shifts increase growth hormone release. J Clin Endocrinol Metab. 1983 Mar;56(3):433–440. doi: 10.1210/jcem-56-3-433. [DOI] [PubMed] [Google Scholar]
  26. Graf M. V., Kastin A. J. Delta-sleep-inducing peptide (DSIP): a review. Neurosci Biobehav Rev. 1984 Spring;8(1):83–93. doi: 10.1016/0149-7634(84)90022-8. [DOI] [PubMed] [Google Scholar]
  27. Graf M. V., Kastin A. J. Delta-sleep-inducing peptide (DSIP): an update. Peptides. 1986 Nov-Dec;7(6):1165–1187. doi: 10.1016/0196-9781(86)90148-8. [DOI] [PubMed] [Google Scholar]
  28. Haq A. U., Maca R. D. Role of IFN-gamma and alpha in IL 1 synthesis and secretion of in vitro differentiated human macrophages: a comparative study. Immunobiology. 1986 Jul;171(4-5):451–460. doi: 10.1016/s0171-2985(86)80076-6. [DOI] [PubMed] [Google Scholar]
  29. Hayaishi O. Sleep-wake regulation by prostaglandins D2 and E2. J Biol Chem. 1988 Oct 15;263(29):14593–14596. [PubMed] [Google Scholar]
  30. Helle M., Brakenhoff J. P., De Groot E. R., Aarden L. A. Interleukin 6 is involved in interleukin 1-induced activities. Eur J Immunol. 1988 Jun;18(6):957–959. doi: 10.1002/eji.1830180619. [DOI] [PubMed] [Google Scholar]
  31. Inoué S., Honda K., Komoda Y., Uchizono K., Ueno R., Hayaishi O. Differential sleep-promoting effects of five sleep substances nocturnally infused in unrestrained rats. Proc Natl Acad Sci U S A. 1984 Oct;81(19):6240–6244. doi: 10.1073/pnas.81.19.6240. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Kaji H., Chihara K., Abe H., Kita T., Kashio Y., Okimura Y., Fujita T. Effect of passive immunization with antisera to vasoactive intestinal polypeptide and peptide histidine isoleucine amide on 5-hydroxy-L-tryptophan-induced prolactin release in rats. Endocrinology. 1985 Nov;117(5):1914–1919. doi: 10.1210/endo-117-5-1914. [DOI] [PubMed] [Google Scholar]
  33. Kapás L., Obál F., Jr, Alföldi P., Rubicsek G., Penke B., Obál F. Effects of nocturnal intraperitoneal administration of cholecystokinin in rats: simultaneous increase in sleep, increase in EEG slow-wave activity, reduction of motor activity, suppression of eating, and decrease in brain temperature. Brain Res. 1988 Jan 12;438(1-2):155–164. doi: 10.1016/0006-8993(88)91334-0. [DOI] [PubMed] [Google Scholar]
  34. Koella W. P. The organization and regulation of sleep. A review of the experimental evidence and a novel integrated model of the organizing and regulating apparatus. Experientia. 1984 Apr 15;40(4):309–338. doi: 10.1007/BF01952538. [DOI] [PubMed] [Google Scholar]
  35. Krueger J. M., Dinarello C. A., Shoham S., Davenne D., Walter J., Kubillus S. Interferon alpha-2 enhances slow-wave sleep in rabbits. Int J Immunopharmacol. 1987;9(1):23–30. doi: 10.1016/0192-0561(87)90107-x. [DOI] [PubMed] [Google Scholar]
  36. Krueger J. M., Kubillus S., Shoham S., Davenne D. Enhancement of slow-wave sleep by endotoxin and lipid A. Am J Physiol. 1986 Sep;251(3 Pt 2):R591–R597. doi: 10.1152/ajpregu.1986.251.3.R591. [DOI] [PubMed] [Google Scholar]
  37. Krueger J. M., Majde J. A., Blatteis C. M., Endsley J., Ahokas R. A., Cady A. B. Polyriboinosinic:polyribocytidylic acid enhances rabbit slow-wave sleep. Am J Physiol. 1988 Nov;255(5 Pt 2):R748–R755. doi: 10.1152/ajpregu.1988.255.5.R748. [DOI] [PubMed] [Google Scholar]
  38. Krueger J. M., Pappenheimer J. R., Karnovsky M. L. Sleep-promoting effects of muramyl peptides. Proc Natl Acad Sci U S A. 1982 Oct;79(19):6102–6106. doi: 10.1073/pnas.79.19.6102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Krueger J. M., Pappenheimer J. R., Karnovsky M. L. The composition of sleep-promoting factor isolated from human urine. J Biol Chem. 1982 Feb 25;257(4):1664–1669. [PubMed] [Google Scholar]
  40. Krueger J. M., Walter J., Dinarello C. A., Wolff S. M., Chedid L. Sleep-promoting effects of endogenous pyrogen (interleukin-1). Am J Physiol. 1984 Jun;246(6 Pt 2):R994–R999. doi: 10.1152/ajpregu.1984.246.6.R994. [DOI] [PubMed] [Google Scholar]
  41. Kruisbrink J., Mirmiran M., Van der Woude T. P., Boer G. J. Effects of enhanced cerebrospinal fluid levels of vasopressin, vasopressin antagonist or vasoactive intestinal polypeptide on circadian sleep-wake rhythm in the rat. Brain Res. 1987 Sep 1;419(1-2):76–86. doi: 10.1016/0006-8993(87)90570-1. [DOI] [PubMed] [Google Scholar]
  42. Lumpkin M. D. The regulation of ACTH secretion by IL-1. Science. 1987 Oct 23;238(4826):452–454. doi: 10.1126/science.2821618. [DOI] [PubMed] [Google Scholar]
  43. Mansbach R. S., Lorenz D. N. Cholecystokinin (CCK-8) elicits prandial sleep in rats. Physiol Behav. 1983 Feb;30(2):179–183. doi: 10.1016/0031-9384(83)90002-1. [DOI] [PubMed] [Google Scholar]
  44. Matsumura H., Goh Y., Ueno R., Sakai T., Hayaishi O. Awaking effect of PGE2 microinjected into the preoptic area of rats. Brain Res. 1988 Mar 22;444(2):265–272. doi: 10.1016/0006-8993(88)90935-3. [DOI] [PubMed] [Google Scholar]
  45. McCann S. M., Ono N., Khorram O., Kentroti S., Aguila C. The role of brain peptides in neuroimmunomodulation. Ann N Y Acad Sci. 1987;496:173–181. doi: 10.1111/j.1749-6632.1987.tb35763.x. [DOI] [PubMed] [Google Scholar]
  46. Mendelson W. B., Slater S., Gold P., Gillin J. C. The effect of growth hormone administration on human sleep: a dose-response study. Biol Psychiatry. 1980 Aug;15(4):613–618. [PubMed] [Google Scholar]
  47. Mitsugi N., Kimura F. Simultaneous determination of blood levels of corticosterone and growth hormone in the male rat: relation to sleep-wakefulness cycle. Neuroendocrinology. 1985 Aug;41(2):125–130. doi: 10.1159/000124165. [DOI] [PubMed] [Google Scholar]
  48. Moldofsky H., Lue F. A., Eisen J., Keystone E., Gorczynski R. M. The relationship of interleukin-1 and immune functions to sleep in humans. Psychosom Med. 1986 May-Jun;48(5):309–318. doi: 10.1097/00006842-198605000-00001. [DOI] [PubMed] [Google Scholar]
  49. Nisticò G., De Sarro G. B., Bagetta G., Müller E. E. Behavioural and electrocortical spectrum power effects of growth hormone releasing factor in rats. Neuropharmacology. 1987 Jan;26(1):75–78. doi: 10.1016/0028-3908(87)90047-5. [DOI] [PubMed] [Google Scholar]
  50. Obal F., Jr, Alföldi P., Cady A. B., Johannsen L., Sary G., Krueger J. M. Growth hormone-releasing factor enhances sleep in rats and rabbits. Am J Physiol. 1988 Aug;255(2 Pt 2):R310–R316. doi: 10.1152/ajpregu.1988.255.2.R310. [DOI] [PubMed] [Google Scholar]
  51. Obal F., Jr, Opp M., Cady A. B., Johannsen L., Krueger J. M. Prolactin, vasoactive intestinal peptide, and peptide histidine methionine elicit selective increases in REM sleep in rabbits. Brain Res. 1989 Jun 26;490(2):292–300. doi: 10.1016/0006-8993(89)90246-1. [DOI] [PubMed] [Google Scholar]
  52. Obál F., Jr Effects of peptides (DSIP, DSIP analogues, VIP, GRF and CCK) on sleep in the rat. Clin Neuropharmacol. 1986;9 (Suppl 4):459–461. [PubMed] [Google Scholar]
  53. Obál F., Jr, Kovalzon V. M., Kalikhevich V. N., Török A., Alföldi P., Sáry G., Hajós M., Penke B. Structure-activity relationship in the effects of delta-sleep-inducing peptide (DSIP) on rat sleep. Pharmacol Biochem Behav. 1986 Apr;24(4):889–894. doi: 10.1016/0091-3057(86)90432-6. [DOI] [PubMed] [Google Scholar]
  54. Obál F., Jr, Rubicsek G., Alföldi P., Sáry G., Obál F. Changes in the brain and core temperatures in relation to the various arousal states in rats in the light and dark periods of the day. Pflugers Arch. 1985 May;404(1):73–79. doi: 10.1007/BF00581494. [DOI] [PubMed] [Google Scholar]
  55. Obál F., Jr, Sáry G., Alföldi P., Rubicsek G., Obál F. Vasoactive intestinal polypeptide promotes sleep without effects on brain temperature in rats at night. Neurosci Lett. 1986 Feb 28;64(2):236–240. doi: 10.1016/0304-3940(86)90107-2. [DOI] [PubMed] [Google Scholar]
  56. Opp M. R., Obál F., Jr, Krueger J. M. Effects of alpha-MSH on sleep, behavior, and brain temperature: interactions with IL 1. Am J Physiol. 1988 Dec;255(6 Pt 2):R914–R922. doi: 10.1152/ajpregu.1988.255.6.R914. [DOI] [PubMed] [Google Scholar]
  57. Opp M., Obal F., Jr, Cady A. B., Johannsen L., Krueger J. M. Interleukin-6 is pyrogenic but not somnogenic. Physiol Behav. 1989 May;45(5):1069–1072. doi: 10.1016/0031-9384(89)90239-4. [DOI] [PubMed] [Google Scholar]
  58. Opp M., Obál F., Jr, Krueger J. M. Corticotropin-releasing factor attenuates interleukin 1-induced sleep and fever in rabbits. Am J Physiol. 1989 Sep;257(3 Pt 2):R528–R535. doi: 10.1152/ajpregu.1989.257.3.R528. [DOI] [PubMed] [Google Scholar]
  59. Pappenheimer J. R., Koski G., Fencl V., Karnovsky M. L., Krueger J. Extraction of sleep-promoting factor S from cerebrospinal fluid and from brains of sleep-deprived animals. J Neurophysiol. 1975 Nov;38(6):1299–1311. doi: 10.1152/jn.1975.38.6.1299. [DOI] [PubMed] [Google Scholar]
  60. Pappenheimer J. R., Miller T. B., Goodrich C. A. Sleep-promoting effects of cerebrospinal fluid from sleep-deprived goats. Proc Natl Acad Sci U S A. 1967 Aug;58(2):513–517. doi: 10.1073/pnas.58.2.513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Pavel S., Goldstein R., Petrescu M., Popa M. REM sleep induction in prepubertal boys by vasotocin: evidence for the involvement of serotonin containing neurons. Peptides. 1981 Fall;2(3):245–250. doi: 10.1016/s0196-9781(81)80113-1. [DOI] [PubMed] [Google Scholar]
  62. Pavel S., Psatta D., Goldstein R. Slow-wave sleep induced in cats by extremely small amounts of synthetic and pineal vasotocin injected into the third ventricle of the brain. Brain Res Bull. 1977 Jul-Aug;2(4):251–254. doi: 10.1016/0361-9230(77)90080-6. [DOI] [PubMed] [Google Scholar]
  63. Radulovacki M., Virus R. M., Djuricic-Nedelson M., Green R. D. Adenosine analogs and sleep in rats. J Pharmacol Exp Ther. 1984 Feb;228(2):268–274. [PubMed] [Google Scholar]
  64. Rettori V., Jurcovicova J., McCann S. M. Central action of interleukin-1 in altering the release of TSH, growth hormone, and prolactin in the male rat. J Neurosci Res. 1987;18(1):179–183. doi: 10.1002/jnr.490180125. [DOI] [PubMed] [Google Scholar]
  65. Roszman T. L., Jackson J. C., Cross R. J., Titus M. J., Markesbery W. R., Brooks W. H. Neuroanatomic and neurotransmitter influences on immune function. J Immunol. 1985 Aug;135(2 Suppl):769s–772s. [PubMed] [Google Scholar]
  66. Sapolsky R., Rivier C., Yamamoto G., Plotsky P., Vale W. Interleukin-1 stimulates the secretion of hypothalamic corticotropin-releasing factor. Science. 1987 Oct 23;238(4826):522–524. doi: 10.1126/science.2821621. [DOI] [PubMed] [Google Scholar]
  67. Sassin J. F., Parker D. C., Mace J. W., Gotlin R. W., Johnson L. C., Rossman L. G. Human growth hormone release: relation to slow-wave sleep and sleep-walking cycles. Science. 1969 Aug 1;165(3892):513–515. doi: 10.1126/science.165.3892.513. [DOI] [PubMed] [Google Scholar]
  68. Schoenenberger G. A., Maier P. F., Tobler H. J., Wilson K., Monnier M. The delta EEG (sleep)-inducing peptide (DSIP). XI. Amino-acid analysis, sequence, synthesis and activity of the nonapeptide. Pflugers Arch. 1978 Sep 6;376(2):119–129. doi: 10.1007/BF00581575. [DOI] [PubMed] [Google Scholar]
  69. Shoham S., Davenne D., Cady A. B., Dinarello C. A., Krueger J. M. Recombinant tumor necrosis factor and interleukin 1 enhance slow-wave sleep. Am J Physiol. 1987 Jul;253(1 Pt 2):R142–R149. doi: 10.1152/ajpregu.1987.253.1.R142. [DOI] [PubMed] [Google Scholar]
  70. Shoham S., Krueger J. M. Muramyl dipeptide-induced sleep and fever: effects of ambient temperature and time of injections. Am J Physiol. 1988 Jul;255(1 Pt 2):R157–R165. doi: 10.1152/ajpregu.1988.255.1.R157. [DOI] [PubMed] [Google Scholar]
  71. Stern W. C., Jalowiec J. E., Shabshelowitz H., Morgane P. J. Effects of growth hormone on sleep-waking patterns in cats. Horm Behav. 1975 Jun;6(2):189–196. doi: 10.1016/0018-506x(75)90035-5. [DOI] [PubMed] [Google Scholar]
  72. Torii S., Mitsumori K., Inubushi S., Yanagisawa I. The REM sleep-inducing action of a naturally occurring organic bromine compound in the encéphale isolé cat. Psychopharmacologia. 1973 Feb 27;29(1):65–75. doi: 10.1007/BF00421212. [DOI] [PubMed] [Google Scholar]
  73. Toth L. A., Krueger J. M. Alteration of sleep in rabbits by Staphylococcus aureus infection. Infect Immun. 1988 Jul;56(7):1785–1791. doi: 10.1128/iai.56.7.1785-1791.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Toth L. A., Krueger J. M. Effects of microbial challenge on sleep in rabbits. FASEB J. 1989 Jul;3(9):2062–2066. doi: 10.1096/fasebj.3.9.2663582. [DOI] [PubMed] [Google Scholar]
  75. Ueno R., Honda K., Inoué S., Hayaishi O. Prostaglandin D2, a cerebral sleep-inducing substance in rats. Proc Natl Acad Sci U S A. 1983 Mar;80(6):1735–1737. doi: 10.1073/pnas.80.6.1735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Vermeulen M. W., Gray G. R. Processing of Bacillus subtilis peptidoglycan by a mouse macrophage cell line. Infect Immun. 1984 Nov;46(2):476–483. doi: 10.1128/iai.46.2.476-483.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Weitzman E. D., Nogeire C., Perlow M., Fukushima D., Sassin J., McGregor P., Hellman L. Effects of a prolonged 3-hour sleep-wake cycle on sleep stages, plasma cortisol, growth hormone and body temperature in man. J Clin Endocrinol Metab. 1974 Jun;38(6):1018–1030. doi: 10.1210/jcem-38-6-1018. [DOI] [PubMed] [Google Scholar]
  78. Zini I., Merlo Pich E., Fuxe K., Lenzi P. L., Agnati L. F., Härfstrand A., Mutt V., Tatemoto K., Moscara M. Actions of centrally administered neuropeptide Y on EEG activity in different rat strains and in different phases of their circadian cycle. Acta Physiol Scand. 1984 Sep;122(1):71–77. doi: 10.1111/j.1748-1716.1984.tb07483.x. [DOI] [PubMed] [Google Scholar]

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