Neuroscience and Behavioral Physiology

, Volume 39, Issue 3, pp 289–296 | Cite as

Microinjection of 70-kDal heat shock protein into the oral reticular nucleus of the pons suppresses rapid eye movement sleep in pigeons

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Previous studies have demonstrated that increases in the duration of slow-wave sleep and decreases in somatovisceral measures in response to microinjections of 70-kDal heat shock protein (Hsp70) into the third ventricle in pigeons may be due to activation of GABAA receptors in the preoptic area of the hypothalamus. With the aim of identifying the transmitter mechanisms whose activation is temporally (2–3 h) linked with suppression of rapid eye movement sleep, the present studies were based on injection of Hsp70 into the oral reticular pontine nucleus (nucleus reticularis pontis oralis, NRPO), whose cholinergic neurons are critical for generating rapid eye movement sleep. Hsp70 was found to induce earlier (within the first 2 h) decreases in the number of episodes and the total duration of rapid eye movement sleep, with decreases in electroencephalogram (EEG) spectral power in the range 9–14 Hz, the level of muscle contractile activity, and brain temperature. It is hypothesized that the effects of Hsp70 are mediated by activation of GABAA receptors in the NRPO, evoking suppression of the cholinergic mechanisms initiating rapid eye movement sleep. The increase in the total duration of slow-wave sleep occurring with a long latent period (8–12 h after injection of Hsp70 into the NRPO) may be due to the influence of Hsp70 on the population of neurons responsible for maintaining slow-wave sleep outside the NRPO.

KEY WORDS

rapid eye movement sleep slow-wave sleep 70-kDal heat shock protein nucleus reticularis pontis oralis (oral reticular nucleus of the pons) pigeons 
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References

  1. 1.
    E. A. Gusel'nikova, I. V. Ekimova, and Yu. F. Pastukhov, “Microinjection of carbachol in the reticular formation of the midbrain evokes dose-dependent increases in paradoxical sleep or waking in pigeons,” Psikhofarmakol. Biologich. Narkol., No. 3–4, 385–386 (2002).Google Scholar
  2. 2.
    E. A. Gusel'nikova, “Effects of microinjections of carbachol into the reticular formation of the midbrain on measures of rapid sleep in the pigeon Columba livia,” Zh. Évolyuts. Biokhim. Fiziol., 43, No. 4, 369–371 (2007).Google Scholar
  3. 3.
    I. V. Ekimova and Yu. F. Pastukhov, “The GABAergic system of the midbrain is involved in controlling sleep and temperature homeostasis in pigeons,” Dokl. Ros. Akad. Nauk, 387, No. 1, 121–124 (2002).Google Scholar
  4. 4.
    I. V. Ekimova, “Thermoregulation in the pigeon Columba livia in stress evoked by food deprivation,” Zh. Évolyuts. Biokhim. Fiziol., 41, No. 1, 62–68 (2005).Google Scholar
  5. 5.
    I. V. Ekimova and Yu. F. Pastukhov, “Involvement of GABAergic mechanisms of the ventrolateral preoptic area of the hypothalamus in controlling sleep and waking states and temperature homeostasis in the pigeon Columba livia,” Zh. Évolyuts. Biokhim. Fiziol., 41, No. 4, 356–363 (2005).Google Scholar
  6. 6.
    V. M. Kovalzon, Yu. F. Pastukhov, and L. M. Mukhametov, “Comparative physiology of sleep in mammals,” Fiziol. Chel. Zhivot., 31, 65–78 (1986).Google Scholar
  7. 7.
    T. G. Komarova, I. V. Ekimov, and Yu. F. Pastukhov, “The role of cholinergic mechanisms of the ventrolateral preoptic area of the hypothalamus in controlling sleep and waking states in pigeons,” Ros. Fiziol. Zh. im. I. M. Sechenova, 93, No. 2, 189–200 (2007).Google Scholar
  8. 8.
    T. G. Komarova, I. V. Ekimova, and Yu. F. Pastukhov, “Involvement of muscarinic and nicotinic cholinoreceptors in the ventrolateral preoptic part of the hypothalamus in controlling thermoregulation and waking and sleep states in the pigeon Columba Livia,” Zh. Évolyuts. Biokhim. Fiziol., 43, No. 3, 332–336 (2007).Google Scholar
  9. 9.
    G. A. Merkulov, Pathological Histological Techniques [in Russian], Leningrad (1961).Google Scholar
  10. 10.
    Yu. F. Pastukhov, “Paradoxical sleep as a measure of different types of hypometabolism in mammals and birds,” Dokl. Ros. Akad. Nauk, 358, No. 1, 131–133 (1998).Google Scholar
  11. 11.
    Yu. F. Pastukhov, I. V. Ekimova, A. D. Nozdrachev, E. A. Guselnikova, E. L. Sedunova, and A. L. Zimin, “The state of sleep makes a significant contribution to both ‘cooling’ and ‘heating’ of the brain during the dark phase of the day in pigeons,” Dokl. Ros. Akad. Nauk, 376, No. 6, 836–840 (2001).Google Scholar
  12. 12.
    Yu. F. Pastukhov, I. V. Ekimova, and I. V. Guzhova, “Basic stress protein has a pyrogenic action,” Dokl. Ros. Akad. Nauk, 388, No. 6, 837–841 (2003).Google Scholar
  13. 13.
    Yu. F. Pastukhov, I. V. Ekimova, I. V. Guzhova, and K. A. Khudik, “Integrative mechanisms of the pyrogenic and somnogenic effects of 70-kDal heat shock protein: a hypothesis,” in: Problems in the Integration of Functions in Physiology and Medicine [in Russian], Moscow, PChUP Biznesofset, pp. 291–198 (2004).Google Scholar
  14. 14.
    Yu. F. Pastukhov and I. V. Ekimova, “Molecular, cellular and systems mechanisms of the protective function of 70-kDal heat shock protein,” Neironauka, 2, No. 2, 3–25 (2005).Google Scholar
  15. 15.
    Yu. F. Pastukhov, I. V. Ekimova, K. A. Khudik, and I. V. Guzhova, “Lipopolysaccharide-free 70-kDal heat shock protein has hypothermic and somnogenic actions,” Dokl. Ros. Akad. Nauk, 402, No. 2, 275–278 (2005).Google Scholar
  16. 16.
    Yu. F. Pastukhov, I. V. Ekimova, K. A. Khudik, and I. V. Guzhova, “70-kDal protein in the control of sleep and thermoregulation,” Zh. Évolyuts. Biokhim. Fiziol., (in press) (2007).Google Scholar
  17. 17.
    E. V. Sedunova, “Temperature homeostasis and its regulation in the birds class,” Zh. Évolyuts. Biokhim. Fiziol., 32, No. 2, 129–140 (1996).Google Scholar
  18. 18.
    D. A. Bechtold, S. J. Rush, and I. R. Brown, “Localization of the heat-shock protein Hsp70 to the synapse following hyperthermic stress in the brain,” J. Neurochem., 74, 641–646 (2000).PubMedCrossRefGoogle Scholar
  19. 19.
    P. Bourgin, P. Escourrou, C. Gaultier, and J. Adrien, “Induction of rapid eye movement sleep by carbachol infusion into the pontine reticular formation in the rat,” Neuroreport, 6, No. 3, 532–536 (1995).PubMedCrossRefGoogle Scholar
  20. 20.
    P. Franken, D. Dijk, I. Tobler, and A. Borbely, “Sleep deprivation in rats: effects on EEG power spectra, vigilance states, and cortical temperature,” Amer. J. Physiol., 261, No. 1–2, 198–208 (1991).Google Scholar
  21. 21.
    I. V. Guzhova, A. C. Arnholdt, Z. A. Darieva, A. V. Kinev, E. B. Lasunskaia, K. Nilsson, V. M. Bozhkov, A. P. Voronin, and B. Margulis, “Effects of exogenous stress protein 70 on the functional properties of human promonocytes through binding to cell surface and internalization,” Cell Stress Chaperones, 31, 67–77 (1998).CrossRefGoogle Scholar
  22. 22.
    B. E. Jones, “Paradoxical REM sleep promoting and permitting neuronal networks,” Arch. Ital. Biol., 142, No. 4, 379–396 (2004).PubMedGoogle Scholar
  23. 23.
    H. J. Karten and W. Hodos, A Stereotaxic Atlas of the Brain of the Pigeon (Columba livia), Johns Hopkins Press, Maryland (1967).Google Scholar
  24. 24.
    J. D. Kelty, P. A. Noseworthy, M. E. Feder, R. M. Robertson, and J.-M. Ramirez, “Thermal preconditioning and heat-shock protein 72 preserve synaptic transmission during thermal stress,” J. Neurosci., 22, RC193, 1–6 (2002).Google Scholar
  25. 25.
    G. G. Kinney, G. W. Vogel, and P. Feng, “Brainstem carbachol injections in the urethane anesthetized rat produce hippocampal theta rhythm and cortical desynchronization: a comparison of pedunculopontine tegmental versus nucleus pontis oralis injections,” Brain Res., 809, No. 2, 307–313 (1998).PubMedCrossRefGoogle Scholar
  26. 26.
    M. E. Rashotte, Iu. F. Pastukhov, E. L. Poliakov, and R. P. Henderson, “Vigilance states and body temperature during the circadian cycle in fed and fasted pigeons (Columba livia),” Amer. J. Physiol., 275, No. 5, 1690–1702 (1998).Google Scholar
  27. 27.
    A. Rechtschaffen, “Current perspectives on the function of sleep,” Perspect. Biol. Med., 41, 359–390 (1998).PubMedGoogle Scholar
  28. 28.
    C. B. Saper, T. E. Scammell, and J. Lu, “Hypothalamic regulation of sleep and circadian rhythms,” Nature, 437, 1257–1263 (2005).PubMedCrossRefGoogle Scholar
  29. 29.
    J. M. Siegel, “Brainstem mechanisms generating REM sleep,” in: Principles and Practice of Sleep Medicine, Saunders, New York (2000), pp. 132–143.Google Scholar
  30. 30.
    D. Stenberg, “Neuroanatomy and neurochemistry of sleep,” Cell. Mol. Life Sci., 64, No. 10, 1187–1204 (2007).PubMedCrossRefGoogle Scholar
  31. 31.
    D. Tanase, H. Baghdoyan, and R. Lydic, “Dialysis delivery of an adenosine Al receptor agonist to the pontine reticular formation decreases acetylcholine release and increases anesthesia recovery time,” Anesthesiology, 98, No. 4, 912–929 (2003).PubMedCrossRefGoogle Scholar
  32. 32.
    A. Terao, M. A. Greco, R. W. Davis, H. C. Heller, and T. S. Kilduff, “Region-specific changes in immediate early gene expression in response to sleep deprivation and recovery sleep in the mouse brain,” Neurosci., 4, No. 120, 1115–1124 (2003).CrossRefGoogle Scholar
  33. 33.
    I. Kobler, C. Kopp, T. Deboer, and U. Rudolph, “Diazepam-induced changes in sleep: role of the αlGABAA receptor subtype,” Pharmacology, 98, No. 11, 6464–6469 (2001).Google Scholar
  34. 34.
    J. Vazquez and H. A. Baghdoyan, “GABAA receptors inhibit acetylcholine release in cat pontine reticular formation: implications for REM sleep regulation,” J. Neurophysiol., 92, 2198–2206 (2004).PubMedCrossRefGoogle Scholar
  35. 35.
    M. C. Xi, F. R. Morales, and M. H. Chase, “Interactions between GABAergic and cholinergic processes in the nucleus pontis oralis: neuronal mechanisms controlling active (rapid eye movement) sleep and wakefulness,” J. Neurosci., 24, No. 47, 10670–10678 (2004).PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2009

Authors and Affiliations

  1. 1.I. M. Sechenov Institute of Evolutionary Physiology and BiochemistryRussian Academy of SciencesSt. PetersburgRussia

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