The rat ponto-medullary network responsible for paradoxical sleep onset and maintenance: A combined microinjection and functional neuroanatomical study

European Journal of Neuroscience

Volumn 16, Issue 10, 2002, Pages 1959-1973

  Boissard, Romuald ^a   Gervasoni, Damien ^a   Schmidt, Markus H ^b   Barbagli, Bruno ^a   Fort, Patrice ^a   Luppi, Pierre Hervé ^a  

^a UNIVERSITÉ LYON 1   (France)

^b Ohio Sleep Medicine and Neuroscience Institute   (United States)

Author keywords

C Fos; GABA; Glycine; REM sleep; Subcoeruleus

Indexed keywords

3 AMINO 2 (3 CARBOXYPROPYL) 6 (4 METHOXYPHENYL)PYRIDAZINIUM BROMIDE; BICUCULLINE; CARBACHOL; CHOLERA TOXIN B SUBUNIT; KAINIC ACID; LEUKOAGGLUTININ; 4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; AMINO ACID RECEPTOR BLOCKING AGENT; AMINO ACID RECEPTOR STIMULATING AGENT; CHOLINE ACETYLTRANSFERASE; CHOLINERGIC RECEPTOR STIMULATING AGENT; KYNURENIC ACID; LEUKOAGGLUTININS, PLANTS; PHYTOHEMAGGLUTININ; PROTEIN C FOS; PYRIDAZINE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; GABAERGIC SYSTEM; IMMUNOHISTOCHEMISTRY; MALE; MICROIONTOPHORESIS; MICROPIPETTE; MUSCLE ATONIA; NERVE CELL NETWORK; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; RAT; REM SLEEP; SLEEP WAKING CYCLE; ANIMAL; DRUG EFFECT; EFFERENT NERVE; ELECTROENCEPHALOGRAPHY; ELECTROMYOGRAPHY; HISTOLOGY; MEDULLA OBLONGATA; PHYSIOLOGY; PONS; SPRAGUE DAWLEY RAT; TEGMENTUM; WAKEFULNESS;

ANIMALS; BICUCULLINE; CARBACHOL; CHOLINE O-ACETYLTRANSFERASE; CHOLINERGIC AGONISTS; EFFERENT PATHWAYS; ELECTROENCEPHALOGRAPHY; ELECTROMYOGRAPHY; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; GABA ANTAGONISTS; IMMUNOHISTOCHEMISTRY; KAINIC ACID; KYNURENIC ACID; MALE; MEDULLA OBLONGATA; PHYTOHEMAGGLUTININS; PONS; PROTO-ONCOGENE PROTEINS C-FOS; PYRIDAZINES; RATS; RATS, SPRAGUE-DAWLEY; SLEEP, REM; TEGMENTUM MESENCEPHALI; WAKEFULNESS;

EID: 0036836273     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2002.02257.x     Document Type: Article

References (59)

1. Akaoka, H., Charlety, P.J., Saunier, C.F., Buda, M. & Chouvet, G. (1992) Combining in vivo volume -controlled pressure microinjection with extracellular unit recording. J. Neurosci. Meth, 42, 119-129.
2. Aserinsky, E. & Kleitman, N. (1953) Regularly occurring periods of eye motility and concomitant phenomena during sleep. Science, 118, 273-274.
3. Baghdoyan, H.A., Rodrigo-Angulo, M.L., McCarley, R.W. & Hobson, J.A. (1987) A neuroanatomical gradient in the pontine tegmentum for the cholinoceptive induction of desynchronized sleep signs. Brain Res., 414, 245-261.
4. Bourgin, P., Escourrou, P., Gaultier, C. & Adrien, J. (1995) Induction of rapid eye movement sleep by carbachol infusion into the pontine reticular formation in the rat. Neuroreport, 6, 532-536.
5. Chase, M.H., Soja, P.J. & Morales, F.R. (1989) Evidence that glycine mediates the postsynaptic potentials that inhibit lumbar motoneurones during the atonia of active sleep. J. Neurosci., 9. 743-751.
6. Darracq, L., Gervasoni, D., Soulière, F., Lin, J.S., Fort, P., Chouvet, G. & Luppi, P.H. (1996) Effect of strychnine on rat locus coeruleus neurones during sleep and wakefulness. Neuroreport, 8, 351-355.
7. Datta, S., Siwek, D.F., Patterson, E.H. & Cipolloni, P.B. (1998) Localization of pontine PGO wave generation sites and their anatomical projections in the rat. Synapse, 30, 409-423.
8. Debarbieux, F., Brunton, J. & Charpak, S. (1998) Effect of bicuculline on thalamic activity: a direct blockade of IAHP in reticularis neurones. J. Neurophysiol., 79, 2911-2918.
9. Dement, W. (1958) The occurrence of low voltage, fast, electroencephalogram patterns during behavioral sleep in the cat. Electroencephalogr. Clin. Neurophysiol., 10, 291-296.
10. Dement, W. & Kleitman, N. (1957) Cyclic variations of EEG during sleep and their relation to eye movement., body motility. & dreaming. Electroencephalogr. Clin. Neurophysiol., 9, 673-690.
11. Deurveilher, S., Hars, B. & Hennevin, E. (1997) Pontine microinjection of carbachol does not reliably enhance paradoxical sleep in rats. Sleep, 20, 593-607.
12. El Mansari, M., Sakai, K. & Jouvet, M. (1989) Unitary characteristics of presumptive cholinergic tegmental neurones during the sleep-waking cycle in freely moving cats. Exp. Brain. Res., 76, 519-529.
13. Ford, B., Holmes, C.J., Mainville, L. & Jones, B.E. (1995) GABAergic neurones in the rat pontomesencephalic tegmentum: codistribution with cholinergic and other tegmental neurones projecting to the posterior lateral hypothalamus. J. Comp. Neurol., 363, 177-196.
14. Fort, P., Luppi, P.H. & Jouvet, M. (1993) Glycine-immunoreactive neurones in the cat brain stem reticular formation. Neuroreport, 4, 1123-1126.
15. Fort, P., Luppi, P.H. & Jouvet, M. (1994) Afferents to the nucleus reticularis parvicellularis of the cat medulla oblongata: a tract-tracing study with cholera toxin B subunit. J. Comp. Neurol., 342, 603-618.
16. Fort, P., Luppi, P.H., Wenthold, R. & Jouvet, M. (1990) [Glycine immunoreactive neurones in the medulla oblongata in cats] Neurones immunoreactifs a la glycine dans le bulbe rachidien du chat. C R. Acad. Sci., III, 311, 205-212.
17. Garzùn, M., De Andrès, I. & Reinoso-Suarez, F. (1998) Sleep patterns after carbachol delivery in the ventral oral pontine tegmentum of the cat. Neuroscience, 83, 17-31.
18. Gervasoni, D., Darracq, L., Fort, P., Soulière, F., Chouvet, G. & Luppi, P.H. (1998) Electrophysiological evidence that noradrenergic neurones of the rat locus coeruleus are tonically inhibited by GABA during sleep. Eur. J. Neurosci., 10, 964-970.
19. Gervasoni, D., Peyron, C., Rampon, C., Barbagli, B., Chouvet, G., Urbain, N., Fort, P. & Luppi, P.H. (2000) Role and origin of the GABAergic innervation of dorsal raphe serotonergic neurones. J. Neurosci., 20, 4217-4225.
20. Gnadt, J.W. & Pegram, G.V. (1986) Cholinergic brainstem mechanisms of REM sleep in the rat. Brain Res, 384, 29-41.
21. Hobson, J.A., McCarley, R.W. & Wyzinski, P. (1975) Sleep cycle oscillation: reciprocal discharge by two brainstem neuronal groups. Science, 189, 55-58.
22. Holstege, J.C. & Bongers, C.M. (1991) A glycinergic projection from the ventromedial lower brainstem to spinal motoneurones. An ultrastructural double labeling study in rat. Brain Res., 566, 308-315.
23. Jones, B.E. (1991) Paradoxical sleep and its chemical/structural substrates in the brain. Neuroscience, 40, 637-656.
24. Jones, B.E. & Yang, T.Z. (1985) The efferent projections from the reticular formation and the locus coeruleus studied by anterograde and retrograde axonal transport in the rat. J. Comp. Neurol., 242, 56-92.
25. Jouvet, M. & Michel, F. (1959) Corrélations électromyographiques du sommeil chez. le chat décortiqué et méncéphalique chronique. C. R. Soc. Biol., 153, 422-425.
26. Kohlmeier, K.A., Lopez-Rodriguez, F., Liu, R.H., Morales, F.R. & Chase, M.H. (1996) State-dependent phenomena in cat masseter motoneurones. Brain Res., 722, 30-38.
27. Koyama, Y. & Sakai, K. (2000) Modulation of presumed cholinergic mesopontine tegmental neurones by acetylcholine and monoamines applied iontophoretically in unanesthetized cats. Neuroscience, 96, 723-733.
28. Koyama, Y., Schmidt, M.H., Takahashi, K. & Kayama, Y. (2001) Cholinergic neurones in the laterodorsal tegmental nucleus regulate penile erection during paradoxical sleep. Soc. Neurosci. Abstr., 522, 20.
29. Kubin, L. (2001) Carbachol models of REM sleep: Recent developments and new directions. Arch. Ital. Biol., 139, 147-168.
30. Lai, Y.Y. & Siegel, J.M. (1990) Cardiovascular and muscle tone changes produced by microinjection of cholinergic and glutamatergic agonists in dorsolateral pons and medial medulla. Brain Res., 514, 27-36.
31. Li, Y.Q., Takada, M., Kaneko, T. & Mizuno, N. (1996) GABAergic and glycinergic neurones projecting to the trigeminal motor nucleus: a double labeling study in the rat. J. Comp. Neurol., 373, 498-510.
32. Luppi, P.H., Aston-Jones, G., Akaoka, H., Chouvet, G. & Jouvet, M. (1995) Afferent projections to the rat locus coeruleus demonstrated by retrograde and anterograde tracing with cholera-toxin B subunit and Phaseolus vulgaris leucoagglutinin. Neuroscience, 65, 119-160.
33. Luppi, P.H., Fort, P. & Jouvet, M. (1995) Iontophoretic application of unconjugated cholera toxin amp; subunit CTb combined with immunohistochemistry of neurochemical substances: a method for transmitter identification of retrogradely labelled neurones. Brain Res., 534, 209-224.
34. Luppi, P.H., Sakai, K., Fort, P., Salvert, D. & Jouvet, M. (1988) The nuclei of origin of monoaminergic., peptidergic, & cholinergic afferents to the cat nucleus reticularis magnocellularis: a double-labeling study with cholera toxin as a retrograde tracer. J. Comp. Neurol., 277, 1-20.
35. Maloney, K.J., Mainville, L. & Jones, B.E. (1999) Differential c-Fos expression in cholinergic., monoaminergic and GABAergic cell groups of the pontomesencephalic tegmentum after paradoxical sleep deprivation and recovery. J. Neurosci., 19, 3057-3072.
36. Morales, F.R., Sampogna, S., Yamuy, J. & Chase, M.H. (1999) C-Fos expression in brainstem premotor interneurones during cholinergically induced active sleep in the cat. J. Neurosci., 19, 9508-9518.
37. Onoe, H. & Sakai, K. (1995) Kainate receptors: a novel mechanism in paradoxical (REM) sleep generation. Neuroreport, 6, 353-356.
38. Paxinos, G. & Watson, C. (1997) The Rat Brain in Stereotaxic Coordinates. Academic Press, Sydney.
39. Peyron, C., Luppi, P.H., Fort, P., Rampon, C. & Jouvet, M. (1996) Lower brainstem catecholamine afferents to the rat dorsal raphe nucleus. J. Comp. Neurol., 364, 402-413.
40. Peyron, C., Petit, J.M., Rampon, C., Jouvet, M. & Luppi, P.H. (1998) Forebrain afferents to the rat dorsal raphe nucleus demonstrated by retrograde and anterograde tracing methods. Neuroscience, 82, 443-468.
41. Rampon, C., Peyron, C., Petit, J.M., Fort, P., Gervasoni D. & Luppi, P.H. (1996) Origin of the glycinergic innervation of the rat trigeminal motor nucleus. Neuroreport, 7, 3081-3085.
42. Sakai, K., Crochet, S. & Onoe, H. (2001) Pontine structures and mechanisms involved in the generation of paradoxical (REM) sleep. Arch. Ital. Biol., 139, 93-107.
43. Sakai, K. & Koyama, Y. (1996) Are there cholinergic and non-cholinergic paradoxical sleep-on neurones in the pons? Neuroreport, 7, 2449-2453.
44. Sakai, K., Sastre, J.P., Kanamori, N. & Jouvet, M. (1981) State-specific neurones in the ponto-medullary reticular formation with special reference to the postural atonia during paradoxical sleep in the cat. In Pompeiano, O. & Aimone Marsan, C. (eds), Brain Mechanisms of Perceptual Awareness and Purposeful Behavior. Paven Press, New York, pp. 405-429.
45. Sakai, K., Sastre, J.P., Salvert, D., Touret, M., Tohyama, M. & Jouvet, M. (1979) Tegmentoreticular projections with special reference to the muscular atonia during paradoxical sleep in the cat: an HRP study. Brain Res., 176, 233-254.
46. Schmidt, M.H., Valatx, J.L., Sakai, K., Fort, P. & Jouvet, M. (2000) Role of the lateral preoptic area in sleep-related erectile mechanisms and sleep generation in the rat. J. Neurosci., 20, 6640-6647.
47. Schmidt, M.H., Valatx, J.L., Schmidt, H.S., Wauquier, A. & Jouvet, M. (1994) Experimental evidence of penile erections during paradoxical sleep in the rat. Neuroreport, 5, 561-564.
48. Shiromani, P.J. & Fishbein, W. (1986) Continuous pontine cholinergic microinfusion via mini-pump induces sustained alterations in rapid eye movement (REM) sleep. Pharmacol. Biochem. Behav., 25, 1253-1261.
49. Siegel, J.M. & McGinty, D.J. (1977) Pontine reticular formation neurones: relationship of discharge to motor activity. Science, 196, 678-680.
50. Soja, P.J., Lopez-Rodriguez, F., Morales, F.R. & Chase M.H. (1991) The postsynaptic inhibitory control of lumbar motoneurones during the atonia of active sleep: effect of strychnine on motoneuron properties. J. Neurosci., 11, 2804-2811.
51. Souliere, F., Urbain, N., Gervasoni, D., Schmitt, P., Guillemort, C., Fort, P., Renaud, B., Luppi, P.H. & Chouvet, G. (2000) Single-unit and polygraphic recordings associated with systemic or local pharmacology: a multi-purpose stereotaxic approach for the awake., anaesthetic-free. & head-restrained rat. J. Neurosci. Res., 61, 88-100.
52. Steriade, M., Datta, S., Paré D., Oakson, G. & Curro Dossi, R.C. (1990) Neuronal activities in brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical systems. J. Neurosci., 10, 2541-2559.
53. Stone, T.W. (1985) Microiontophoresis and pressure ejection. In Smith, A.D. (ed), Methods in the Neurosciences. Wiley, New York, pp. xxx-xxx.
54. Swanson, L.W. (1992) Structure of the Rat Brain. Elsevier Science Publishers, Location, pp. xxx-xxx.
55. Vanni-Mercier, G., Sakai, K., Lin, J.S. & Jouvet, M. (1989) Mapping of cholinoceptive brainstem structures responsible for the generation of paradoxical sleep in the cat. Arch. Ital. Biol., 127, 133-164.
56. Velazquez-Moctezuma, J., Gillin, J.C. & Shiromani, P.J. (1989) Effect of specific MI., M2 muscarinic receptor agonists on REM sleep generation. Brain Res., 503, 128-131.
57. Xi, M.C., Morales, F.R. & Chase, M.H. (1999) Evidence that wakefulness and REM sleep are controlled by a GABAergic pontine mechanism. J. Neurophysiol., 82, 2015-2019.
58. Yamamoto, K., Mamelak, A.N., Quattrochi, J.J. & Hobson, J.A. (1990) A cholinoceptive desynchronized sleep induction zone in the anterodorsal pontine tegmentum: locus of the sensitive region. Neuroscience, 39, 279-293.
59. Yamuy, J., Fung, S.J., Xi, M., Morales, F.R. & Chase, M.H. (1999) Hypoglossal motoneurones are postsynaptically inhibited during carbachol-induced rapid eye movement sleep. Neuroscience, 94, 11-15.