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. 1996 Feb 1;490(Pt 3):745–758. doi: 10.1113/jphysiol.1996.sp021182

Behaviour of raphe cells projecting to the dorsomedial medulla during carbachol-induced atonia in the cat.

G Woch 1, R O Davies 1, A I Pack 1, L Kubin 1
PMCID: PMC1158711  PMID: 8683472

Abstract

1. The activity of most brainstem serotonergic cells is suppressed during sleep, particularly the rapid eye movement (REM) phase. Thus, they may play a major role in state-dependent changes in CNS functioning. Our main goal was to search for medullary raphe cells having axonal branches in the region of the hypoglossal (XII) motor nucleus and assess their behaviour during the atonia produced by microinjections of a cholinergic agonist, carbachol, into the dorsal pontine tegmentum. In chronic animals, such microinjections evoke a desynchronized sleep-like state similar to natural REM sleep; in decerebrate animals, they produce eye movements and a motor suppression similar to the postural atonia of REM sleep. 2. In decerebrate, paralysed, vagotomized and artificially ventilated cats, we recorded extracellularly from medullary raphe cells antidromically activated from the XII nucleus region. Forty-five cells recorded in the raphe obscurus and pallidus nuclei were antidromically activated with latencies characteristic of non-myelinated fibres (4.4-42.0 ms). For thirty-three of the forty-five cells, we found one or more axonal branches within or just below the XII nucleus. The remaining twelve cells, in addition to the XII nucleus, had axonal ramifications in the medial nucleus of the solitary tract (NTS) and/or the dorsal motor nucleus of the vagus (DMV). 3. A subset of fourteen spontaneously active cells with identified axonal projections were held long enough to be recorded during the carbachol-induced atonia, and eight of these also during the subsequent recovery and a systemic administration of the serotonergic 1A receptor agonist (+/-)8-hydroxy-2-(di-N-propylamino)tetrealin hydrobromide (8-OH-DPAT). All but one were suppressed during the atonia in parallel to the suppression of XII, phrenic and postural nerve activities (firing rate, 1.3 +/- 0.7 Hz before and 0.1 +/- 0.2 Hz after carbachol (means +/- S.D.)). Following the recovery from the atonia, the firing rates of the eight cells increased to the pre-carbachol level (1.6 +/- 1.0 Hz). Subsequently, all were silenced by 8-OH-DPAT. 4. These cells fulfil most physiological criteria for serotonergic cells and have the potential to modulate, in a state-dependent manner, activities in the motor XII nucleus, visceral sensory NTS, and DMV. The decrements in serotonergic neuronal activity that occur during the carbachol-induced atonia suggest that a similar withdrawal of serotonergic input may occur during REM sleep and contribute to the characteristic reductions in upper airway motor tone.

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Selected References

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  1. Allen G. V., Cechetto D. F. Serotoninergic and nonserotoninergic neurons in the medullary raphe system have axon collateral projections to autonomic and somatic cell groups in the medulla and spinal cord. J Comp Neurol. 1994 Dec 15;350(3):357–366. doi: 10.1002/cne.903500303. [DOI] [PubMed] [Google Scholar]
  2. Barman S. M., Gebber G. L. The axons of raphespinal sympathoinhibitory neurons branch in the cervical spinal cord. Brain Res. 1988 Feb 16;441(1-2):371–376. doi: 10.1016/0006-8993(88)91417-5. [DOI] [PubMed] [Google Scholar]
  3. Berger A. J., Bayliss D. A., Viana F. Modulation of neonatal rat hypoglossal motoneuron excitability by serotonin. Neurosci Lett. 1992 Aug 31;143(1-2):164–168. doi: 10.1016/0304-3940(92)90257-8. [DOI] [PubMed] [Google Scholar]
  4. Davies R. O., Kubin L. Projection of pulmonary rapidly adapting receptors to the medulla of the cat: an antidromic mapping study. J Physiol. 1986 Apr;373:63–86. doi: 10.1113/jphysiol.1986.sp016035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Fort P., Luppi P. H., Sakai K., Salvert D., Jouvet M. Nuclei of origin of monoaminergic, peptidergic, and cholinergic afferents to the cat trigeminal motor nucleus: a double-labeling study with cholera-toxin as a retrograde tracer. J Comp Neurol. 1990 Nov 8;301(2):262–275. doi: 10.1002/cne.903010209. [DOI] [PubMed] [Google Scholar]
  6. Gilbey M. P., Futuro-Neto H. A., Zhou S. Y. Respiratory-related discharge patterns of caudal raphe neurones projecting to the upper thoracic spinal cord in the rat. J Auton Nerv Syst. 1995 Jan 3;50(3):263–273. doi: 10.1016/0165-1838(94)00097-4. [DOI] [PubMed] [Google Scholar]
  7. Heym J., Steinfels G. F., Jacobs B. L. Activity of serotonin-containing neurons in the nucleus raphe pallidus of freely moving cats. Brain Res. 1982 Nov 18;251(2):259–276. doi: 10.1016/0006-8993(82)90743-0. [DOI] [PubMed] [Google Scholar]
  8. Jacobs B. L., Azmitia E. C. Structure and function of the brain serotonin system. Physiol Rev. 1992 Jan;72(1):165–229. doi: 10.1152/physrev.1992.72.1.165. [DOI] [PubMed] [Google Scholar]
  9. Kimura H., Kubin L., Davies R. O., Pack A. I. Cholinergic stimulation of the pons depresses respiration in decerebrate cats. J Appl Physiol (1985) 1990 Dec;69(6):2280–2289. doi: 10.1152/jappl.1990.69.6.2280. [DOI] [PubMed] [Google Scholar]
  10. Kodama T., Takahashi Y., Honda Y. Enhancement of acetylcholine release during paradoxical sleep in the dorsal tegmental field of the cat brain stem. Neurosci Lett. 1990 Jul 13;114(3):277–282. doi: 10.1016/0304-3940(90)90576-u. [DOI] [PubMed] [Google Scholar]
  11. Kubin L., Kimura H., Davies R. O. The medullary projections of afferent bronchopulmonary C fibres in the cat as shown by antidromic mapping. J Physiol. 1991 Apr;435:207–228. doi: 10.1113/jphysiol.1991.sp018506. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kubin L., Kimura H., Tojima H., Davies R. O., Pack A. I. Suppression of hypoglossal motoneurons during the carbachol-induced atonia of REM sleep is not caused by fast synaptic inhibition. Brain Res. 1993 May 21;611(2):300–312. doi: 10.1016/0006-8993(93)90517-q. [DOI] [PubMed] [Google Scholar]
  13. Kubin L., Reignier C., Tojima H., Taguchi O., Pack A. I., Davies R. O. Changes in serotonin level in the hypoglossal nucleus region during carbachol-induced atonia. Brain Res. 1994 May 9;645(1-2):291–302. doi: 10.1016/0006-8993(94)91663-2. [DOI] [PubMed] [Google Scholar]
  14. Kubin L., Tojima H., Davies R. O., Pack A. I. Serotonergic excitatory drive to hypoglossal motoneurons in the decerebrate cat. Neurosci Lett. 1992 May 25;139(2):243–248. doi: 10.1016/0304-3940(92)90563-m. [DOI] [PubMed] [Google Scholar]
  15. Lai Y. Y., Siegel J. M. Cardiovascular and muscle tone changes produced by microinjection of cholinergic and glutamatergic agonists in dorsolateral pons and medial medulla. Brain Res. 1990 Apr 23;514(1):27–36. doi: 10.1016/0006-8993(90)90432-b. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Li Y. Q., Takada M., Mizuno N. The sites of origin of serotoninergic afferent fibers in the trigeminal motor, facial, and hypoglossal nuclei in the rat. Neurosci Res. 1993 Sep;17(4):307–313. doi: 10.1016/0168-0102(93)90114-6. [DOI] [PubMed] [Google Scholar]
  17. Lovick T. A., Robinson J. P. Bulbar raphe neurones with projections to the trigeminal nucleus caudalis and the lumbar cord in the rat: a fluorescence double-labelling study. Exp Brain Res. 1983;50(2-3):299–308. doi: 10.1007/BF00239194. [DOI] [PubMed] [Google Scholar]
  18. Manaker S., Tischler L. J., Morrison A. R. Raphespinal and reticulospinal axon collaterals to the hypoglossal nucleus in the rat. J Comp Neurol. 1992 Aug 1;322(1):68–78. doi: 10.1002/cne.903220106. [DOI] [PubMed] [Google Scholar]
  19. Manaker S., Tischler L. J. Origin of serotoninergic afferents to the hypoglossal nucleus in the rat. J Comp Neurol. 1993 Aug 15;334(3):466–476. doi: 10.1002/cne.903340310. [DOI] [PubMed] [Google Scholar]
  20. McCall R. B., Clement M. E. Identification of serotonergic and sympathetic neurons in medullary raphe nuclei. Brain Res. 1989 Jan 16;477(1-2):172–182. doi: 10.1016/0006-8993(89)91405-4. [DOI] [PubMed] [Google Scholar]
  21. Morales F. R., Engelhardt J. K., Soja P. J., Pereda A. E., Chase M. H. Motoneuron properties during motor inhibition produced by microinjection of carbachol into the pontine reticular formation of the decerebrate cat. J Neurophysiol. 1987 Apr;57(4):1118–1129. doi: 10.1152/jn.1987.57.4.1118. [DOI] [PubMed] [Google Scholar]
  22. Morrison S. F., Gebber G. L. Axonal branching patterns and funicular trajectories of raphespinal sympathoinhibitory neurons. J Neurophysiol. 1985 Mar;53(3):759–772. doi: 10.1152/jn.1985.53.3.759. [DOI] [PubMed] [Google Scholar]
  23. Morrison S. F., Gebber G. L. Raphe neurons with sympathetic-related activity: baroreceptor responses and spinal connections. Am J Physiol. 1984 Mar;246(3 Pt 2):R338–R348. doi: 10.1152/ajpregu.1984.246.3.R338. [DOI] [PubMed] [Google Scholar]
  24. Sauerland E. K., Orr W. C., Hairston L. E. DMG patterns of oropharyngeal muscles during respiration in wakefulness and sleep. Electromyogr Clin Neurophysiol. 1981 Feb-Mar;21(2-3):307–316. [PubMed] [Google Scholar]
  25. Schaffar N., Kessler J. P., Bosler O., Jean A. Central serotonergic projections to the nucleus tractus solitarii: evidence from a double labeling study in the rat. Neuroscience. 1988 Sep;26(3):951–958. doi: 10.1016/0306-4522(88)90111-x. [DOI] [PubMed] [Google Scholar]
  26. Shima K., Nakahama H., Yamamoto M. Firing properties of two types of nucleus raphe dorsalis neurons during the sleep-waking cycle and their responses to sensory stimuli. Brain Res. 1986 Dec 10;399(2):317–326. doi: 10.1016/0006-8993(86)91522-2. [DOI] [PubMed] [Google Scholar]
  27. Silberman E. K., Vivaldi E., Garfield J., McCarley R. W., Hobson J. A. Carbachol triggering of desynchronized sleep phenomena: enhancement via small volume infusions. Brain Res. 1980 Jun 2;191(1):215–224. doi: 10.1016/0006-8993(80)90324-8. [DOI] [PubMed] [Google Scholar]
  28. Skagerberg G., Björklund A. Topographic principles in the spinal projections of serotonergic and non-serotonergic brainstem neurons in the rat. Neuroscience. 1985 Jun;15(2):445–480. doi: 10.1016/0306-4522(85)90225-8. [DOI] [PubMed] [Google Scholar]
  29. Takakusaki K., Matsuyama K., Kobayashi Y., Kohyama J., Mori S. Pontine microinjection of carbachol and critical zone for inducing postural atonia in reflexively standing decerebrate cats. Neurosci Lett. 1993 Apr 30;153(2):185–188. doi: 10.1016/0304-3940(93)90318-f. [DOI] [PubMed] [Google Scholar]
  30. Thor K. B., Helke C. J. Serotonin- and substance P-containing projections to the nucleus tractus solitarii of the rat. J Comp Neurol. 1987 Nov 8;265(2):275–293. doi: 10.1002/cne.902650210. [DOI] [PubMed] [Google Scholar]
  31. Tojima H., Kubin L., Kimura H., Davies R. O. Spontaneous ventilation and respiratory motor output during carbachol-induced atonia of REM sleep in the decerebrate cat. Sleep. 1992 Oct;15(5):404–414. doi: 10.1093/sleep/15.5.404. [DOI] [PubMed] [Google Scholar]
  32. Trulson M. E., Frederickson C. J. A comparison of the electrophysiological and pharmacological properties of serotonin-containing neurons in the nucleus raphe dorsalis, raphe medianus and raphe pallidus recorded from mouse brain slices in vitro: role of autoreceptors. Brain Res Bull. 1987 Feb;18(2):179–190. doi: 10.1016/0361-9230(87)90189-4. [DOI] [PubMed] [Google Scholar]
  33. Trulson M. E., Trulson V. M. Activity of nucleus raphe pallidus neurons across the sleep-waking cycle in freely moving cats. Brain Res. 1982 Apr 8;237(1):232–237. doi: 10.1016/0006-8993(82)90572-8. [DOI] [PubMed] [Google Scholar]
  34. Vanni-Mercier G., Sakai K., Lin J. S., Jouvet M. Mapping of cholinoceptive brainstem structures responsible for the generation of paradoxical sleep in the cat. Arch Ital Biol. 1989 Jun;127(3):133–164. [PubMed] [Google Scholar]
  35. Wessendorf M. W., Anderson E. G. Single unit studies of identified bulbospinal serotonergic units. Brain Res. 1983 Nov 21;279(1-2):93–103. doi: 10.1016/0006-8993(83)90166-x. [DOI] [PubMed] [Google Scholar]
  36. Willcockson W. S., Gerhart K. D., Cargill C. L., Willis W. D. Effects of biogenic amines on raphe-spinal tract cells. J Pharmacol Exp Ther. 1983 Jun;225(3):637–645. [PubMed] [Google Scholar]

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