Stimulation of the rat medullary raphe nuclei induces differential responses in respiratory muscle activity

Respiratory Physiology and Neurobiology

Volumn 165, Issue 2-3, 2009, Pages 208-214

  Besnard, S ^a   Denise, P ^a   Cappelin, B ^b   Dutschmann, M ^c   Gestreau, C ^c  

^a Laboratoire de Physiologie   (France)

^b UNIVERSITÉ DE POITIERS   (France)

^c University of Mediterranée   (France)

Author keywords

Apnea; Medullary raphe; Serotonin; Sleep; Stimulation

Indexed keywords

ANESTHESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APNEA; ARTICLE; BRAIN DEPTH STIMULATION; BREATHING MUSCLE; DIAPHRAGM; GENIOHYOID MUSCLE; GLOBUS PALLIDUS; MALE; MEDULLA OBLONGATA; MUSCLE CONTRACTION; NONHUMAN; PRIORITY JOURNAL; RAPHE MAGNUS NUCLEUS; RAPHE NUCLEUS; RAT; SKELETAL MUSCLE; TACHYPNEA; TOPOGRAPHY;

ANESTHESIA; ANIMALS; ELECTRIC STIMULATION; MALE; MEDULLA OBLONGATA; MOTOR NEURONS; NEURAL INHIBITION; NEURAL PATHWAYS; RAPHE NUCLEI; RATS; RATS, SPRAGUE-DAWLEY; RESPIRATORY MECHANICS; RESPIRATORY MUSCLES; SPINAL CORD;

EID: 60749118366     PISSN: 15699048     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.resp.2008.12.004     Document Type: Article

References (67)

1. Aldes L.D., Marco L.A., and Chronister R.B. Serotonin-containing axon terminals in the hypoglossal nucleus of the rat. An immuno-electronmicroscopic study. Brain Res. Bull. 23 (1989) 249-256
2. Alvarenga R.M., Pires J.G., and Futuro Neto H.A. Functional mapping of the cardiorespiratory effects of dorsal and median raphe nuclei in the rat. Braz. J. Med. Biol. Res. 38 (2005) 1719-1727
3. Arata A., Hernandez Y.M., Lindsey B.G., Morris K.F., and Shannon R. Transient configurations of baroresponsive respiratory-related brainstem neuronal assemblies in the cat. J. Physiol. 525 (2000) 509-530
4. Baekey D.M., Morris K.F., Nuding S.C., Segers L.S., Lindsey B.G., and Shannon R. Medullary raphe neuron activity is altered during fictive cough in the decerebrate cat. J. Appl. Physiol. 94 (2003) 93-100
5. Bouryi V.A., and Lewis D.I. The modulation by 5-HT of glutamatergic inputs from the raphe pallidus to rat hypoglossal motoneurones, in vitro. J. Physiol. 553 (2003) 1019-1031
6. Cao Y., Matsuyama K., Fujito Y., and Aoki M. Involvement of medullary GABAergic and serotonergic raphe neurons in respiratory control: electrophysiological and immunohistochemical studies in rats. Neurosci. Res. 56 (2006) 322-331
7. Cao Y., Fujito Y., Matsuyama K., and Aoki M. Effects of electrical stimulation of the medullary raphe nuclei on respiratory movement in rats. J. Comp. Physiol. A: Neuroethol. Sens. Neural Behav. Physiol. 192 (2006) 497-505
8. Comet M.A., Bernard J.F., Hamon M., Laguzzi R., and Sévoz-Couche C. Activation of nucleus tractus solitarius 5-HT2A but not other 5-HT2 receptor subtypes inhibits the sympathetic activity in rats. Eur. J. Neurosci. 26 (2007) 345-354
9. Curran A.K., and Leiter J.C. Baroreceptor-mediated inhibition of respiration after peripheral and central administration of a 5-HT1A receptor agonist in neonatal piglets. Exp. Physiol. 92 (2007) 757-767
10. Dobbins E.G., and Feldman J.L. Brainstem network controlling descending drive to phrenic motoneurons in rat. J. Comp. Neurol. 347 (1994) 64-86
11. Dong H.H., and Liu L. Effects of stimulation of ventromedian area of nucleus hypoglossus on respiratory rhythm in rabbits. Sheng Li Xue Bao 46 (1994) 299-303
12. Dostrovsky J.O., and Lozano A.M. Mechanisms of deep brain stimulation. Mov. Disord. 17 (2002) 63-68
13. 2. Respir. Physiol. 111 (1998) 15-23
14. Feldman J.L., and Del Negro C.A. Looking for inspiration: new perspectives on respiratory rhythm. Nat. Rev. Neurosci. 7 (2006) 232-242
15. Fenik V., Davies R.O., Pack A.I., and Kubin L. Differential suppression of upper airway motor activity during carbachol-induced, REM sleep-like atonia. Am. J. Physiol. 275 (1998) 1013-1024
16. Feroah T.R., Forster H.V., Pan L., Wenninger J., Martino P., and Rice T. Effect of slow wave and REM sleep on thyropharyngeus and stylopharyngeus activity during induced central apneas. Respir. Physiol. 124 (2001) 129-140
17. Fogel R.B., White D.P., Pierce R.J., Malhotra A., Edwards J.K., Dunai J., Kleverlaan D., and Trinder J. Control of upper airway muscle activity in younger versus older men during sleep onset. J. Physiol. 553 (2003) 533-544
18. Fogel R.B., Trinder J., White D.P., Malhotra A., Raneri J., Schory K., Kleverlaan D., and Pierce R.J. The effect of sleep onset on upper airway muscle activity in patients with sleep apnoea versus controls. J. Physiol. 564 (2005) 549-562
19. Gestreau C., Dutschmann M., Obled S., and Bianchi A.L. Activation of XII motoneurons and premotor neurons during various oropharyngeal behaviors. Respir. Physiol. Neurobiol. 147 (2005) 159-176
20. Guyenet P.G., Mulkey D.K., Stornetta R.L., and Bayliss D.A. Regulation of ventral surface chemoreceptors by the central respiratory pattern generator. J. Neurosci. 25 (2005) 8938-8947
21. Haji A., Takeda R., and Okazaki M. Neuropharmacology of control of respiratory rhythm and pattern in mature mammals. Pharmacol. Ther. 86 (2000) 277-304
22. Haxhiu M.A., van Lunteren E., Mitra J., and Cherniack N.S. Comparison of the response of diaphragm and upper airway dilating muscle activity in sleeping cats. Respir. Physiol. 70 (1987) 183-193
23. Haxhiu M.A., Mack S.O., Wilson C.G., Feng P., and Strohl K.P. Sleep networks and the anatomic and physiologic connections with respiratory control. Front. Biosci. 8 (2003) 946-962
24. Hendricks J.C., Petrof B.J., Panckeri K., and Pack A.I. Upper airway dilating muscle hyperactivity during non-rapid eye movement sleep in English bulldogs. Am. Rev. Respir. Dis. 148 (1993) 185-194
25. Hilaire G., Morin D., Lajard A.M., and Monteau R. Changes in serotonin metabolism may elicit obstructive apnoea in the newborn rat. J. Physiol. 466 (1993) 367-381
26. Holtman Jr. J.R., Dick T.E., and Berger A.J. Involvement of serotonin in the excitation of phrenic motoneurons evoked by stimulation of the raphe obscurus. J. Neurosci. 6 (1986) 1185-1193
27. Holtman Jr. J.R., Marion L.J., and Speck D.F. Origin of serotonin-containing projections to the ventral respiratory group in the rat. Neuroscience 37 (1990) 541-552
28. Holtman Jr. J.R., and King K.A. Effect of activation of 5-HT1A receptors at the ventral medulla on phrenic nerve activity. Eur. J. Pharmacol. 253 (1994) 307-310
29. Jakus J., Stránsky A., Poliacek I., Baráni H., and Bosel'ová L. Effects of medullary midline lesions on cough and other airway reflexes in anaesthetized cats. Physiol. Res. 47 (1998) 203-213
30. Jacobs B.L., and Fornal C.A. Activity of brain serotonergic neurons in the behaving animal. Pharmacol. Rev. 43 (1991) 563-578
31. Jacobs B.L., and Azmitia E.C. Structure and function of the brain serotonin system. Physiol. Rev. 72 (1992) 165-229
32. Jacobs B.L., and Fornal C.A. Activity of serotonergic neurons in behaving animals. Neuropsychopharmacology 21 (1999) 9-15
33. Katz E.S., and White D.P. Genioglossus activity during sleep in normal control subjects and children with obstructive sleep apnea. Am. J. Respir. Crit. Care Med. 170 (2004) 553-560
34. King K.A., and Holtman Jr. J.R. Characterization of the effects of activation of ventral medullary serotonin receptor subtypes on cardiovascular activity and respiratory motor outflow to the diaphragm and larynx. J. Pharmacol. Exp. Ther. 252 (1990) 665-674
35. Kubin L., Alheid G.F., Zuperku E.J., and McCrimmon D.R. Central pathways of pulmonary and lower airway vagal afferents. J. Appl. Physiol. 101 (2006) 618-627
36. Kurtz D., Krieger J., and Stierle J.C. EMG activity of cricothyroid and chin muscles during wakefulness and sleeping in the sleep apnea syndrome. Electroencephalogr. Clin. Neurophysiol. 45 (1978) 777-784
37. Lalley P.M. Responses of phrenic motoneurones of the cat to stimulation of medullary raphe nuclei. J. Physiol. 380 (1986) 349-371
38. Lalley P.M. Serotoninergic and non-serotoninergic responses of phrenic motoneurones to raphe stimulation in the cat. J. Physiol. 380 (1986) 373-385
39. Lalley P.M., Benacka R., Bischoff A.M., and Richter D.W. Nucleus raphe obscurus evokes 5-HT-1A receptor-mediated modulation of respiratory neurons. Brain Res. 747 (1997) 156-159
40. Li Y.Q., Takada M., and Mizuno N. The sites of origin of serotoninergic afferent fibers in the trigeminal motor, facial, and hypoglossal nuclei in the rat. Neurosci. Res. 17 (1993) 307-313
41. Li Y., Song G., Cao Y., Wang H., Wang G., Yu S., and Zhang H. Modulation of the Hering-Breuer reflex by raphe pallidus in rabbits. Neurosci. Lett. 397 (2006) 259-262
42. Li Z., Morris K.F., Baekey D.M., Shannon R., and Lindsey B.G. Responses of simultaneously recorded respiratory-related medullary neurons to stimulation of multiple sensory modalities. J. Neurophysiol. 82 (1999) 176-187
43. Lindsey B.G., Segers L.S., Morris K.F., Hernandez Y.M., Saporta S., and Shannon R. Distributed actions and dynamic associations in respiratory-related neuronal assemblies of the ventrolateral medulla and brain stem midline: evidence from spike train analysis. J. Neurophysiol. 72 (1994) 1830-1851
44. Lindsey B.G., Arata A., Morris K.F., Hernandez Y.M., and Shannon R. Medullary raphe neurones and baroreceptor modulation of the respiratory motor pattern in the cat. J. Physiol. 512 (1998) 863-882
45. Lu J.W., Mann G.L., Ross R.J., Morrison A.R., and Kubin L. Differential effect of sleep-wake states on lingual and dorsal neck muscle activity in rats. Respir. Physiol. Neurobiol. 147 (2005) 191-203
46. Man H.Y., and Liu L. Effects of electrical and l-glutamate stimulation of nucleus raphe obscures on phrenic nerve activity in rabbits. Acta Physiol. Sin. 44 (1992) 92-97
47. Mezzanotte W.S., Tangel D.J., and White D.P. Waking genioglossal electromyogram in sleep apnea patients versus normal controls (a neuromuscular compensatory mechanism). J. Clin. Invest. 89 (1992) 1571-1579
48. Millhorn D.E. Stimulation of raphe (obscurus) nucleus causes long-term potentiation of phrenic nerve activity in cat. J. Physiol. 381 (1986) 169-179
49. Mohammed J.R., Saska T.A., Chi J., and Stephens Jr. R.L. Stimulation of the nucleus raphe obscurus produces marked serotonin release into the dorsal medulla of fed but not fasted rats-glutamatergic dependence. Brain Res. 695 (1995) 100-103
50. Morin D., Hennequin S., Monteau R., and Hilaire G. Depressant effect of raphe stimulation on inspiratory activity of the hypoglossal nerve: in vitro study in the newborn rat. Neurosci. Lett. 116 (1990) 299-303
51. Morin D., Monteau R., and Hilaire G. Compared effects of serotonin on cervical and hypoglossal inspiratory activities: an in vitro study in the newborn rat. J. Physiol. 451 (1992) 605-629
52. Morin D. Compared effects of serotonin on the inspiratory activity of glossopharyngeal, vagal, hypoglossal and cervical motoneurons in neonatal rat brain stem-spinal cord preparations. Neurosci. Lett. 160 (1993) 61-64
53. Morris K.F., Arata A., Shannon R., and Lindsey B.G. Long-term facilitation of phrenic nerve activity in cats: responses and short time scale correlations of medullary neurones. J. Physiol. 490 (1996) 463-480
54. Mulkey D.K., Rosin D.L., West G., Takakura A.C., Moreira T.S., Bayliss D.A., and Guyenet P.G. Serotonergic neurons activate chemosensitive retrotrapezoid nucleus neurons by a pH-independent mechanism. J. Neurosci. 27 (2007) 14128-14138
55. Penatti E.M., Berniker A.V., Kereshi B., Cafaro C., Kelly M.L., Niblock M.M., Gao H.G., Kinney H.C., Li A., and Nattie E.E. Ventilatory response to hypercapnia and hypoxia after extensive lesion of medullary serotonergic neurons in newborn conscious piglets. J. Appl. Physiol. 101 (2006) 1177-1188
56. Richerson G.B. Serotonergic neurons as carbon dioxide sensors that maintain pH homeostasis. Nat. Rev. Neurosci. 5 (2004) 449-461
57. Richerson G.B., Wang W., Hodges M.R., Dohle C.I., and Diez-Sampedro A. Homing in on the specific phenotype(s) of central respiratory chemoreceptors. Exp. Physiol. 90 (2005) 259-266
58. Richter D.W., Lalley P.M., Pierrefiche O., Haji A., Bischoff A.M., Wilken B., and Hanefeld F. Intracellular signal pathways controlling respiratory neurons. Respir. Physiol. 110 (1997) 113-212
59. Roda F., Pio J., Bianchi A.L., and Gestreau C. Effects of anesthetics on hypoglossal nerve discharge and c-Fos expression in brainstem hypoglossal premotor neurons. J. Comp. Neurol. 468 (2004) 571-586
60. Rosin D.L., Chang D.A., and Guyenet P.G. Afferent and efferent connections of the rat retrotrapezoid nucleus. J. Comp. Neurol. 499 (2006) 64-89
61. Sauerland E.K., and Harper R.M. The human tongue during sleep: electromyographic activity of the genioglossus muscle. Exp. Neurol. 51 (1976) 160-170
62. Sood S., Raddatz E., Liu X., Liu H., and Horner R.L. Inhibition of serotonergic medullary raphe obscurus neurons suppresses genioglossus and diaphragm activities in anesthetized but not conscious rats. J. Appl. Physiol. 100 (2006) 1807-1821
63. 2. J. Appl. Physiol. 97 (2004) 1763-1773
64. Taylor N.C., Li A., and Nattie E.E. Medullary serotonergic neurones modulate the ventilatory response to hypercapnia, but not hypoxia in conscious rats. J. Physiol. 566 (2005) 543-557
65. Veasey S.C., Fenik P., Panckeri K., Pack A.I., and Hendricks J.C. The effects of trazodone with l-tryptophan on sleep-disordered breathing in the English bulldog. Am. J. Respir. Crit. Care Med. 160 (1999) 1659-1667
66. Vizek M., and Bonora M. Diaphragmatic activity during biphasic ventilatory response to hypoxia in rats. Respir. Physiol. 111 (1998) 153-162
67. Wang G., Song G., Tin C., and Poon C.S. Nonassociative learning in expiratory inhibition of inspiratory motor output: an experimental and modeling study. Conf. Proc. IEEE Eng. Med. Biol. Soc. 6 (2005) 5843-5846