Medullary serotonergic neurones modulate the ventilatory response to hypercapnia, but not hypoxia in conscious rats

Journal of Physiology

Volumn 566, Issue 2, 2005, Pages 543-557

  Taylor, Natalie C ^a,b   Li, Aihua ^a   Nattie, Eugene E ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b DARTMOUTH HITCHCOCK MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 DIPROPYLAMINO 8 HYDROXYTETRALIN; CARBON DIOXIDE; SEROTONIN 1A RECEPTOR; SEROTONIN 1A AGONIST;

AMBIENT AIR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AROUSAL; ARTICLE; BODY TEMPERATURE; BREATHING PATTERN; CEREBROSPINAL FLUID; CHEMORECEPTOR; CONCENTRATION RESPONSE; CONSCIOUSNESS; CONTROLLED STUDY; FREQUENCY ANALYSIS; GLOBUS PALLIDUS; HYPERCAPNIA; HYPOXIA; MALE; MEDULLA OBLONGATA; MICRODIALYSIS; NEUROMODULATION; NONHUMAN; NONREM SLEEP; PRIORITY JOURNAL; RAPHE MAGNUS NUCLEUS; RAPHE NUCLEUS; RAT; RESPIRATION CONTROL; SEROTONINERGIC NERVE CELL; SEROTONINERGIC SYSTEM; THERMOREGULATION; TIDAL VOLUME; TIME; TISSUE DISTRIBUTION; WAKEFULNESS; ADULT; BREATHING; CARBON DIOXIDE BREATHING; NERVE CELL; RESPIRATORY FUNCTION;

8-HYDROXY-2-(DI-N-PROPYLAMINO)TETRALIN; ANIMALS; ANOXIA; BODY TEMPERATURE; ELECTROENCEPHALOGRAPHY; ELECTROMYOGRAPHY; HYPERCAPNIA; MALE; MEDULLA OBLONGATA; MICRODIALYSIS; NEURONS; OXYGEN CONSUMPTION; PLETHYSMOGRAPHY, WHOLE BODY; RAPHE NUCLEI; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, SEROTONIN, 5-HT1A; RESPIRATORY MECHANICS; SEROTONIN; SEROTONIN AGONISTS; SLEEP STAGES; WAKEFULNESS;

EID: 22744440628     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1113/jphysiol.2005.083873     Document Type: Article

References (54)

1. Arvidsson LE, Hacksell U, Nilsson JL, Hjorth S, Carlsson A, Lindberg P et al. (1981). 8-Hydroxy-2-(di-n-propylamino) tetralin, a new centrally acting 5-hydroxytryptamine receptor agonist. J Med Chem 24, 921-923.
2. Azmitia EC, Gannon PJ, Kheck NM & Whitaker-Azmitia PM (1996). Cellular localization of the 5-HT1A receptor in primate brain neurons and glial cells. Neuropsychopharmacology 14, 35-46.
3. Berner NJ, Grahn DA & Heller HC (1999). 8-OH-DPAT-sensitive neurons in the nucleus raphe magnus modulate thermoregulatory output in rats. Brain Res 831, 155-164.
4. Connelly CA, Ellenberger HH & Feldman JL (1989). Are there serotonergic projections from raphe and retrotrapezoid nuclei to the ventral respiratory group in the rat? Neurosci Lett 105, 34-40.
5. Cream C, Nattie E & Li A (1999). TRH microdialysis into the RTN of the conscious rat increases breathing, metabolism, and temperature. J Appl Physiol 87, 673-682.
6. Dobbins EG & Feldman JL (1994). Brainstem network controlling descending drive to phrenic motoneurons in rat. J Comp Neurol 347, 64-86.
7. Erickson JT & Millhorn DE (1994). Hypoxia and electrical stimulation of the carotid sinus nerve induce Fos-like immunoreactivity within catecholaminergic and serotoninergic neurons of the rat brainstem. J Comp Neurol 348, 161-182.
8. Gao B, Fritschy JM, Benke D & Mohler H (1993). Neuron-specific expression of GABAA-receptor subtypes: differential association of the [alpha]1- and [alpha]3-subunits with serotonergic and gabaergic neurons. Neuroscience 54, 881-892.
9. Gargaglioni LH, Coimbra NC & Branco LG (2003). The nucleus raphe magnus modulates hypoxia-induced hyperventilation but not anapyrexia in rats. Neurosci Lett 347, 121-125.
10. Guyenet PG, Stornetta RL, Bayliss DA & Mulkey DK (2005). Retrotrapezoid nucleus: a litmus test for the identification of central chemoreceptors. Exp Physiol 90, 247-253.
11. Helke CJ, Capuano S, Tran N & Zhuo H (1997). Immunocytochemical studies of the 5-HT(1A) receptor in ventral medullary neurons that project to the intermediolateral cell column and contain serotonin or tyrosine hydroxylase immunoreactivity. J Comp Neurol 379, 261-270.
12. Heym J, Steinfels GF & Jacobs BL (1982). Activity of serotonin-containing neurons in the nucleus raphe pallidus of freely moving cats. Brain Res 251, 259-276.
13. Hjorth S & Magnusson T (1988). The 5-HT 1A receptor agonist, 8-OH-DPAT, preferentially activates cell body 5-HT autoreceptors in rat brain in vivo. Naunyn Schmiedebergs Arch Pharmacol 338, 463-471.
14. Hodges MR, Klum L, Leekley T, Brozoski DT, Bastasic J, Davis S et al. (2004). Effects on breathing in awake and sleeping goats of focal acidosis in the medullary raphe. J Appl Physiol 96, 1815-1824.
15. Housley GD & Sinclair JD (1988). Localization by kainic acid lesions of neurones transmitting the carotid chemoreceptor stimulus for respiration in rat. J Physiol 406, 99-114.
16. Howe PR (1985). Blood pressure control by neurotransmitters in the medulla oblongata and spinal cord. J Auton Nerv Syst 12, 95-115.
17. Jacobs BL, Martin-Cora FJ & Fornal CA (2002). Activity of medullary serotonergic neurons in freely moving animals. Brain Res Brain Res Rev 40, 45-52.
18. Jelev A, Sood S, Liu H, Nolan P & Horner RL (2001). Microdialysis perfusion of 5-HT into hypoglossal motor nucleus differentially modulates genioglossus activity across natural sleep-wake states in rats. J Physiol 532, 467-481.
19. Kalia M, Fuxe K, Hokfelt T, Johansson O, Lang R, Ganten D et al. (1984). Distribution of neuropeptide immunoreactive nerve terminals within the subnuclei of the nucleus of the tractus solitarius of the rat. J Comp Neurol 222, 409-444.
20. Kia HK, Brisorgueil MJ, Hamon M, Calas A & Verge D (1996). Ultrastructural localization of 5-hydroxytryptamine1A receptors in the rat brain. J Neurosci Res 46, 697-708.
21. Kinney HC, Filiano JJ & White WF (2001). Medullary serotonergic network deficiency in the sudden infant death syndrome: review of a 15-year study of a single dataset. J Neuropathol Exp Neurol 60, 228-247.
22. Kirby LG, Pernar L, Valentino RJ & Beck SG (2003). Distinguishing characteristics of serotonin and non-serotonin-containing cells in the dorsal raphe nucleus: electrophysiological and immunohistochemical studies. Neuroscience 116, 669-683.
23. Lalley PM (1986). Serotoninergic and non-serotoninergic responses of phrenic motoneurones to raphe stimulation in the cat. J Physiol 380, 373-385.
24. 2 microdialysis in retrotrapezoid nucleus of the rat increases breathing in wakefulness but not in sleep. J Appl Physiol 87, 910-919.
25. Maskrey M (1990). Body temperature effects on hypoxic and hypercapnic responses in awake rats. Am J Physiol 259, R492-R498.
26. 2 response in newborn piglets. J Appl Physiol 96, 1909-1919.
27. Monti JM & Monti D (2000). Role of dorsal raphe nucleus serotonin 5-HT1A receptor in the regulation of REM sleep. Life Sci 66, 1999-2012.
28. Morrison SF (2004). Central pathways controlling brown adipose tissue thermogenesis. News Physiol Sci 19, 67-74.
29. Mulkey DK, Stornetta RL, Weston MC, Simmons JR, Parker A, Bayliss DA et al. (2004). Respiratory control by ventral surface chemoreceptor neurons in rats. Nat Neurosci 7, 1360-1369.
30. Nattie E (2000). Multiple sites for central chemoreception: their roles in response sensitivity and in sleep and wakefulness. Respir Physiol 122, 223-235.
31. 2 dialysis in the medullary raphe of the rat increases ventilation in sleep. J Appl Physiol 90, 1247-1257.
32. 2 dialysis in nucleus tractus solitarius region of rat increases ventilation in sleep and wakefulness. J Appl Physiol 92, 2119-2130.
33. Nattie EE & Li A (2002b). Substance P-saporin lesion of neurons with NK1 receptors in one chemoreceptor site in rats decreases ventilation and chemosensitivity. J Physiol 544, 603-616.
34. Nattie EE, Li A, Richerson G & Lappi DA (2004). Medullary serotonergic neurones and adjacent neurones that express neurokinin-1 receptors are both involved in chemoreception in vivo. J Physiol 556, 235-253.
35. Niblock MM, Kinney HC, Luce CJ, Belliveau RA & Filiano JJ (2004). The development of the medullary serotonergic system in the piglet. Auton Neurosci 110, 65-80.
36. Nitz DA & McNaughton BL (1999). Hippocampal EEG and unit activity responses to modulation of serotonergic median raphe neurons in the freely behaving rat. Learn Mem 6, 153-167.
37. Ootsuka Y, Blessing WW & McAllen RM (2004). Inhibition of rostral medullary raphe neurons prevents cold-induced activity in sympathetic nerves to rat tail and rabbit ear arteries. Neurosci Lett 357, 58-62.
38. Palkovits M, Mezey E, Eskay RL & Brownstein MJ (1986). Innervation of the nucleus of the solitary tract and the dorsal vagal nucleus by thyrotropin-releasing hormone-containing raphe neurons. Brain Res 373, 246-251.
39. Pappenheimer JR (1977). Sleep and respiration of rats during hypoxia. J Physiol 266, 191-207.
40. Paxinos G & Watson C (1982). The Rat Brain in Sterotaxic Coordinates. Academic Press, New York.
41. Perez H & Ruiz S (1995). Medullary responses to chemoreceptor activation are inhibited by locus coeruleus and nucleus raphe magnus. Neuroreport 6, 1373-1376.
42. Richerson GB, Wang W, Hodges MR, Dohle CI & Diez-Sampedro A (2005). Homing in on the specific phenotype (s) of central respiratory chemoreceptors. Exp Physiol 90, 259-266.
43. Richter DW, Schmidt-Garcon P, Pierrefiche O, Bischoff AM & Lalley PM (1999). Neurotransmitters and neuromodulators controlling the hypoxic respiratory response in anaesthetized cats. J Physiol 514, 567-578.
44. Schmidek WR, Hoshino K, Schmidek M & Timo-Iaria C (1972). Influence of environmental temperature on the sleep-wakefulness cycle in the rat. Physiol Behav 8, 363-371.
45. Semba K (1993). Aminergic and cholinergic afferents to REM sleep induction regions of the pontine reticular formation in the rat. J Comp Neurol 330, 543-556.
46. Smith JE, Jansen AS, Gilbey MP & Loewy AD (1998). CNS cell groups projecting to sympathetic outflow of tail artery: neural circuits involved in heat loss in the rat. Brain Res 786, 153-164.
47. 2. J Appl Physiol 97, 1763-1773.
48. Thor KB, Blitz-Siebert A & Helke CJ (1990). Discrete localization of high-density 5-HT1A binding sites in the midline raphe and parapyramidal region of the ventral medulla oblongata of the rat. Neurosci Lett 108, 249-254.
49. Thor KB & Helke CJ (1987). Serotonin- and substance P-containing projections to the nucleus tractus solitarii of the rat. J Comp Neurol 265, 275-293.
50. Vanhoenacker P, Haegeman G & Leysen JE (2000). 5-HT7 receptors: current knowledge and future prospects. Trends Pharmacol Sci 21, 70-77.
51. Voss MD, De Castro D, Lipski J, Pilowsky PM & Jiang C (1990). Serotonin immunoreactive boutons form close appositions with respiratory neurons of the dorsal respiratory group in the cat. J Comp Neurol 295, 208-218.
52. Wang W, Pizzonia JH & Richerson GB (1998). Chemosensitivity of rat medullary raphe neurones in primary tissue culture. J Physiol 511, 433-450.
53. Wang W, Tiwari JK, Bradley SR, Zaykin RV & Richerson GB (2001). Acidosis-stimulated neurons of the medullary raphe are serotonergic. J Neurophysiol 85, 2224-2235.
54. Young AA & Dawson NJ (1982). Evidence for on-off control of heat dissipation from the tail of the rat. Can J Physiol Pharmacol 60, 392-398.