Serotonin neurons and central respiratory chemoreception: Where are we now?

Progress in Brain Research

Volumn 209, Issue , 2014, Pages 207-233

  Teran, Frida A ^a   Massey, Cory A ^b   Richerson, George B ^b,c  

^a ST MARY'S UNIVERSITY   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

5 HT neurons; Acidosis; Chemoreceptors; Control of breathing; Hypercapnia; Raph

Indexed keywords

2,3 DIHYDRO 3 ISOPROPYL 2 OXO 1 BENZIMIDAZOLECARBOXYLIC ACID 3ALPHA TROPANYLAMIDE; SEROTONIN 1A RECEPTOR; SEROTONIN 2A RECEPTOR;

APNEA; AROUSAL; ARTICLE; BLOOD CARBON DIOXIDE TENSION; BRAIN CORTEX; BREATHING; BREATHING RATE; CARBON DIOXIDE TENSION; CENTRAL RESPIRATORY CHEMORECEPTION; CHEMORECEPTOR; CHEMOSENSITIVITY; CHEYNE STOKES BREATHING; CHRONIC OBSTRUCTIVE LUNG DISEASE; HIPPOCAMPUS; HUMAN; HYPERCAPNIA; HYPERPOLARIZATION; HYPERVENTILATION; HYPOVENTILATION; LOCUS CERULEUS; LUNG MINUTE VOLUME; LUNG VENTILATION; MOTONEURON; NERVE CELL PLASTICITY; NONHUMAN; PREOPTIC NUCLEUS; PRIORITY JOURNAL; REM SLEEP; RESPIRATION CONTROL; RESPIRATION DEPRESSION; SEROTONINERGIC NERVE CELL; SOLITARY TRACT NUCLEUS; WAKEFULNESS; ANIMAL; CHEMORECEPTOR CELL; PHYSIOLOGY; RESPIRATION CENTER; RESPIRATORY FUNCTION;

ANIMALS; CHEMORECEPTOR CELLS; HUMANS; RESPIRATORY CENTER; RESPIRATORY PHYSIOLOGICAL PROCESSES; SEROTONERGIC NEURONS;

EID: 84924719252     PISSN: 00796123     EISSN: 18757855     Source Type: Book Series    
DOI: 10.1016/B978-0-444-63274-6.00011-4     Document Type: Chapter

References (119)

1. Bach K.B., Mitchell G.S. Hypoxia-induced LTF of respiratory activity is 5-HT dependent. Respir. Physiol. 1996, 104:251-260.
2. Baker T.L., Mitchell G.S. Episodic but not continuous hypoxia elicits long-term facilitation of phrenic motor output in rats. J. Physiol. 2000, 529(1):215-219.
3. Baker-Herman T.L., Mitchell G.S. Phrenic long-term facilitation requires spinal serotonin receptor activation and protein synthesis. J. Neurosci. 2002, 22(14):6239-6246.
4. 2a receptors activated by serotonin and protein kinase C-mediated mechanisms. Proc. Natl. Acad. Sci. U.S.A. 2002, 99(22):14470-14475.
5. Bocchiaro C.M., Feldman J.L. Synaptic activity-independent persistent plasticity in endogenously active mammalian motoneurons. Proc. Natl. Acad. Sci. U.S.A. 2004, 101(12):4292-4295.
6. Bockaert J., Claeysen S., Becamel C., Dumuis A., Marin P. Neuronal 5-HT metabotropic receptors: fine-tuning of their structure, signaling, and roles in synaptic modulation. Cell Tissue Res. 2006, 326(2):553-572.
7. Bradley S.R., Pieribone V.A., Wang W., Severson C.A., Jacobs R.A., Richerson G.B. Chemosensitive serotonergic neurons are closely associated with large medullary arteries. Nat. Neurosci. 2002, 5(5):401-402.
8. Brandes I.F., Zuperku E.J., Stucke A.G., Jakovcevic D., Hopp F.A., Stuth E.A.E. Serotonergic modulation of inspiratory hypoglossal motoneurons in decerebrate dogs. J. Neurophysiol. 2006, 95(6):3449-3459.
9. Buchanan G.F., Richerson G.B. Role of chemoreceptors in mediating dyspnea. Respir. Physiol. Neurobiol. 2009, 167(1):9-19.
10. 2. Proc. Natl. Acad. Sci. U.S.A. 2010, 107(37):16354-16359.
11. Buchanan G.F., Hodges M.R., Richerson G.B. Contributions of Chemosensitive Serotonergic Neurons to Interactions Between the Sleep-Wake Cycle and Respiratory Control, Serotonin and Sleep: Molecular, Functional and Clinical Aspects 2008, 529-554. Birkhäuser Verlag, Switzerland.
12. Bulow K. Respiration and wakefulness in man. Acta physiol. Scand. Suppl. 1963, 209:1-110.
13. Cayetanot F., Gros F., Larnicol N. Postnatal changes in the respiratory response of the conscious rat to serotonin 2A/2C receptor activation are reflected in the developmental pattern of fos expression in the brainstem. Brain Res. 2002, 942(1-2):51-57.
14. Chaput Y., Lesieur P., Demontigny C. Effects of short-term serotonin depletion on the efficacy of serotonin neurotransmission-electrophysiological studies in the rat central nervous system. Synapse 1990, 6(4):328-337.
15. Conrad S.C., Nichols N.L., Ritucci N.A., Dean J.B., Putnam R.W. Development of chemosensitivity in neurons from the nucleus tractus solitarii (NTS) of neonatal rats. Respir. Physiol. Neurobiol. 2009, 166(1):4-12.
16. 2 chemoreception. Respir. Physiol. Neurobiol. 2009, 168(1-2):49-58.
17. 1a receptor activation on breathing in neonatal mice. J. Neurosci. 2014, 34:51-59.
18. Cummings K.J., Frappell P.B. Characterizing the breath-to-breath hypercapnic ventilatory response in neonatal rats. FASEB J. 2008, 22:955.9.
19. Dahan A., Teppema L.J. Influence of anaesthesia and analgesia on the control of breathing. Br. J. Anaesth. 2003, 91(1):40-49.
20. 2 sensitivity in rats. J. Appl. Physiol. 2006, 101(4):1097-1103.
21. Dean J.B., Bayliss D.A., Erickson J.T., Lawing W.L., Millhorn D.E. Depolarization and stimulation of neurons in nucleus tractus solitarii by carbon-dioxide does not require chemical synaptic input. Neuroscience 1990, 36(1):207-216.
22. Dekin M.S., Richerson G.B., Getting P.A. Thyrotropin-releasing-hormone induces rhythmic bursting in neurons of the nucleus tractus solitarius. Science 1985, 229(4708):67-69.
23. DePuy S.D., Kanbar R., Coates M.B., Stornetta R.L., Guyenet P.G. Control of breathing by raphe obscurus serotonergic neurons in mice. J. Neurosci. 2011, 31(6):1981-1990.
24. Dillon G.H., Waldrop T.G. In vitro responses of caudal hypothalamic neurons to hypoxia and hypercapnia. Neuroscience 1992, 51(4):941-950.
25. Doi A., Ramirez J.-M. State-dependent interactions between excitatory neuromodulators in the neuronal control of breathing. J. Neurosci. 2010, 30(24):8251-8262.
26. 3- in Cerebral Fluids, Ion Homeostasis of the Brain. The Regulation of Hydrogen and Potassium Ion Concentrations in Cerebral Intra- and Extracellular Fluids 1971, 175-185.
27. Fenik P., Veasey S.C. Pharmacological characterization of serotonergic receptor activity in the hypoglossal nucleus. Am. J. Respir. Crit. Care Med. 2003, 167(4):563-569.
28. Fiske B. Putative chemoreceptors get close to arteries. Nat. Neurosci. 2002, 5(5):396.
29. +. J. Appl. Physiol. 2010, 108(4):989-994.
30. Fuller D.D., Bach K.B., Baker T.L., Kinkead R., Mitchell G.S. Long term facilitation of phrenic motor output. Respir. Physiol. 2000, 121(2-3):135-146.
31. Gourine A.V., Kasymov V., Marina N., Tang F., Figueiredo M.F., Lane S., Teschemacher A.G., Spyer K.M., Deisseroth K., Kasparov S. Astrocytes control breathing through pH-dependent release of ATP. Science 2010, 329(5991):571-575.
32. Guyenet P.G., Stornetta R.L., Bayliss D.A., Mulkey D.K. Retrotrapezoid nucleus: a litmus test for the identification of central chemoreceptors. Exp. Physiol. 2005, 90(3):247-253.
33. Guyenet P.G., Stornetta R.L., Bayliss D.A. Retrotrapezoid nucleus and central chemoreception. J. Physiol. 2008, 586(8):2043-2048.
34. Guyenet P.G., Stornetta R.L., Bayliss D.A. Central respiratory chemoreception. J. Comp. Neurol. 2010, 518(19):3883-3906.
35. Haxhiu M.A., Tolentino-Silva F., Pete G., Ke P., Mack S.O. Monoaminergic neurons, chemosensation and arousal. Respir. Physiol. 2001, 129(1-2):191-209.
36. Hare G.M.T., Kavanagh B.P., Mazer C.D., Hum K.M., Kim S.Y., Coackley C., Barr A., Baker A.J. Hypercapnia increases cerebral tissue oxygen tension in anesthetized rats. Can. J. Anaesth. 2003, 50(10):1061-1068.
37. Hedner J., Hedner T., Wessberg P., Lundberg D., Jonason J. Effects of TRH and TRH analogs on the central regulation of breathing in the rat. Acta Physiol. Scand. 1983, 117(3):427-437.
38. Hirshman C.A., McCullough R.E., Cohen P.J., Weil J.V. Depression of hypoxic ventilatory response by halothane, enflurane and isoflurane in dogs. Br. J. Anaesth. 1977, 49(10):957-963.
39. Hodges M.R., Richerson G.B. Contributions of 5-HT neurons to respiratory control: neuromodulatory and trophic effects. Respir. Physiol. Neurobiol. 2008, 164(1-2):222-232.
40. Hodges M.R., Richerson G.B. Interaction between defects in ventilatory and thermoregulatory control in mice lacking 5-HT neurons. Respir. Physiol. Neurobiol. 2008, 164(3):350-357.
41. 2 chemoreception, and thermoregulation. J. Appl. Physiol. 2010, 108(5):1425-1432.
42. Hodges M.R., Tattersall G.J., Harris M.B., McEvoy S.D., Richerson D.N., Deneris E.S., Johnson R.L., Chen Z.-F., Richerson G.B. Defects in breathing and thermoregulation in mice with near-complete absence of central serotonin neurons. J. Neurosci. 2008, 28(10):2495-2505.
43. Hodges M.R., Wehner M., Aungst J., Smith J.C., Richerson G.B. Transgenic mice lacking serotonin neurons have severe apnea and high mortality during development. J. Neurosci. 2009, 29(33):10341-10349.
44. Jacobs B.L., Fornal C.A. Serotonin and motor activity. Curr. Opin. Neurobiol. 1997, 7(6):820-825.
45. 2 Sensitive and Insensitive Raphé Neurons. Soc. Neurosci. 2012, Abstr. 38, 897.08.
46. Johnson P.L., Hollis J.H., Moratalla R., Lightman S.L., Lowry C.A. Acute hypercarbic gas exposure reveals functionally distinct subpopulations of serotonergic neurons in rats. J. Psychopharmacol. 2005, 19(4):327-341.
47. Jouvet M. Sleep and serotonin: an unfinished story. Neuropsychopharmacology 1999, 21(2):S24-S27.
48. Kaczmarek L.K., Levitan I.B. What is neuromodulation?. Neuromodulation: The Biochemical Control of Neuronal Excitability 1987, 1-17. Oxford University Press, New York, NY. L.K. Kaczmarek, I.B. Levitan (Eds.).
49. 2 inhalation on 5-HT release in the dorsomedial medulla oblongata in infant. Neurosci. Res. 2007, 58:S162.
50. Kannurpatti S.S., Biswal B.B., Hudetz A.G. Baseline physiological state and the fMRI-BOLD signal response to apnea in anesthetized rats. NMR Biomed. 2003, 16(5):261-268.
51. Kinkead R., Mitchell G.S. Time-dependent hypoxic ventilatory responses in rats: effects of ketanserin and 5-carboxamidotryptamine. Am. J. Physiol. Regul. Integr. Comp. Physiol. 1999, 277(3):R658-R666.
52. Koo K.W., Sax D.S., Snider G.L. Arterial blood gases and pH during sleep in chronic obstructive pulmonary disease. Am. J. Med. 1975, 58(5):663-670.
53. Kubin L., Tojima H., Davies R.O., Pack A.I. Serotonergic excitatory drive to hypoglossal motoneurons in the decerebrate cat. Neurosci. Lett. 1992, 139(2):243-248.
54. Larnicol N., Wallois F., Berquin P., Gros F., Rose D. C-fos-like immunoreactivity in the cats neuroaxis following moderate hypoxia or hypercapnia. J. Physiol. Paris 1994, 88(1):81-88.
55. Lalley P.M., Benacka R., Bischoff A.M., Richter D.W. Nucleus raphe obscurus evokes 5-HT-1A receptor-mediated modulation of respiratory neurons. Brain Res. 1997, 747(1):156-159.
56. Lambertsen C.J. Chemical control of respiration at rest. Medical Physiology 1980, 1447-1487. Mosby Company, St. Louis, MO. 14th ed. V.B. Montcastle (Ed.).
57. Lovick T.A. The medullary raphe nuclei: a system for integration and gain control in autonomic and somatomotor responsiveness?. Exp. Physiol. 1997, 82(1):31-41.
58. 4a receptors avert opioid-induced breathing depression without loss of analgesia. Science 2003, 301(5630):226-229.
59. Mason P. Contributions of the medullary raphe and ventromedial reticular region to pain modulation and other homeostatic functions. Annu. Rev. Neurosci. 2001, 24:737-777.
60. Massey C.A., Wu Y., Richerson G.B. Isoflurane eliminates serotonin (5-HT) neuron chemosensitivity in vitro and markedly depresses the hypercapnic ventilatory response in vivo. Soc. Neurosci. 2012, Abstr. 38, 897.04.
61. Massey C.A., Wu Y., Zaykin A., Wang W., Hodges M.R., Wylie C.J., Deneris E.S., Richerson G.B. A novel pH-sensitive calcium-activated nonselective cation current is responsible for medullary raphe 5-HT neuron chemosensitivity. Soc. Neurosci. 2013, 39:656.04.
62. McGinty D.J., Harper R.M. Dorsal raphe neurons-depression of firing during sleep in cats. Brain Res. 1976, 101(3):569-575.
63. 2 response in newborn piglets. J. Appl. Physiol. 2004, 96(5):1909-1919.
64. Mitchell G.S., Smith C.A., Vidruk E.H. Effects of p-chlorophenylalanine on ventilatory control in goats. J. Appl. Physiol. 1983, 54:277-283.
65. Mitchell G.S., Baker T.L., Nanda S.A., Fuller D.D., Zabka A.G., Hodgeman B.A., Bavis R.W., Mack K.J., Olson E.B. Physiological and genomic consequences of intermittent hypoxia: invited review: intermittent hypoxia and respiratory plasticity. J. Appl. Physiol. 2001, 90(6):2466-2475.
66. Monckton J.E., McCormick D.A. Neuromodulatory role of serotonin in the ferret thalamus. J. Neurophysiol. 2002, 87(4):2124-2136.
67. + channels TASK-1 and -2. Pflugers Arch. 2003, 445(5):577-583.
68. Mueller R.A., Towle A.C., Breese G.R. Supersensitivity to the respiratory stimulatory effect of TRH in 5,7-dihydroxytryptamine-treated rats. Brain Res. 1984, 298(2):370-373.
69. Mulkey D.K., Stornetta R.L., Weston M.C., Simmons J.R., Parker A., Bayliss D.A., Guyenet P.G. Respiratory control by ventral surface chemoreceptor neurons in rats. Nat. Neurosci. 2004, 7(12):1360-1369.
70. Mulkey D.K., Rosin D.L., West G., Takakura A.C., Moreira T.S., Bayliss D.A., Guyenet P.G. Serotonergic neurons activate chemosensitive retrotrapezoid nucleus neurons by a pH-independent mechanism. J. Neurosci. 2007, 27(51):14128-14138.
71. Mulkey D.K., Talley E.M., Stornetta R.L., Siegel A.R., West G.H., Chen X., Sen N., Mistry A.M., Guyenet P.G., Bayliss D.A. TASK channels determine pH sensitivity in select respiratory neurons but do not contribute to central respiratory chemosensitivity. J. Neurosci. 2007, 27(51):14049-14058.
72. Nattie E.E.L.A., Richerson G.B., Lappi D.A. Medullary serotonergic neurones and adjacent neurones that express neurokinin-1 receptors are both involved in chemoreception in vivo. J. Physiol. 2004, 556:235-253.
73. Nichols N.L., Mulkey D.K., Wilkinson K.A., Powell F.L., Dean J.B., Putnam R.W. Characterization of the chemosensitive response of individual solitary complex neurons from adult rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009, 296(3):R763-R773.
74. Nink M., Krause U., Lehnert H., Heuberger W., Huber I., Schulz R., Hommel G., Beyer J. Thyrotropin-releasing-hormone has stimulatory effects on ventilation in humans. Acta Physiol. Scand. 1991, 141(3):309-318.
75. Olson E.B., Dempsey J.A., McCrimmon D.R. Serotonin and the control of ventilation in awake rats. J. Clin. Invest. 1979, 64:689-693.
76. Patel A.J., Honore E., Lesage F., Fink M., Romey G., Lazdunski M. Inhalational anesthetics activate two-pore-domain background K+ channels. Nat. Neurosci. 1999, 2(5):422-426.
77. Pena F., Ramirez J.M. Endogenous activation of serotonin-2A receptors is required for respiratory rhythm generation in vitro. J. Neurosci. 2002, 22(24):11055-11064.
78. Penatti E.M., Berniker A.V., Kereshi B., Cafaro C., Kelly M.L., Niblock M.M., Gao H.G., Kinney H.C., Li A., Nattie E.E. Ventilatory response to hypercapnia and hypoxia after extensive lesion of medullary serotonergic neurons in newborn conscious piglets. J. Appl. Physiol. 2006, 101(4):1177-1188.
79. 2-induced c-Fos expression in brainstem preprotachykinin mRNA containing neurons. Respir. Physiol. Neurobiol. 2002, 130(3):265-274.
80. Pineda J., Aghajanian G.K. Carbon dioxide regulates the tonic activity of locus coeruleus neurons by modulating a proton- and polyamine-sensitive inward rectifier potassium current. Neuroscience 1997, 77(3):723-743.
81. Ptak K., Yamanishi T., Aungst J., Milescu L.S., Zhang R., Richerson G.B., Smith J.C. Raphe neurons stimulate respiratory circuit activity by multiple mechanisms via endogenously released serotonin and substance P. J. Neurosci. 2009, 29(12):3720-3737.
82. Rajan S., Wischmeyer E., Liu G.X., Muller R.P., Daut J., Karschin A., Derst C. TASK-3, a novel tandem pore domain acid-sensitive K+ channel-an extracellular histidine as pH sensor. J. Biol. Chem. 2000, 275(22):16650-16657.
83. Ray R.S., Corcoran A.E., Brust R.D., Kim J.C., Richerson G.B., Nattie E., Dymecki S.M. Impaired respiratory and body temperature control upon acute serotonergic neuron inhibition. Science 2011, 333(6042):637-642.
84. Reader T.A., Gauthier P. Catecholamines and serotonin in the rat central nervous system after 6-OHDA, 5-7-DHT and P-CPA. J. Neural Transm. 1984, 59(3):207-227.
85. 2 of neurons in the rostral ventral medulla in vitro. J. Neurophysiol. 1995, 73(3):933-944.
86. Richerson G.B. pH effects on respiratory neurons. pH and Brain Function 1998, John Wiley & Sons, New York, NY. K. Kaila, B.R. Ransom (Eds.).
87. Richerson G.B. Serotonergic neurons as carbon dioxide sensors that maintain pH homeostasis. Nat. Rev. Neurosci. 2004, 5(6):449-461.
88. Richerson G.B., Wang W.G., Tiwari J., Bradley S.R. Chemo sensitivity of serotonergic neurons in the rostral ventral medulla. Respir. Physiol. 2001, 129(1-2):175-189.
89. Richerson G.B., Wang W., Hodges M.R., Dohle C.I., Diez-Sampedro A. Homing in on the specific phenotype(s) of central respiratory chemoreceptors. Exp. Physiol. 2005, 90(3):259-266. discussion 266-9.
90. Richerson, G.B., Wu, Y., Hodges, M.R., Wang, W., Zaykin, A.J.W.C., Deneris, E.S. 2009. Acidosis Inhibits a Calcium-Activated Non-selective Cation Current in Mature Serotonergic Neurons (Nara, Trans.), Japan.
91. Richter D.W., Manzke T., Wilken B., Ponimaskin E. Serotonin receptors: guardians of stable breathing. Trends Mol. Med. 2003, 9(12):542-548.
92. Sahibzada N., Ferreira M., Wasserman A.M., Taveira-Dasilva A.M., Gillis R.A. Reversal of morphine-induced apnea in the anesthetized rat by drugs that activate 5-hydroxytryptamine(1A) receptors. J. Pharmacol. Exp. Ther. 2000, 292(2):704-713.
93. Saper C.B., Scammell T.E., Lu J. Hypothalamic regulation of sleep and circadian rhythms. Nature 2005, 437(7063):1257-1263.
94. 2 chemoreceptor neuron identification by c-fos immunocytochemistry. J. Appl. Physiol. 1992, 73:96-100.
95. Serra A., Brozoski D., Hedin N., Franciosi R., Forster H.V. Mortality after carotid body denervation in rats. J. Appl. Physiol. 2001, 91(3):1298-1306.
96. Severson C.A., Wang W., Pieribone V.A., Dohle C.I., Richerson G.B. Midbrain serotonergic neurons are central pH chemoreceptors. Nat. Neurosci. 2003, 6(11):1139-1140.
97. Sirois J.E., Lei Q.B., Talley E.M., Lynch C., Bayliss D.A. The TASK-1 two-pore domain K+ channel is a molecular substrate for neuronal effects of inhalation anesthetics. J. Neurosci. 2000, 20(17):6347-6354.
98. Smith J.C., Morrison D.E., Ellenberger H.H., Otto M.R., Feldman J.L. Brainstem projections to the major respiratory neuron populations in the medulla of the cat. J. Comp. Neurol. 1989, 281(1):69-96.
99. 2 in unanesthetized intact dogs: central vs. peripheral chemoreceptors. J. Appl. Physiol. 2006, 100(1):13-19.
100. Somjen G.G., Tombaugh G.C. pH modulation of neuronal excitability and central nervous system functions. pH and Brain Function 1998, Wiley-Liss, New York. K. Kaila, B.R. Ransom (Eds.).
101. Steriade M., McCormick D.A., Sejnowski T.J. Thalamocortical oscillations in the sleeping and aroused brain. Science 1993, 262(5134):679-685.
102. Stunden C.E., Filosa J.A., Garcia A.J., Dean J.B., Putnam R.W. Development of in vivo ventilatory and single chemosensitive neuron responses to hypercapnia in rats. Respir. Physiol. 2001, 127(2-3):135-155.
103. 2-sensitive neurons in rats. J. Physiol. 2006, 572(2):503-523.
104. Talley E.M., Solorzano G., Lei Q.B., Kim D., Bayliss D.A. CNS distribution of members of the two-pore-domain (KCNK) potassium channel family. J. Neurosci. 2001, 21(19):7491-7505.
105. Taverna S., Tkatch T., Metz A.E., Martina M. Differential expression of TASK channels between horizontal interneurons and pyramidal cells of rat hippocampus. J. Neurosci. 2005, 25(40):9162-9170.
106. Taylor N.C., Li A., Nattie E.E. Medullary serotonergic neurones modulate the ventilatory response to hypercapnia, but not hypoxia in conscious rats. J. Physiol. 2005, 566(Pt. 2):543-557.
107. Trulson M.E., Jacobs B.L. Raphe unit-activity in freely moving cats-correlation with level of behavioral arousal. Brain Res. 1979, 163(1):135-150.
108. Veasey S.C., Fornal C.A., Metzler C.W., Jacobs B.L. Response of serotonergic caudal raphe neurons in relation to specific motor activities in freely moving cats. J. Neurosci. 1995, 15(7):5346-5359.
109. Veasey S.C., Fornal C.A., Metzler C.W., Jacobs B.L. Single-unit responses of serotonergic dorsal raphe neurons to specific motor challenges in freely moving cats. Neuroscience 1997, 79(1):161-169.
110. Wang W., Richerson G.B. Development of chemosensitivity of rat medullary raphe neurons. Neuroscience 1999, 90(3):1001-1011.
111. Wang W.A., Richerson G.B. Chemosensitivity of non-respiratory rat CNS neurons in tissue culture. Brain Res. 2000, 860(1-2):119-129.
112. Wang W.G., Pizzonia J.H., Richerson G.B. Chemosensitivity of rat medullary raphe neurones in primary tissue culture. J. Physiol. 1998, 511(2):433-450.
113. Wang W.G., Tiwari J.K., Bradley S.R., Zaykin A.V., Richerson G.B. Acidosis-stimulated neurons of the medullary raphe are serotonergic. J. Neurophysiol. 2001, 85(5):2224-2235.
114. 2. J. Physiol. 2002, 540(3):951-970.
115. Wang S., Benamer N., Zanella S., Kumar N.N., Shi Y., Bevengut M., Penton D., Guyenet P.G., Lesage F., Gestreau C., Barhanin J., Bayliss D.A. TASK-2 channels contribute to pH sensitivity of retrotrapezoid nucleus chemoreceptor neurons. J. Neurosci. 2013, 33(41):16033-16044.
116. Washburn C.P., Sirois J.E., Talley E.M., Guyenet P.G., Bayliss D.A. Serotonergic raphe neurons express TASK channel transcripts and a TASK-like pH-and halothane-sensitive K+ conductance. J. Neurosci. 2002, 22(4):1256-1265.
117. Wu Y., Hodges M.R., Richerson G.B. Stimulation by Hypercapnic Acidosis in Mouse 5-HT Neurons is Enhanced by Age and Increased Temperature. Soc. Neurosci. 2008, Abstr. 34, 383.9.
118. Yamamoto Y., Lagercrantz H., Voneuler C. Effects of substance P and TRH on ventilation and pattern of breathing in newborn rabbits. Acta Physiol. Scand. 1981, 113(4):541-543.
119. Zhao Z.-Q., Scott M., Chiechio S., Wang J.-S., Renner K.J., Gereau R.W., Johnson R.L., Deneris E.S., Chen Z.-F. Lmx1b is required for maintenance of central serotonergic neurons and mice lacking central serotonergic system exhibit normal locomotor activity. J. Neurosci. 2006, 26(49):12781-12788.