Medullary serotonin neurons are CO2 sensitive in situ

Journal of Neurophysiology

Volumn 110, Issue 11, 2013, Pages 2536-2544

  Iceman, Kimberly E ^a   Richerson, George B ^b,c   Harris, Michael B ^a  

^a UNIVERSITY OF ALASKA FAIRBANKS   (United States)

^b UNIVERSITY OF IOWA HOSPITALS AND CLINICS   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Breathing; Chemosensitivity; Raph ; Serotonin

Indexed keywords

CARBON DIOXIDE; TRYPTOPHAN HYDROXYLASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN STEM; BREATHING; CHEMORECEPTOR; CHEMOSENSITIVITY; HYPERCAPNIA; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MALE; NONHUMAN; PRIORITY JOURNAL; RAPHE NUCLEUS; RAT; RESPIRATION CONTROL; SEROTONINERGIC NERVE CELL;

BREATHING; CHEMOSENSITIVITY; RAPHÉ; SEROTONIN;

ACTION POTENTIALS; ANIMALS; CARBON DIOXIDE; CHEMORECEPTOR CELLS; MALE; MEDULLA OBLONGATA; RAPHE NUCLEI; RATS; RATS, SPRAGUE-DAWLEY; SEROTONERGIC NEURONS;

EID: 84888631504     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00288.2013     Document Type: Article

References (85)

1. Allers KA, Sharp T. Neurochemical and anatomical identification of fast-and slow-firing neurones in the rat dorsal raphé nucleus using juxtacellular labelling methods in vivo. Neuroscience 122: 193-204, 2003.
2. Azmitia EC. Serotonin and brain: evolution, neuroplasticity, and homeostasis. Int Rev Neurobiol 77: 31-56, 2007.
3. Bang SJ, Jensen P, Dymecki SM, Commons KG. Projections and interconnections of genetically defined serotonin neurons in mice. Eur J Neurosci 35: 85-96, 2011.
4. Barrett KT, Kinney HC, Li A, Daubenspeck JA, Leiter JC, Nattie EE. Subtle alterations in breathing and heart rate control in the 5-HT1A receptor knockout mouse in early postnatal development. J Appl Physiol 113: 1585-1593, 2012.
5. Brust RD, Richerson GB, Wu Y, Dymecki SM. Mapping chemosensitivity onto genetically-defined serotonergic neuron subtypes (Online). Program no. 188.16. 2010 Neuroscience Meeting Planner. San Diego, CA: Society for Neuroscience, 2010.
6. 2. Proc Natl Acad Sci USA 107: 16354-16359, 2010.
7. Calizo LH, Akanwa A, Ma X, Pan YZ, Lemos JC, Craige C, Heemstra LA, Beck SG. Raphé serotonin neurons are not homogenous: electrophysiological, morphological and neurochemical evidence. Neuropharmacology 61: 524-543, 2011.
8. 2 chemoreception. Respir Physiol Neurobiol 168: 49-58, 2009.
9. Corcoran AE, Richerson GB, Harris MB. Serotonergic mechanisms are necessary for central respiratory chemoresponsiveness in situ. Respir Physiol Neurobiol 186: 214-220, 2013.
10. Cummings KJ, Hewitt JC, Li A, Daubenspeck JA, Nattie EE. Postnatal loss of brainstem serotonin neurones compromises the ability of neonatal rats to survive episodic severe hypoxia. J Physiol 589: 5247-5256, 2011a.
11. Cummings KJ, Commons KG, Hewitt JC, Daubenspeck JA, Li A, Kinney HC, Nattie EE. Failed heart rate recovery at a critical age in 5-HT-deficient mice exposed to episodic anoxia: Implications for SIDS. J Appl Physiol 111: 825-833, 2011b.
12. Dahlström A, Fuxe K. Evidence for the existence of monoamine-containing neurons in the central nervous system. I. Demonstration of monoamines in the cell bodies of brainstem neurons. Acta Physiol Scan Suppl 232: 1-55, 1964.
13. 2 and central chemoreception in the control of breathing in the fetus and the neonate. Respir Physiol Neurobiol 173: 201-212, 2010.
14. Dekin MS, Richerson GB, Getting PA. Thyrotropin-releasing hormone induces rhythmic bursting in neurons of the nucleus tractus solitarius. Science 229: 67-69, 1985.
15. DePuy SD, Kanbar R, Coates MB, Stornetta RL, Guyenet PG. Control of breathing by raphé obscurus serotonergic neurons in mice. J Neurosci 31: 1981-1990, 2011.
16. 2. J Appl Physiol 103: 1780-1788, 2007.
17. Doi A, Ramirez JM. Neuromodulation and the orchestration of the respiratory rhythm. Respir Physiol Neurobiol 164: 96-104, 2008.
18. Duncan JR, Paterson DS, Hoffman JM, Mokler DJ, Borenstein NS, Belliveau RA, Krous HF, Haas EA, Stanley C, Nattie EE, Trachtenberg FL, Kinney HC. Brainstem serotonergic deficiency in sudden infant death syndrome. JAMA 303: 430-437, 2010.
19. Erickson JT, Shafer G, Rossetti MD, Wilson CG, Deneris ES. Arrest of 5HT neuron differentiation delays respiratory maturation and impairs neonatal homeostatic responses to environmental challenges. Respir Physiol Neurobiol 159: 85-101, 2007.
20. Feldman JL, Mitchell GS, Nattie EE. 2003 Breathing: rhythmicity, plasticity, chemosensitivity. Annu Rev Neurosci 26: 239-266, 2003.
21. Fornal C, Auerbach S, Jacobs BL. Activity of serotonin-containing neurons in nucleus raphe magnus in freely moving cats. Exp Neurol 88: 590-608, 1985.
22. Guyenet PG, Stornetta RL, Bayliss DA. Retrotrapezoid nucleus and central chemoreception. J Physiol 586: 2043-2048, 2008.
23. Guyenet PG, Stornetta RL, Bayliss DA, Mulkey DK. Retrotrapezoid nucleus: a litmus test for the identification of central chemoreceptors. Exp Physiol 90: 247-253; discussion 253-257; 2005.
24. Guyenet PG, Stornetta RL, Bayliss DA. Central respiratory chemoreception. J Comp Neurol 518: 3883-3906, 2010.
25. Guyenet PG, Abbott SB, Stornetta RL. The respiratory chemoreception conundrum: light at the end of the tunnel? Brain Res 1511: 126-137, 2012.
26. Hajós M, Allers, KA, Jennings K, Sharp T, Charette G, Sk A, Kocsis B. Neurochemical identification of stereotypic burst-firing neurons in the rat dorsal raphé nucleus using juxtacellular labelling methods. Eur J Neurosci 25: 119-126, 2007.
27. Harper RM, Macey PM, Woo MA, Macey KE, Keens TG, Gozal D, Alger JR. Hypercapnic exposure in congenital central hypoventilation syndrome reveals CNS respiratory control mechanisms. J Neurophysiol 93: 1647-1658, 2005.
28. Haxhiu MA, Tolentino-Silva F, Pete G, Kc P, Mack SO. Monoaminergic neurons, chemosensation and arousal. Respir Physiol 129: 191-209, 2001.
29. Hilaire G, Voituron N, Menuet C, Ichiyama RM, Subramanian HH, Dutschmann M. The role of serotonin in respiratory function and dysfunction. Respir Physiol Neurobiol 174: 76-88, 2010.
30. Hodges MR, Richerson GB. Medullary serotonin neurons and their roles in central respiratory chemoreception. Respir Physiol Neurobiol 173: 256-263, 2010.
31. Hodges MR, Tattersall GJ, Harris MB, McEvoy SD, Richerson DN, Deneris ES, Johnson RL, Chen ZF, Richerson GB. Defects in breathing and thermoregulation in mice with near-complete absence of central serotonin neurons. J Neurosci 28: 2495-2505, 2008.
32. Hodges MR, Klum L, Leekley T, Brozoski DT, Bastasic J, Davis S, Wenninger JM, Feroah TR, Pan LG, Forster HV. Effects on breathing in awake and sleeping goats of focal acidosis in the medullary raphe. J Appl Physiol 96: 1815-1824, 2004.
33. Hodges MR, Wehner M, Aungst J, Smith JC, Richerson GB. Transgenic mice lacking serotonin neurons have severe apnea and high mortality during development. J Neurosci 29: 10341-10349, 2009.
34. Hodges MR, Best S, Richerson GB. Altered ventilatory and thermoregulatory control in male and female adult Pet-1 null mice. Respir Physiol Neurobiol 177: 133-140, 2011.
35. Jacobs BL, Azmitia EC. Structure and function of the brain serotonin system. Physiol Rev 72: 165-229, 1992.
36. Jacobs BL, Fornal CA. Serotonin and motor activity. Curr Opin Neurobiol 7: 820-825, 1997.
37. Jacobs BL, Martn-Cora FJ, Fornal CA. Activity of medullary serotonergic neurons in freely moving animals. Brain Res Brain Res Rev 40: 45-52, 2002.
38. Jensen P, Farago AF, Awatramani RB, Scott MM, Deneris ES, Dymecki SM. Redefining the serotonergic system by genetic lineage. Nat Neurosci 11: 417-419, 2008.
39. 2 sensitive and insensitive raphé neurons (Online). Program no. 897.08. 2012 Neuroscience Meeting Planner. New Orleans, LA: Society for Neuroscience, 2012.
40. Johnson PL, Hollis JH, Moratalla R, Lightman SL, Lowry CA. Acute hypercarbic gas exposure reveals functionally distinct subpopulations of serotonergic neurons in rats. J Psychopharmacol 19: 327-341, 2005.
41. Kinney HC. Brainstem mechanisms underlying the sudden infant death syndrome: evidence from human pathologic studies. Dev Psychobiol 51: 223-233, 2009.
42. Kinney HC, Thach BT. The sudden infant death syndrome. N Engl J Med 361: 795-805, 2009.
43. Kinney HC, Richerson GB, Dymecki SM, Darnall RA, Nattie EE. The brainstem and serotonin in the sudden infant death syndrome. Annu Rev Pathol 4: 517-550, 2009.
44. Kinney HC, Broadbelt KG, Haynes RL, Rognum IJ, Paterson DS. The serotonergic anatomy of the developing human medulla oblongata: Implications for pediatric disorders of homeostasis. J Chem Neuroanat 41: 182-199, 2011.
45. Kirby LG, Pernar L, Valentino RJ, Beck SG. Distinguishing characteristics of serotonin and non-serotonin-containing cells in the dorsal raphé nucleus: electrophysiological and immunohistochemical studies. Neuroscience 116: 669-683, 2003.
46. Kiyasova V, Gaspar P. Development of raphé serotonin neurons from specification to guidance. Eur J Neurosci 34: 1553-1562, 2011.
47. Kiyasova V, Fernandez SP, Laine J, Stankovski L, Muzerelle A, Doly S, Gaspar AP. Genetically defined morphologically and functionally unique subset of 5-ht neurons in the mouse raphé nuclei. J Neurosci 31: 2756-2768, 2011.
48. Kocsis B, Varga V, Dahan L, Sik A. Serotonergic neuron diversity: identification of raphé neurons with discharges time-locked to the hippocampal theta rhythm. Proc Natl Acad Sci USA 103: 1059-1064, 2006.
49. Larnicol N, Wallois F, Berquin P, Gros F, Rose D. C-fos-like immunoreactivity in the cat's neuraxis following moderate hypoxia or hypercapnia. J Physiol (Paris) 88: 81-88, 1994.
50. Li A, Nattie E. Serotonin transporter knockout mice have a reduced ventilatory response to hypercapnia. J Physiol 586: 2321-2329, 2008.
51. Madden CJ, Morrison SF. Serotonin potentiates sympathetic responses evoked by spinal NMDA. J Physiol 577: 525-537, 2006.
52. Mason P. Physiological identification of pontomedullary serotonergic neurons in the rat. J Neurophysiol 77: 1087-1098, 1997.
53. Mason P. 2011 From descending pain modulation to obesity via the medullary raphé. Pain 152: S20-4, 2011.
54. Massey CA, Richerson GB, Wu Y. Isoflurane eliminates serotonin (5-HT) neuron chemosensitivity in vitro and markedly depresses the hypercapnic ventilatory response in vivo (Online). Program no. 897.04. 2012 Neuroscience Meeting Planner. New Orleans, LA: Society for Neuroscience, 2012.
55. Mulkey DK, Stornetta RL, Weston MC, Simmons JR, Parker A, Bayliss DA, Guyenet PG. Respiratory control by ventral surface chemoreceptor neurons in rats. Nat Neurosci 7: 1360-1369, 2004.
56. Nakamura K, Hasegawa H. Developmental role of tryptophan hydroxylase in the nervous system. Mol Neurobiol 35: 45-54, 2007.
57. Nattie E, Li A. Central chemoreception is a complex system function that involves multiple brain stem sites. J Appl Physiol 106: 1464-1466, 2009.
58. Nattie EE, Li A, Richerson GB, Lappi DA. Medullary serotonergic neurones and adjacent neurones that express neurokinin-1 receptors are both involved in chemoreception in vivo. J Physiol 556: 235-253, 2004.
59. Paterson DS, Trachtenberg FL, Thompson EG, Belliveau RA, Beggs AH, Darnall R, Chadwick AE, Krous HF, Kinney HC. Multiple serotonergic brainstem abnormalities in sudden infant death syndrome. JAMA 296: 2124-2132, 2006.
60. Paxinos G, Watson AC. Stereotaxic Atlas of the Rat Brain. New York: Academic, 1998.
61. 2 at postnatal ages P15 and P25. Respir Physiol Neurobiol 177: 6165, 2011a.
62. Penatti EM, Barina AE, Raju SC, Li A, Kinney HC, Commons KG, Nattie EE. Maternal dietary tryptophan deficiency alters cardiorespiratory control in rat pups. J Appl Physiol 110: 318-328, 2011b.
63. 2-induced c-Fos expression in brainstem preprotachykinin mRNA containing neurons. Respir Physiol Neurobiol 130: 265-274, 2002.
64. Pinault D. A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellularly labeled thalamic cells and other central neurons with biocytin or Neurobiotin. J Neurosci Methods 65: 113-136, 1996.
65. Ptak K, Yamanishi T, Aungst J, Milescu LS, Zhang R, Richerson GB, Smith JC. Raph neurons stimulate respiratory circuit activity by multiple mechanisms via endogenously released serotonin and substance P. J Neurosci 29: 3720-3737, 2009.
66. 2 and acid signaling in chemosensitive neurons. Am J Physiol Cell Physiol 287: C1493-C1526, 2004.
67. Ray RS, Corcoran AE, Brust RD, Kim JC, Richerson GB, Nattie E, Dymecki SM. Impaired respiratory and body temperature control upon acute serotonergic neuron inhibition. Science 333: 637-642, 2011.
68. Richerson GB. Serotonergic neurons as carbon dioxide sensors that maintain pH homeostasis. Nat Rev Neurosci 5: 449-461, 2004.
69. Richerson GB. Respiratory plasticity in sleep apnoea: should it be harnessed or restrained? J Physiol 588: 3-4, 2010.
70. Richerson GB, Wang W, Tiwari J, Bradley SR. Chemosensitivity of serotonergic neurons in the rostral ventral medulla. Respir Physiol 129: 175-189, 2001.
71. Richerson GB, Wang W, Hodges MR, Dohle CI, Diez-Sampedro A. Homing in on the specific phenotype(s) of central respiratory chemoreceptors. Exp Physiol 90: 259-266; discussion 266-269; 2005.
72. Schweimer JV, Ungless MA. Phasic responses in dorsal raphé serotonin neurons to noxious stimuli. Neuroscience 171: 1209-1215, 2010.
73. Severson CA, Wang W, Pieribone VA, Dohle CI, Richerson GB. Midbrain serotonergic neurons are central pH chemoreceptors. Nat Neurosci 6: 1139-1140, 2003.
74. Sowers LP, Massey CA, Gehlbach BK, Granner MA, Richerson GB. Sudden unexpected death in epilepsy: Fatal post-ictal respiratory and arousal mechanisms. Respir Physiol Neurobiol pii: S1569-9048, 2013.
75. Takakura AC, Moreira TS. Arterial chemoreceptor activation reduces the activity of parapyramidal serotonergic neurons in rats. Neuroscience 237C: 199-207, 2013.
76. Taylor NC, Li A, Nattie EE. Medullary serotonergic neurones modulate the ventilatory response to hypercapnia, but not hypoxia in conscious rats. J Physiol 566: 543-557, 2005.
77. Toppin VAL, Harris MB, Kober AM, Leiter JC, St-John WM. Persistence of eupnea and gasping following blockade of both serotonin type 1 and 2 receptors in the in situ juvenile rat preparation. J Appl Physiol 103: 220-227, 2007.
78. Veasey SC, Fornal CA, Metzler CW, Jacobs BL. Response of serotonergic caudal raphé neurons in relation to specific motor activities in freely moving cats. J Neurosci 15: 5346-5359, 1995.
79. Veasey SC, Fornal CA, Metzler CW, Jacobs BL. Single-unit responses of serotonergic dorsal raphé neurons to specific motor challenges in freely moving cats. Neuroscience 79: 161-169, 1997.
80. Wallace JA, Lauder JM. Development of the serotonergic system in the rat embryo: an immunocytochemical study. Brain Res Bull 10: 459-479, 1983.
81. Wang W, Pizzonia JH, Richerson GB. Chemosensitivity of rat medullary raphé neurones in primary tissue culture. J Physiol 51: 433-450, 1998.
82. Wang W, Tiwari JK, Bradley SR, Zaykin RV, Richerson GB. Acidosis stimulated neurons of the medullary raphé are serotonergic. J Neurophysiol 85: 2224-2235, 2001.
83. 2 and pH of the working heart-brain stem preparation during vascular perfusion with aqueous medium. Am J Physiol Regul Integr Comp Physiol 281: R528-R538, 2001.
84. Winkler CW, Hermes SM, Chavkin CI, Drake CT, Morrison SF, Aicher SA. Kappa opioid receptor (KOR) and GAD67 immunoreactivity are found in OFF and NEUTRAL cells in the rostral ventromedial medulla. J Neurophysiol 96: 3465-3473, 2006.
85. Wylie CJ, Hendricks TJ, Zhang B, Wang L, Lu P, Leahy P, Fox S, Maeno H, Deneris ES. Distinct transcriptomes define rostral and caudal serotonin neurons. J Neurosci 30: 670-684, 2010.