A group of non-serotonergic cells is CO2-stimulated in the medullary raphé

Neuroscience

Volumn 259, Issue , 2014, Pages 203-213

  Iceman, K E ^a   Harris, M B ^a  

^a UNIVERSITY OF ALASKA FAIRBANKS   (United States)

Author keywords

Breathing; Chemosensitivity; Raph ; Serotonin

Indexed keywords

CARBON DIOXIDE; NEUROKININ 1 RECEPTOR; TRYPTOPHAN HYDROXYLASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL LABELING; CELL STIMULATION; CHEMOSENSITIVITY; CONTROLLED STUDY; ENZYME SYNTHESIS; HYPERCAPNIA; IMMUNOHISTOCHEMISTRY; JUVENILE ANIMAL; MALE; NERVE CELL NETWORK; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAPHE NUCLEUS; RAT; SEROTONINERGIC NERVE CELL;

5-HT; ANALYSIS OF VARIANCE; ANOVA; BREATHING; CHEMOSENSITIVITY; NEUROKININ-1 RECEPTOR; NK1R; RAPHÉ; SEROTONIN; SEROTONIN SYNTHESIZING; TPH; TRYPTOPHAN HYDROXYLASE;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; CARBON DIOXIDE; DOSE-RESPONSE RELATIONSHIP, DRUG; NEURONS; RAPHE NUCLEI; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, NEUROKININ-1; SEROTONIN; TRYPTOPHAN HYDROXYLASE;

EID: 84891587846     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.11.060     Document Type: Article

References (75)

1. A receptors. Electrophysiological and microdialysis studies. Synapse. 2000, 36:2134.
2. Allers K.A., 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 2003, 122:193-204.
3. Bagdy E., Kiraly I., Harsing L.G. Reciprocal innervation between serotonergic and GABAergic neurons in raphé nuclei of the rat. Neurochem Res 2000, 25:1465-1473.
4. 2C receptors inhibit 5-HT neuronal activity via a GABAergic mechanism. Br J Pharmacol 2006, 149:861-869.
5. B receptor site distribution in the rat central nervous system. Neuroscience 1987, 20:365-383.
6. 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, 5:401-402.
7. A receptor binding in the medullary serotonergic system in the sudden infant death syndrome. J Neuropathol Exp Neurol 2011, 70:799-810.
8. Calizo L.H., Akanwa A., Ma X., Pan Y.-Z., Lemos J.C., Craige C., Heemstra L.A., Beck S.G. Raphé serotonin neurons are not homogenous: electrophysiological, morphological and neurochemical evidence. Neuropharmacology 2011, 61:524-543.
9. Cao W.-H., Morrison S.F. Brown adipose tissue thermogenesis contributes to fentanyl-evoked hyperthermia. Am J Physiol Regul Integr Comp Physiol 2005, 288:R723. 32.
10. Cao Y., Fujito Y., Matsuyama K., Aoki M. Effects of electrical stimulation of the medullary raphé nuclei on respiratory movement in rats. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2006, 192:497-505.
11. Charara A., Parent A. Chemoarchitecture of the primate dorsal raphé nucleus. J Chem Neuroanat 1998, 15:111-127.
12. Chen L.W., Wei L.C., Liu H.L., Rao Z.R. Noradrenergic neurons expressing substance P receptor (NK1) in the locus coeruleus complex: a double immunofluorescence study in the rat. Brain Res 2000, 873:155-159.
13. Commons K.G. Locally collateralizing glutamate neurons in the dorsal raphé nucleus responsive to substance P contain vesicular glutamate transporter 3 (VGLUT3). J Chem Neuroanat 2009, 38:273-281.
14. 2 chemoreception. Respir Physiol Neurobiol 2009, 168:49-58.
15. Corcoran A.E., Richerson G.B., Harris M.B. Serotonergic mechanisms are necessary for central respiratory chemoresponsiveness in situ. Respir Physiol Neurobiol 2013, 186:214-220.
16. DePuy S.D., Kanbar R., Coates M.B., Stornetta R.L., Guyenet P.G. Control of breathing by raphé obscurus serotonergic neurons in mice. J Neurosci 2011, 31:1981-1990.
17. DiMicco J.A., Sarkar S., Zaretskaia M.V., Zaretsky D.V. Stress-induced cardiac stimulation and fever: common hypothalamic origins and brainstem mechanisms. Auton Neurosci 2006, 126-127:106-119.
18. Doi A., Ramirez J.-M. State-dependent interactions between excitatory neuromodulators in the neuronal control of breathing. J Neurosci 2010, 30:8251-8262.
19. Fornal C., Auerbach S., Jacobs B.L. Activity of serotonin-containing neurons in nucleus raphé magnus in freely moving cats. Exp Neurol 1985, 88:590-608.
20. Gallager D.W., Aghajanian G.K. Effect of antipsychotic drugs on the firing of dorsal raphé cells. II. Reversal by picrotoxin. Eur J Pharm 1976, 39:357-364.
21. Gaspar P., Lillesaar C. Probing the diversity of serotonin neurons. Philos Trans R Soc Lond B Biol Sci 2012, 367:2382-2394.
22. Gray P.A., Janczewski W.A., Mellen N., McCrimmon D.R., Feldman J.L. Normal breathing requires preBötzinger complex neurokinin-1 receptor-expressing neurons. Nat Neurosci 2001, 4:927-930.
23. Haxhiu M.A., Tolentino-Silva F., Pete G., Kc P., Mack S.O. Monoaminergic neurons, chemosensation and arousal. Respir Physiol 2001, 129:191-209.
24. Hellman K.M., Brink T.S., Mason P. Activity of murine raphé magnus cells predicts tachypnea and on-going nociceptive responsiveness. J Neurophysiol 2007, 98:3121-3133.
25. Hilaire G., Voituron N., Menuet C., Ichiyama R.M., Subramanian H.H., Dutschmann M. The role of serotonin in respiratory function and dysfunction. Respir Physiol Neurobiol. 2010, 174:76-88.
26. 2 chemoreception, and thermoregulation. J Appl Physiol 2010, 108:1425-1432.
27. Hodges M.R., Richerson G.B. Medullary serotonin neurons and their roles in central respiratory chemoreception. Respir Physiol Neurobiol 2010, 173:256-263.
28. 2 sensitivity after neurotoxic lesions in the medullary raphé area of awake goats. J Appl Physiol 2004, 97:2236-2247.
29. Hodges M.R., Wang W., Richerson G.B. Acidosis-inhibited raphé neurons are GABAergic. FASEB J 2005, 19(369):21.
30. 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, 28:2495-2505.
31. Iceman K.E., Richerson G.B., Harris M.B. GABAergic neurons in the medullary raphé possess network independent chemosensitivity in situ. FASEB J 2012, 26(894):13.
32. Iceman KE, Richerson GB, Harris MB (2013) Medullary serotonin neurons are CO2-sensitive in situ. J Neurophysiol. Published ahead of print September 18, 2013. doi:10.1152/jn.00288.2013.
33. Inyushkin A.N., Merkulova N.A., Orlova A.O., Inyushkina E.M. Local GABAergic modulation of the activity of serotoninergic neurons in the nucleus raphe magnus. Neurosci Behav Physiol 2010, 40:885-893.
34. Jensen P., Farago A.F., Awatramani R.B., Scott M.M., Deneris E.S., Dymecki S.M. Redefining the serotonergic system by genetic lineage. Nat Neurosci 2008, 11:417-419.
35. Kinney H.C. Brainstem mechanisms underlying the sudden infant death syndrome: evidence from human pathologic studies. Dev Psychobiol 2009, 51:223-233.
36. Kinney H.C., Thach B.T. The sudden infant death syndrome. N Engl J Med 2009, 361:795-805.
37. Kirby L.G., Pernar L., Valentino R.J., Beck S.G. Distinguishing characteristics of serotonin and non-serotonin-containing cells in the dorsal raphé nucleus: electrophysiological and immunohistochemical studies. Neuroscience 2003, 116:669-683.
38. Kiyasova V., Gaspar P. Development of raphé serotonin neurons from specification to guidance. Eur J Neurosci 2011, 34:1553-1562.
39. Léger L., Gay N., Cespuglio R. Neurokinin NK1- and NK3-immunoreactive neurons in serotonergic cell groups in the rat brain. Neurosci Lett 2002, 323:146-150.
40. Liu R., Ding Y., Aghajanian G.K. Neurokinins activate local glutamatergic inputs to serotonergic neurons of the dorsal raphé nucleus. Neuropsychopharmacology 2002, 27:329-340.
41. Ljungdahl A., Hökfelt T., Nilsson G. Distribution of substance P-like immunoreactivity in the central nervous system of the rat - I. Cell bodies and nerve terminals. Neuroscience 1978, 3:861943.
42. Mason P. Physiological identification of pontomedullary serotonergic neurons in the rat. J Neurophysiol 1997, 77:1087-1098.
43. Mason P. From descending pain modulation to obesity via the medullary raphé. Pain 2011, 152:S20-S24.
44. Millhorn D.E., Hökfelt T., Seroogy K., Verhofstad A.A. Extent of colocalization of serotonin and GABA in neurons of the ventral medulla oblongata in rat. Brain Res 1988, 461:169-174.
45. 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, 7:1360-1369.
46. Nattie E., Li A. Neurokinin-1 receptor-expressing neurons in the ventral medulla are essential for normal central and peripheral chemoreception in the conscious rat. J Appl Physiol 2006, 101:1596-1606.
47. Nattie E.E., Li A., Richerson G.B., 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 (Lond) 2004, 556:235-253.
48. Paterson D.S., Trachtenberg F.L., Thompson E.G., Belliveau R.A., Beggs A.H., Darnall R., Chadwick A.E., Krous H.F., Kinney H.C. Multiple serotonergic brainstem abnormalities in sudden infant death syndrome. JAMA 2006, 296:2124-2132.
49. 2-induced c-Fos expression in brainstem preprotachykinin mRNA containing neurons. Respir Physiol Neurobiol 2002, 130:265-274.
50. 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 1996, 65:113-136.
51. Ptak K., Yamanishi T., Aungst J., Milescu L.S., Zhang R., Richerson G.B., Smith J.C. Raphé neurons stimulate respiratory circuit activity by multiple mechanisms via endogenously released serotonin and substance P. J Neurosci 2009, 29:3720-3737.
52. 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, 333:637642.
53. Rice C.D., Lois J.H., Kerman I.A., Yates B.J. Localization of serotoninergic neurons that participate in regulating diaphragm activity in the cat. Brain Res 2009, 1279:71-81.
54. Richardson-Jones J.W., Craige C.P., Nguyen T.H., Kung H.F., Gardier A.M., Dranovsky A., David D.J., Guiard B.P., Beck S.G., Hen R., Leonardo E.D. Serotonin-1A autoreceptors are necessary and sufficient for the normal formation of circuits underlying innate anxiety. J Neurosci 2011, 31:6008-6018.
55. 2 of neurons in the rostral ventral medulla in vitro. J Neurophysiol 1995, 73:933-944.
56. Richerson G.B. Serotonergic neurons as carbon dioxide sensors that maintain pH homeostasis. Nat Rev Neurosci 2004, 5:449-461.
57. Severson C.A., Wang W., Pieribone V.A., Dohle C.I., Richerson G.B. Midbrain serotonergic neurons are central pH chemoreceptors. Nat Neurosci 2003, 6:1139-1140.
58. Skagerberg G., Björklund A. Topographic principles in the spinal projections of serotonergic and non-serotonergic brainstem neurons in the rat. Neuroscience 1985, 15:445-480.
59. Soiza-Reilly M., Commons K.G. Glutamatergic drive of the dorsal raphé nucleus. J Chem Neuroanat 2011, 41:247-255.
60. Sternbach H. The serotonin syndrome. Am J Psychiatry 1991, 148:705-713.
61. Stornetta R.L., Rosin D.L., Wang H., Sevigny C.P., Weston M.C., Guyenet P.G. A group of glutamatergic interneurons expressing high levels of both neurokinin-1 receptors and somatostatin identifies the region of the pre-Bötzinger complex. J Comp Neurol 2003, 455:499-512.
62. B receptors in midbrain raphé nuclei and forebrain of rats. Br J Pharmacol 1996, 119:1375-1384.
63. Templin J.S., Bang S.J., Soiza-Reilly M., Berde C.B., Commons K.G. Patterned expression of ion channel genes in mouse dorsal raphé nucleus determined with the Allen Mouse Brain Atlas. Brain Res 2012, 1457:1-12.
64. Toppin V.A.L., Harris M.B., Kober A.M., Leiter J.C., St John W.M. 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 2007, 103:220-227.
65. Valentino R.J., Commons K.G. Peptides that fine-tune the serotonin system. Neuropeptides 2005, 39:1-8.
66. Valentino R.J., Bey V., Pernar L., Commons K.G. Substance P Acts through local circuits within the rat dorsal raphé nucleus to alter serotonergic neuronal activity. J Neurosci 2003, 23:7155-7159.
67. Veasey S.C., Fornal C.A., Metzler C.W., Jacobs B.L. Response of serotonergic caudal raphé neurons in relation to specific motor activities in freely moving cats. J Neurosci 1995, 15:5346-5359.
68. Veasey S.C., Fornal C.A., Metzler C.W., Jacobs B.L. Single-unit responses of serotonergic dorsal raphé neurons to specific motor challenges in freely moving cats. Neuroscience 1997, 79:161-169.
69. Wang W., Richerson G.B. Development of chemosensitivity of rat medullary raphé neurons. Neuroscience 1999, 90:1001-1011.
70. Wang W., Pizzonia J.H., Richerson G.B. Chemosensitivity of rat medullary raphé neurones in primary tissue culture. J Physiol (Lond) 1998, 511(Pt 2):433-450.
71. Wang W., Tiwari J.K., Bradley S.R., Zaykin R.V., Richerson G.B. Acidosis-stimulated neurons of the medullary raphé are serotonergic. J Neurophysiol 2001, 85:2224-2235.
72. PO2 and pH of the working heart-brain stem preparation during vascular perfusion with aqueous medium. Am J Physiol Regul Integr Comp Physiol 2001, 281:R528-R538.
73. Winkler C.W., Hermes S.M., Chavkin C.I., Drake C.T., Morrison S.F., Aicher S.A. Kappa opioid receptor (KOR) and GAD67 immunoreactivity are found in OFF and NEUTRAL cells in the rostral ventromedial medulla. J Neurophysiol 2006, 96:3465-3473.
74. A receptors in the raphé pallidus: effects on body temperature, heart rate, and blood pressure in conscious rats. Am J Physiol Regul Integr Comp Physiol 2003, 285:R110-R116.
75. Zaretsky D.V., Zaretskaia M.V., Samuels B.C., Cluxton L.K., DiMicco J.A. Microinjection of muscimol into raphé pallidus suppresses tachycardia associated with air stress in conscious rats. J Physiol (Lond) 2003, 546:243-250.