Raphe neurons stimulate respiratory circuit activity by multiple mechanisms via endogenously released serotonin and substance p

Journal of Neuroscience

Volumn 29, Issue 12, 2009, Pages 3720-3737

  Ptak, Krzysztof ^a   Yamanishi, Tadashi ^a   Aungst, Jason ^a   Milescu, Lorin S ^a   Zhang, Ruli ^a   Richerson, George B ^b,c   Smith, Jeffrey C ^a  

^a National Institute of Neurological Disorders   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROKININ 1 RECEPTOR; SEROTONIN; SUBSTANCE P; CATION; ION CHANNEL;

ANIMAL TISSUE; ARTICLE; BIOPHYSICS; BRAIN FUNCTION; BRAIN STEM; CELL MEMBRANE DEPOLARIZATION; CONDUCTANCE; ELECTROPHYSIOLOGY; ENZYME RELEASE; EXCITATION; HYPOGLOSSAL NERVE; IN VITRO STUDY; INSPIRATORY CAPACITY; MEDULLA OBLONGATA; MOTONEURON; NERVE CELL; NERVOUS SYSTEM; NEWBORN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAPHE NEURON; RAPHE NUCLEUS; RAT; RESPIRATORY SYSTEM; RHYTHM; SPINAL CORD; ACTION POTENTIAL; ANIMAL; CYTOLOGY; METABOLISM; NERVE CELL NETWORK; PATCH CLAMP; PERIODICITY; PHYSIOLOGY; RESPIRATION CENTER; SPRAGUE DAWLEY RAT;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; BRAIN STEM; CATIONS; HYPOGLOSSAL NERVE; ION CHANNELS; MEDULLA OBLONGATA; MOTOR NEURONS; NERVE NET; NEURONS; PATCH-CLAMP TECHNIQUES; PERIODICITY; RAPHE NUCLEI; RATS; RATS, SPRAGUE-DAWLEY; RESPIRATORY CENTER; SEROTONIN; SPINAL CORD; SUBSTANCE P;

EID: 64849101288     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5271-08.2009     Document Type: Article

References (60)

1. Al-Zubaidy ZA, Erickson RL, Greer JJ (1996) Serotonergic and noradrenergic effects on respiratory neural discharge in the medullary slice preparation of neonatal rats. Pflugers Arch 431:942-949.
2. Bayliss DA, Umemiya M, Berger AJ (1995) Inhibition of Nand P-type calcium currents and the after-hyperpolarization in rat motoneurones by serotonin. J Physiol 485:635-647.
3. Bayliss DA, Li YW, Talley EM (1997) Effects of serotonin on caudal raphe neurons: inhibition of Nand P/Q-type calcium channels and the afterhyperpolarization. J Neurophysiol 77:1362-1374.
4. h in central neurons. Neuron 2:1535-1540.
5. But era RJ Jr, Rinzel J, Smith JC (1999a) Models of respiratory rhythm generation in the pre-B6tzinger complex. I. Bursting pacemaker neurons. J Neurophysiol 82:382-397.
6. Butera RJ Jr, Rinzel J, Smith JC (1999b) Models of respiratory rhythm generation in the pre-B6tzinger complex. II. Populations of coupled pacemaker neuron. J Neurophysiol 82:398-415.
7. Carr DB, Cooper DC, Ulrich SL, Spruston N, Surmeier DJ (2002) Serotonin receptor activation inhibits sodium current and dendritic excitability in prefrontal cortex via a protein kinase C-dependent mechanism. J Neurosci 22:6846-6855.
8. Dean C, Marson L, Kampine JP (1993) Distribution and co-localization of 5-hydroxytryptamine, thyrotropin-releasing hormone and substance P in the cat medulla. Neuroscience 57:811-822.
9. Dekin MS, Richerson GB, Getting PA (1985) Thyrotropin-releasing hormone induces rhythmic bursting in neurons of the nucleus tractus solitarius. Science 229:67-69.
10. Del Negro CA, Johnson SM, Butera RJ, Smith JC (2001) Models of respiratory rhythm generation in the pre-Bötzinger complex. III. Experimental tests of model predictions. J Neurophysiol 86:59-74.
11. Del Negro CA, Koshiya N, Butera RJ Jr, Smith JC (2002) Persistent sodium current, membrane properties and bursting behavior of pre-Bötzinger complex inspiratory neurons in vitro. J Neurophysiol 88:2242-2250.
12. Del Negro CA, Morgado-Valle C, Hayes JA, Mackay DD, Pace RW, Crowder EA, Feldman JL (2005) Sodium and calcium current-mediated pacemaker neurons and respiratory rhythm generation. J Neurosci 25:446-453.
13. Feldman JL, Mitchell GS, Nattie EE (2003) Breathing: rhythmicity, plasticity, chemosensitivity. Annu Rev Neurosci 26:239-266.
14. Funk GD, Smith JC, Feldman JL (1993) Generation and transmission of respiratory oscillations in medullary slices: role of excitatory amino acids. J Neurophysiol 70:1497-1515.
15. Gasparini S, DiFrancesco D (1999) Action of serotonin on the hyperpolarization-activated cation current (Ih) in rat CA1 hippocampal neurons. Eur J Neurosci 11:3093-3100.
16. Gray PA, Janczewski WA, Mellen N, McCrimmon DR, Feldman JL (2001) Normal breathing requires preBotzinger complex neurokinin-1 receptorexpressing neurons. Nat Neurosci 4:927-930.
17. Guyenet PG, Mulkey DK, Stornetta RL, Bayliss DA (2005) Regulation of ventral surface chemoreceptors by the central respiratory pattern generator. J Neurosci 25:8938-8947.
18. Hayes JA, Del Negro CA (2007) Neurokinin receptor-expressing pre-Botzinger complex neurons in neonatal mice studied in vitro. J Neurophysiol 97:4215-4224.
19. Hodges MR, Tattersall GJ, Harris MB, McEvoy SD, Richerson DN, Deneris ES, Johnson RL, Chen ZF, Richerson GB (2008) Defects in breathing and thermoregulation in mice with near-complete absence of central serotonin neurons. J Neurosci 28:2495-2505.
20. Hwang LL, Dun NJ (1999) 5-HT modulates multiple conductances in immature rat rostral ventrolateral medulla neurons in vitro. J Physiol 517:217-228.
21. Iverfeldt K, Serfozo P, Diaz Arnesto L, Bartfai T (1989) Differential release of coexisting neurotransmitters: frequency dependence of the efflux of substance P, thyrotropin releasing hormone and [3H] serotonin from tissue slices of rat ventral spinal cord. Acta Physiol Scand 137:63-71.
22. Jacobs BL, Azmitia EC (1992) Structure and function of the brain serotonin system. Physiol Rev 72:165-229.
23. +-dominated leak currents contribute to inspiratory rhythm generation in the pre-B6tC in vitro. J Neurosci 27:1773-1785.
24. Koizumi H, Wilson CG, Wong S, Yamanishi T, Koshiya N, Smith JC (2008) Functional imaging, spatial reconstruction and biophysical analysis of a respiratory motor circuit isolated in vitro. J Neurosci 28:2353-2365.
25. Koshiya N, Smith JC (1999) Neuronal pacemaker for breathing visualized in vitro. Nature 400:360-363.
26. Kubin L, Davies RO, Pack AI (1998) Control of upper airway motoneurons during REM sleep. News Physiol Sci 13:91-97.
27. Lalley PM (1986) Serotonergic and non-serotonergic responses of phrenic motoneurons to raphe stimulation in the cat. J Physiol 380:373-385.
28. Lalley PM, Bischoff AM, Richter DW (1994) Serotonin lA-receptor activation suppresses respiratory apneusis in the cat. Neurosci Lett 172:59-62.
29. Lindsey BG, Hernandez YM, Morris KF, Shannon R (1992) Functional connectivity between brain stem midline neurons with respiratorymodulated firing rates. J Neurophysiol 67:890-904.
30. Ling L, Fuller DD, Bach KB, Kinkead R, Olson EB Jr, Mitchell GS (2001) Chronic intermittent hypoxia elicits serotonin-dependent plasticity in the central neural control of breathing. J Neurosci 21:5381-5388.
31. LuB, SuY, DasS, LiuJ, XiaJ, Ren D (2007) The neuronal channel NALCN contributes resting sodium permeability and is required for normal respiratory rhythm. Cell 129:371-383.
32. 4(a) receptors avert opioid-induced breathing depression without loss of analgesia. Science 301:226-229.
33. Mason P (1997) Physiological identification of pontomedullary serotonergic neurons in the rat. J Neurophysiol 77:1087-1098.
34. McGuire M, Zhang Y, White DP, Ling L (2004) Serotonin receptor subtypes required for ventilatory long-term facilitation ad its enhancement after chronic intermittent hypoxia in awake rats. Am J Physiol Regul Integr Comp Physiol 286:R334-R341.
35. Menetrey D, Basbaum AI (1987) The distribution of substance P-, enkephalinand dynorphin-immunoreactive neurons in the medulla of the rat and their contribution to bulbospinal pathways. Neuroscience 23:173-187.
36. Morgado-Valle C, Feldman JL (2004) Depletion of substance P and glutamate by capsaicin blocks respiratory rhythm in neonatal rat in vitro. J Physiol 555:783-792.
37. Olson EB Jr, Dempsey JA, McCrimmon DR (1979) Serotonin and the control of ventilation in awake rats. J Clin Invest 64:689-693.
38. Pace RW, Mackay DD, Feldman JL, Del Negro CA (2007) Role of persistent sodium current in mouse preBotzinger complex neurons and respiratory rhythm generation. J Physiol 580:485-496.
39. Paterson DS, Trachtenberg FL, Thompson EG, Belliveau RA, Beggs AH, Darnall R, Chadwick AE, Krous HF, Kinney HC (2006) Multiple serotonergic brainstem abnormalities in sudden infant death syndrome. JAMA 296:2124-2132.
40. Paton JFR (1996) A working heart-brainstem preparation of the mouse. J Neurosci Methods 65:63-68.
41. Peever JH, Necakov A, Duffin J (2001) Nucleus raphe obscurus modulates hypoglossal output of neonatal rat in vitro transverse brain stem slices. J Appl Physiol 90:269-279.
42. Pefia F, Ramirez JM (2002) Endogenous activation of serotonin-2A receptors is required for respiratory rhythm generation in vitro. J Neurosci 22:11055-11064.
43. Pefia F, Ramirez JM (2004) Substance P-mediated modulation of pacemaker properties in the mammalian respiratory network. J Neurosci 24:7549-7556.
44. Pefia F, Parkis MA, Tryba AK, Ramirez JM (2004) Differential contribution of pacemaker properties to the generation of respiratory rhythms during normoxia and hypoxia. Neuron 43:105-117.
45. Pickering AE, Paton JFR (2006) A decerebrate, artificially-perfused in situ preparation of rat: utility for the study of autonomic and nociceptive processing. J Neurosci Methods 155:260-271.
46. Purvis LK, Smith JC, Koizumi H, Butera RJ (2007) Intrinsic bursters increase the robustness of rhythm generation in an excitatory network. J Neurophysiol 97:1515-1526.
47. Richerson GB (2004) Serotonergic neurons as carbon dioxide sensors that maintain pH homeostasis. Nat Rev Neurosci 5:449-461.
48. Richter DW, Manzke T, Wilken B, Ponimaskin E (2003) Serotonin receptors: guardians of stable breathing. Trends Mol Med 9:542-548.
49. Rybak IA, Shevtsova NA, St.-John WM, Paton JFR, Pierrefiche O (2003) Endogenous rhythm generation in the pre-Botzinger complex and ionic currents: modelling and in vitro studies. Eur J Neurosci 18:239-257.
50. Schwarzacher SW, Pestean A, Günther S, Ballanyi K (2002) Serotonergic modulation of respiratory motoneurons and interneurons in brainstem slices of perinatal rats. Neuroscience 115:1247-1259.
51. Smith JC, Ellenberger HH, Ballanyi K, Richter DW, Feldman JL (1991) Pre-Bötzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science 254:726-729.
52. Smith JC. Abdala APL, Koizumi H, Rybak IA, Paton JFR (2007) Spatial and functional architecture of the mammalian brainstem respiratory network: a hierarchy of three oscillatory mechanisms. J Neurophysiol 98:3370-3387.
53. St.-John WM, Leiter JC (2008) Maintenane of gasping and restoration of eupnea after hypoxia is impaired following blockers of alpha 1adrenergic receptors and serotonin 5-HT2 receptors. J Appl Physiol 104:665-673.
54. Stornetta RL, Rosin DL, Wang H, Sevigny CP, Weston MC, Guyenet PG (2003) 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 455:499-512.
55. Talley EM, Lei Q, Sirois JE, Bayliss DA (2000) TASK-1, a two-pore domain K+ channel, is modulated by multiple neurotransmitters in motoneurons. Neuron 25:399-410.
56. Talley EM, Solorzano G, Lei Q, Kim D, Bayliss DA (2001) CNS distribution of members of the two-pore-domain (KCNK) potassium channel family. J Neurosci 21:7491-7505.
57. Toppin VAL, Harris MB, Kober AM, Leiter JC, St.-John WM (2007) 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.
58. Vandermaelen CP, Aghajanian GK (1983) Electrophysiological and pharmacological characterization of serotonergic dorsal raphe neurons recorded extracellularly and intracellularly in rat brain slices. Brain Res 289:109-119.
59. Wang W, Tiwari JK, Bradley SR, Zaykin RV, Richerson GB (2001) Acidosisstimulated neurons of the medullary raphe are serotonergic. J Neurophysiol 85:2224-2235.
60. Xiang Z, Wang L, Kitai ST (2005) Modulation of spontaneous firing in rat subthalamic neurons by 5-HT receptor subtypes. J Neurophysiol 93:1145-1157.