Neurokinin-1 receptor activation in Bötzinger complex evokes bradypnoea

Journal of Physiology

Volumn 575, Issue 3, 2006, Pages 869-885

  Fong, Angelina Y ^a   Potts, Jeffrey T ^a,b  

^a UNIVERSITY OF MISSOURI   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 (2 METHOXYBENZYLAMINO) 2 PHENYLPIPERIDINE; MUSCIMOL; NEUROKININ 1 RECEPTOR; SUBSTANCE P; TACHYKININ RECEPTOR AGONIST; 4 AMINOBUTYRIC ACID A RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRADYPNEA; BREATHING MECHANICS; BREATHING RATE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ELECTROSTIMULATION; EXPIRATORY FLOW RATE; HERING BREUER REFLEX; INSPIRATORY CAPACITY; MALE; MICROINJECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; STATISTICAL SIGNIFICANCE; TACHYPNEA; VAGUS NERVE STIMULATION; BOTZINGER COMPLEX; JUVENILE ANIMAL; PHRENIC NERVE; PREBOTZINGER COMPLEX; RESPIRATION CENTER; VENTRAL RESPIRATORY GROUP;

ANIMALS; DIAPHRAGM; ELECTRIC STIMULATION; MALE; MICROINJECTIONS; PHRENIC NERVE; PIPERIDINES; RATS; RATS, WISTAR; RECEPTORS, NEUROKININ-1; REFLEX; RESPIRATORY CENTER; RESPIRATORY FUNCTION TESTS; RESPIRATORY MECHANICS; SUBSTANCE P; VAGUS NERVE;

EID: 33748328205     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2006.114314     Document Type: Article

References (78)

1. Alheid GF, Gray PA, Jiang MC, Feldman JL & McCrimmon DR (2002). Parvalbumin in respiratory neurons of the ventrolateral medulla of the adult rat. J Neurocytol 31, 693-717.
2. Block CH & Hoffman GE (1987). Neuropeptide and monoamine components of the parabrachial pontine complex. Peptides 8, 267-283.
3. Bonham AC & McCrimmon DR (1990). Neurones in a discrete region of the nucleus tractus solitarius are required for the Breuer-Hering reflex in rat. J Physiol 427, 261-280.
4. Brunner MJ, Sussman MS, Greene AS, Kallman CH & Shoukas AA (1982). Carotid sinus baroreceptor reflex control of respiration. Circ Res 51, 624-636.
5. Chen ZB, Engberg G, Hedner T & Hedner J (1991). Antagonistic effects of somatostatin and substance P on respiratory regulation in the rat ventrolateral medulla oblongata. Brain Res 556, 13-21.
6. Chen ZB, Hedner J & Hedner T (1990). Local effects of substance P on respiratory regulation in the rat medulla oblongata. J Appl Physiol 68, 693-699.
7. Chitravanshi VC & Sapru HN (1999). Phrenic nerve responses to chemical stimulation of the subregions of ventral medullary respiratory neuronal group in the rat. Brain Res 821, 443-460.
8. Cohen MI & Shaw CF (2004). Role in the inspiratory off-switch of vagal inputs to rostral pontine inspiratory-modulated neurons. Respir Physiol Neurobiol 143, 127-140.
9. Connelly CA, Dobbins EG & Feldman JL (1992). Pre-Botzinger complex in cats: Respiratory neuronal discharge patterns. Brain Res 590, 337-340.
10. Ptak K, Di Pasquale E & Monteau R (1999). Substance P and central respiratory activity: A comparative in vitro study on foetal and newborn rat. Dev Brain Res 114, 217-227.
11. Dobbins EG & Feldman JL (1994). Brainstem network controlling descending drive to phrenic motoneurons in rat. J Comp Neurol 347, 64-86.
12. Douglas FL, Palkovits M & Brownstein MJ (1982). Regional distribution of substance P-like immunoreactivity in the lower brainstem of the rat. Brain Res 245, 376-378.
13. Ellenberger HH & Feldman JL (1988). Monosynaptic transmission of respiratory drive to phrenic motoneurons from brainstem bulbospinal neurons in rats. J Comp Neurol 269, 47-57.
14. Ellenberger HH & Feldman JL (1990). Subnuclear organization of the lateral tegmental field of the rat. I: Nucleus ambiguus and ventral respiratory group. J Comp Neurol 294, 202-211.
15. Ezure K (1990). Synaptic connections between medullary respiratory neurons and considerations on the genesis of respiratory rhythm. Prog Neurobiol 35, 429-450.
16. Ezure K (2004). Respiration-related afferents to parabrachial pontine regions. Respir Physiol Neurobiol 143, 167-175.
17. Ezure K & Manabe M (1988). Decrementing expiratory neurons of the Botzinger complex. II. Direct inhibitory synaptic linkage with ventral respiratory group neurons. Exp Brain Res 72, 159-166.
18. Ezure K & Tanaka I (1996). Pump neurons of the nucleus of the solitary tract project widely to the medulla. Neurosci Lett 215, 123-126.
19. Ezure K, Tanaka I & Miyazaki M (1998). Pontine projections of pulmonary slowly adapting receptor relay neurons in the cat. Neuroreport 9, 411-414.
20. Ezure K, Tanaka I & Saito Y (2003). Brainstem and spinal projections of augmenting expiratory neurons in the rat. Neurosci Res 45, 41-51.
21. Ezure K, Tanaka I, Saito Y & Otake K (2002). Axonal projections of pulmonary slowly adapting receptor relay neurons in the rat. J Comp Neurol 446, 81-94.
22. Feldman JL & McCrimmon DR (2003). Neural Control of Breathing. 2nd edn, pp. 967-990. Fundamental Neuroscience Eds: Squire, Bloom, McConnell, Roberts, Spitzer & Zigmond, Academic Press, Boston.
23. Feldman JL, Smith JC, Ellenberger HH, Connelly CA, Liu GS, Greer JJ, Lindsay AD & Otto MR (1990). Neurogenesis of respiratory rhythm and pattern: Emerging concepts. Am J Physiol 259, R879-R886.
24. Fong AY & Potts JT (2005). Microinjection of substance P (SP) into the ventral respiratory group (VRG) complex excites expiratory activity. FASEB J 19, 372.8 (Abstract).
25. Gray PA, Janczewski WA, Mellen N, McCrimmon DR & Feldman JL (2001). Normal breathing requires preBotzinger complex neurokinin-1 receptor-expressing neurons. Nat Neurosci 4, 927-930.
26. Gray PA, Rekling JC, Bocchiaro CM & Feldman JL (1999). Modulation of respiratory frequency by peptidergic input to rhythmogenic neurons in the preBotzinger complex. Science 286, 1566-1568.
27. Guyenet PG, Sevigny CP, Weston MC & Stornetta RL (2002). Neurokinin-1 receptor-expressing cells of the ventral respiratory group are functionally heterogeneous and predominantly glutamatergic. J Neurosci 22, 3806-3816.
28. Hayashi F, Coles SK & McCrimmon DR (1996). Respiratory neurons mediating the Breuer-Hering reflex prolongation of expiration in rat. J Neurosci 16, 6526-6536.
29. Hedner J, Hedner T, Wessberg P & Jonason J (1984). Interaction of substance P with the respiratory control system in the rat. J Pharmacol Exp Ther 228, 196-201.
30. Holtman JR & Speck DF (1994). Substance P immunoreactive projections to the ventral respiratory group in the rat. Peptides 15, 803-808.
31. Janczewski WA & Feldman JL (2006). Distinct rhythm generators for inspiration and expiration in the juvenile rat. J Physiol 570, 407-420.
32. Jiang M, Alheid GF, Calandriello T & McCrimmon DR (2004). Parabrachial-lateral pontine neurons link nociception and breathing. Respir Physiol Neurobiol 143, 215-233.
33. Johnson SM, Smith JC & Feldman JL (1996). Modulation of respiratory rhythm in vitro: Role of Gi/o protein-mediated mechanisms. J Appl Physiol 80, 2120-2133.
34. Kubin L, Alheid GF, Zuperku EJ & McCrimmon DR (2006). (2006). Central pathways of pulmonary and lower airway vagal afferents. J Appl Physiol (in press).
35. Lee LY & Pisarri TE (2001). Afferent properties and reflex functions of bronchopulmonary C-fibers. Respir Physiol 125, 47-65.
36. Leger L, Charnay Y, Chayvialle JA, Berod A, Dray F, Pujol JF, Jouvet M & Dubois PM (1983). Localization of substance P- and enkephalin-like immunoreactivity in relation to catecholamine-containing cell bodies in the cat dorsolateral pontine tegmentum: An immunofluorescence study. Neuroscience 8, 525-546.
37. Li Q, Goodchild AK, Seyedabadi M & Pilowsky PM (2005). Pre-protachykinin A mRNA is colocalized with tyrosine hydroxylase-immunoreactivity in bulbospinal neurons. Neuroscience 136, 205-216.
38. Li Y, Song G, Cao Y, Wang H, Wang G, Yu S & Zhang H (2006). Modulation of the Hering-Breuer reflex by raphe pallidus in rabbits. Neurosci Lett 397, 259-262.
39. Liu YY, Wong-Riley MTT, Liu JP, Wei XY, Jia Y, Liu HL, Fujiyama F & Ju G (2004). Substance P and enkephalinergic synapses onto neurokinin-1 receptor-immunoreactive neurons in the pre-Botzinger complex of rats. Eur J Neurosci 19, 65-75.
40. Lumsden T (1923). Observations on the respiratory centres in the cat. J Physiol 57, 153-160.
41. Makeham JM, Goodchild AK & Pilowsky PM (2005). NK1 receptor activation in rat rostral ventrolateral medulla selectively attenuates somato-sympathetic reflex while antagonism attenuates sympathetic chemoreflex. Am J Physiol 288, R1707-R1715.
42. Maley BE (1996). Immunohistochemical localization of neuropeptides and neurotransmitters in the nucleus solitarius. Chem Senses 21, 367-376.
43. Manabe M & Ezure K (1988). Decrementing expiratory neurons of the Botzinger complex. I. Response to lung inflation and axonal projection. Exp Brain Res 72, 150-158.
44. McCrimmon DR, Feldman JL & Speck DF (1986). Respiratory motoneuronal activity is altered by injections of picomoles of glutamate into cat brain stem. J Neurosci 6, 2384-2392.
45. McCrimmon DR, Monnier A, Hayashi F & Zuperku EJ (2000). Pattern formation and rhythm generation in the ventral respiratory group. Clin Exp Pharmacol Physiol 27, 126-131.
46. McKay LC, Janczewski WA & Feldman JL (2005). Sleep-disordered breathing after targeted ablation of preBotzinger complex neurons. Nat Neurosci 8, 1142-1144.
47. Monnier A, Alheid GF & McCrimmon DR (2003). Defining ventral medullary respiratory compartments with a glutamate receptor agonist in the rat. J Physiol 548, 859-874.
48. Monteau R, Ptak K, Broquere N & Hilaire G (1996). Tachykinins and central respiratory activity: An in vitro study on the newborn rat. Eur J Pharmacol 314, 41-50.
49. 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.
50. Nakaya Y, Kaneko T, Shigemoto R, Nakanishi S & Mizuno N (1994). Immunohistochemical localization of substance P receptor in the central nervous system of the adult rat. J Comp Neurol 347, 249-274.
51. Nattie EE & Li A (2002). Substance P-saporin lesion of neurons with NK1 receptors in one chemoreceptor site in rats decreases ventilation and chemosensitivity. J Physiol 544, 603-616.
52. Onimaru H & Homma I (2003). A novel functional neuron group for respiratory rhythm generation in the ventral medulla. J Neurosci 23, 1478-1486.
53. Paton JF (1996). The ventral medullary respiratory network of the mature mouse studied in a working heart-brainstem preparation. J Physiol 493, 819-831.
54. Paton JF (1998). Pattern of cardiorespiratory afferent convergence to solitary tract neurons driven by pulmonary vagal C-fiber stimulation in the mouse. J Neurophysiol 79, 2365-2373.
55. Paton JF, Deuchars J, Ahmad Z, Wong LF, Murphy D & Kasparov S (2001). Adenoviral vector demonstrates that angiotensin II-induced depression of the cardiac baroreflex is mediated by endothelial nitric oxide synthase in the nucleus tractus solitarii of the rat. J Physiol 531, 445-458.
56. Pena F & Ramirez JM (2004). Substance P-mediated modulation of pacemaker properties in the mammalian respiratory network. J Neurosci 24, 7549-7556.
57. Potts JT, Paton JF, Mitchell JH, Garry MG, Kline G, Anguelov PT & Lee SM (2003). Contraction-sensitive skeletal muscle afferents inhibit arterial baroreceptor signalling in the nucleus of the solitary tract: role of intrinsic GABA interneurons. Neuroscience 119, 201-214.
58. Potts JT, Rybak IA & Paton JF (2005). Respiratory rhythm entrainment by somatic afferent stimulation. J Neurosci 25, 1965-1978.
59. Ptak K, Burnet H, Blanchi B, Sieweke M, De Felipe C, Hunt SP, Monteau R & Hilaire G (2002). The murine neurokinin NK1 receptor gene contributes to the adult hypoxic facilitation of ventilation. Eur J Neurosci 16, 2245-2252.
60. Ptak K, Hunt SP & Monteau R (2000). Substance P and central respiratory activity: A comparative in vitro study in NK1 receptor knockout and wild-type mice. Pflugers Arch 440, 446-451.
61. Remmers JE, Richter DW, Ballantyne D, Bainton CR & Klein JP (1986). Reflex prolongation of stage I of expiration. Pflugers Arch 407, 190-198.
62. Richter DW (1982). Generation and maintenance of the respiratory rhythm. J Exp Biol 100, 93-107.
63. Richter DW, Ballantyne D & Remmers JE (1986). How is the respiratory rhythm generated?A Model. News Physiol Sci 1, 109-112.
64. Richter DW & Spyer KM (2001). Studying rhythmogenesis of breathing: comparison of in vivo and in vitro models. Trends Neurosci 24, 464-472.
65. Rybak IA, Shevtsova NA, Paton JF, Dick TE, St-John WM, Morschel M & Dutschmann M (2004). Modeling the ponto-medullary respiratory network. Resp Physiol Neurobiol 143, 307-319.
66. Schwarzacher SW, Smith JC & Richter DW (1995). Pre-Botzinger complex in the cat. J Neurophysiol 73, 1452-1461.
67. Schwarzacher SW, Wilhelm Z, Anders K & Richter DW (1991). The medullary respiratory network in the rat. J Physiol 435, 631-644.
68. Shvarev YN, Lagercrantz H & Yamamoto Y (2002). Biphasic effects of substance P on respiratory activity and respiration-related neurones in ventrolateral medulla in the neonatal rat brainstem in vitro. Acta Physiol Scand 174, 67-84.
69. Siniaia MS, Young DL & Poon CS (2000). Habituation and desensitization of the Hering-Breuer reflex in rat. J Physiol 523, 479-491.
70. Smith JC, Butera RJ, Del Koshiya NNC, Wilson CG & Johnson SM (2000). Respiratory rhythm generation in neonatal and adult mammals: The hybrid pacemaker-network model. Resp Physiol 122, 131-147.
71. Smith JC, Ellenberger HH, Ballanyi K, Richter DW & Feldman JL (1991). Pre-Botzinger complex: A brainstem region that may generate respiratory rhythm in mammals. Science 254, 726-729.
72. Smotherman M, Kobayasi K, Ma J, Zhang S & Metzner W (2006). A mechanism for vocal-respiratory coupling in the mammalian parabrachial nucleus. J Neurosci 26, 4860-4869.
73. Sun QJ, Goodchild AK, Chalmers JP & Pilowsky PM (1998). The pre-Botzinger complex and phase-spanning neurons in the adult rat. Brain Res 809, 204-213.
74. Wang H, Germanson TP & Guyenet PG (2002). Depressor and tachypneic responses to chemical stimulation of the ventral respiratory group are reduced by ablation of neurokinin-1 receptor-expressing neurons. J Neurosci 22, 3755-3764.
75. Wang GM, Song G & Zhang H (2005). Phenomenon of non-associative learning in Hering-Breuer reflex simulated by electrical vagal stimulation in rabbits. Sheng Li Xue Bao 57, 511-516.
76. Wang H, Stornetta RL, Rosin DL & Guyenet PG (2001). Neurokinin-1 receptor-immunoreactive neurons of the ventral respiratory group in the rat. J Comp Neurol 434, 128-146.
77. Wenninger JM, Pan LG, Klum L, Leekley T, Bastastic J, Hodges MR, Feroah T, Davis S & Forster HV (2004). Small reduction of neurokinin-1 receptor-expressing neurons in the pre-Botzinger complex area induces abnormal breathing periods in awake goats. J Appl Physiol 97, 1620-1628.
78. Wickstrom HR, Berner J, Holgert H, Hokfelt T & Lagercrantz H (2004). Hypoxic response in newborn rat is attenuated by neurokinin-1 receptor blockade. Resp Physiol Neurobiol 140, 19-31.