Substance P-mediated modulation of pacemaker properties in the mammalian respiratory network

Journal of Neuroscience

Volumn 24, Issue 34, 2004, Pages 7549-7556

  Peña, Fernando ^a,b   Ramirez, Jan Marino ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b DEPARTAMENTO DE FÍSICA   (Mexico)

Author keywords

Bursting properties; Neuromodulation; Pacemaker neurons; Respiratory network; Substance P; TTX resistant Na+ current

Indexed keywords

CADMIUM; ION CHANNEL; N METHYL DEXTRO ASPARTIC ACID; SODIUM ION; SUBSTANCE P; TETRODOTOXIN;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ARTICLE; BRAIN SLICE; BRAIN STEM; CONTROLLED STUDY; DEPOLARIZATION; EXCITATION; FEMALE; ION CURRENT; ION EXCHANGE; MALE; MAMMAL; MOUSE; NERVE CELL NETWORK; NEUROMODULATION; NONHUMAN; OSCILLATORY POTENTIAL; PACEMAKER; PRIORITY JOURNAL; REGULATORY MECHANISM; RESPIRATION CENTER; RETT SYNDROME;

ACTION POTENTIALS; ANIMALS; CADMIUM; FEMALE; MALE; MICE; NERVE NET; NEURONS; PATCH-CLAMP TECHNIQUES; POTASSIUM; RECEPTORS, N-METHYL-D-ASPARTATE; RESPIRATORY CENTER; SODIUM CHANNELS; SUBSTANCE P; TETRODOTOXIN;

EID: 4444226344     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1871-04.2004     Document Type: Article

References (70)

1. Adams PR, Brown DA, Jones SW (1983) Substance P inhibits the M-current in bullfrog sympathetic neurones. Br J Pharmacol 79:330-333.
2. Akasu T, Ishimatsu M, Yamada K (1996) Tachykinins cause inward current through NK1 receptors in bullfrog sensory neurons. Brain Res 713:160-167.
3. Alberi S, Dubois-Dauphin M, Dreifuss JJ, Raggenbass M (1993) Modulation by divalent cations of the current generated by vasopressin in facial motoneurons. Brain Res 624:326-330.
4. Aosaki T, Kawaguchi Y (1996) Actions of substance P on rat neostriatal neurons in vitro. J Neurosci 16:5141-5153.
5. Bell MI, Richardson PJ, Lee K (1998) Characterization of the mechanism of action of tachykinins in rat striatal cholinergic interneurons. Neuroscience 87:649-658.
6. Bertrand PP, Galligan JJ (1994) Contribution of chloride conductance increase to slow EPSC and tachykinin current in guinea-pig myenteric neurones. J Physiol (Lond) 481:47-60.
7. Blanchi B, Kelly LM, Viemari JC, Lafon I, Burnet H, Bevengut M, Tillmanns S, Daniel L, Graf T, Hilaire G, Sieweke MH (2003) MafB deficiency causes defective respiratory rhythmogenesis and fatal central apnea at birth. Nat Neurosci 6:1091-1100.
8. Bley KR, Tsien RW (1990) Inhibition of Ca2+ and K+ channels in sympathetic neurons by neuropeptides and other ganglionic transmitters. Neuron 4:379-391.
9. Chen RZ, Akbarian S, Tudor M, Jaenisch R (2001) Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice. Nat Genet 27:327-331.
10. Cirignotta F, Lugaresi E, Montagna P (1986) Breathing impairment in Rett syndrome. Am J Med Genet Suppl 1:167-173.
11. Deguchi K, Antalffy BA, Twohill LJ, Chakraborty S, Glaze DG, Armstrong DD (2000) Substance P immunoreactivity in Rett syndrome. Pediatr Neurol 22:259-266.
12. Dekin MS, Richerson GB, Getting PA (1985) Thyrotropin-releasing hormone induces rhythmic bursting in neurons of the nucleus tractus solitarius. Science 229:67-69.
13. Delmas P, Niel JP, Gola M (1996) Muscarinic activation of a novel voltage-sensitive inward current in rabbit prevertebral sympathetic neurons. Eur J Neurosci 8:598-610.
14. Delmas P, Raggenbass M, Gola M (1997) Low-threshold Na+ currents: a new family of receptor-operated inward currents in mammalian nerve cells. Brain Res Brain Res Rev 25:246-254.
15. Dickinson PS, Nagy F (1983) Control of a central pattern generator by an identified modulatory interneurone in crustacea. II. Induction and modification of plateau properties in pyloric neurones. J Exp Biol 105:59-82.
16. Dunn HG, MacLeod PM (2001) Rett syndrome: review of biological abnormalities. Can J Neurol Sci 28:16-29.
17. Gola M, Delmas P, Chagneux H (1998a) Encoding properties induced by a persistent voltage-gated muscarinic sodium current in rabbit sympathetic neurones. J Physiol (Lond) 510:387-399.
18. Gola M, Delmas P, Chagneux H (1998b) Encoding properties induced by a persistent voltage-gated muscarinic sodium current in rabbit sympathetic neurones. J Physiol (Lond) 510:387-399.
19. 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.
20. 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.
21. Guy J, Hendrich B, Holmes M, Martin JE, Bird A (2001) A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat Genet 27:322-326.
22. 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.
23. Haji A, Takeda R, Okazaki M (2000) Neuropharmacology of control of respiratory rhythm and pattern in mature mammals. Pharmacol Ther 86:277-304.
24. Harris-Warrick RM, Flamm RE (1987) Multiple mechanisms of bursting in a conditional bursting neuron. J Neurosci 7:2113-2128.
25. Herrero JF, Laird JM, Lopez-Garcia JA (2000) Wind-up of spinal cord neurones and pain sensation: much ado about something? Prog Neurobiol 61:169-203.
26. Hilaire G, Duron B (1999) Maturation of the mammalian respiratory system. Physiol Rev 79:325-360.
27. Inoue K, Nakazawa K, Inoue K, Fujimori K (1995) Nonselective cation channels coupled with tachykinin receptors in rat sensory neurons. J Neurophysiol 73:736-742.
28. Koyano K, Velimirovic BM, Grigg JJ, Nakajima S, Nakajima Y (1993) Two signal transduction mechanisms of substance P-induced depolarization in locus coeruleus neurons. Eur J Neurosci 5:1189-1197.
29. Lepre M, Olpe HR, Brugger F (1996) The effects of neurokinin-1 receptor agonists on spinal motoneurones of the neonatal rat. Neuropharmacology 35:511-522.
30. Lieske SP, Thoby-Brisson M, Telgkamp P, Ramirez JM (2000) Reconfiguration of the neural network controlling multiple breathing patterns: eupnea, sighs and gasps. Nat Neurosci 3:600-607.
31. Liu X, Andre D, Puizillout JJ (1998) Substance P post-synaptically potentiates glutamate-induced currents in dorsal vagal neurons. Brain Res 804:95-104.
32. Lugaresi E, Cirignotta F, Montagna P (1985) Abnormal breathing in the Rett syndrome. Brain Dev 7:329-333.
33. Marder E, Calabrese RL (1996) Principles of rhythmic motor pattern generation. Physiol Rev 76:687-717.
34. Marder E, Thirumalai V (2002) Cellular, synaptic and network effects of neuromodulation. Neural Netw 15:479-493.
35. Matsuishi T, Nagamitsu S, Yamashita Y, Murakami Y, Kimura A, Sakai T, Shoji H, Kato H, Percy AK (1997) Decreased cerebrospinal fluid levels of substance P in patients with Rett syndrome. Ann Neurol 42:978-981.
36. Moore KA, Taylor GE, Weinreich D (1999) Serotonin unmasks functional NK-2 receptors in vagal sensory neurones of the guinea-pig. J Physiol (Lond) 514:111-124.
37. Morisset V, Nagy F (1999) Ionic basis for plateau potentials in deep dorsal horn neurons of the rat spinal cord. J Neurosci 19:7309-7316.
38. Morton RE, Pinnington L, Ellis RE (2000) Air swallowing in Rett syndrome. Dev Med Child Neurol 42:271-275.
39. Neher E (1992) Correction for liquid junction potentials in patch clamp experiments. Methods Enzymol 207:123-131.
40. Nusbaum MP, Beenhakker MP (2002) A small-systems approach to motor pattern generation. Nature 417:343-350.
41. Oh EJ, Gover TD, Cordoba-Rodriguez R, Weinreich D (2003) Substance P evokes cation currents through TRP channels in HEK293 cells. J Neurophysiol 90:2069-2073.
42. Partridge LD, Valenzuela CF (2000) Block of hippocampal CAN channels by flufenamate. Brain Res 867:143-148.
43. Peña F, Ramirez JM (2002) Endogenous activation of serotonin 2A receptors is required for respiratory rhythm generation in vitro. J Neurosci 22:11055-11064.
44. Peña 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. Ptak K, Di Pasquale E, Monteau R (1999) Substance P and central respiratory activity: a comparative in vitro study on foetal and newborn rat. Brain Res Dev Brain Res 114:217-227.
46. Ptak K, Konrad M, Di Pasquale E, Tell F, Hilaire G, Monteau R (2000) Cellular and synaptic effect of substance P on neonatal phrenic motoneutons. Eur J Neurosci 12:126-138.
47. 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.
48. Raggenbass M, Dreifuss JJ (1992) Mechanism of action of oxytocin in rat vagal neurones: induction of a sustained sodium-dependent current. J Physiol (Lond) 457:131-142.
49. Ramirez JM, Quellmalz UJ, Richter DW (1996) Postnatal changes in the mammalian respiratory network as revealed by the transverse brainstem slice of mice. J Physiol (Lond) 491:799-812.
50. Saito Y, Ito M, Ozawa Y, Matsuishi T, Hamano K, Takashima S (2001) Reduced expression of neuropeptides can be related to respiratory disturbances in Rett syndrome. Brain Dev 23 [Suppl 1]:S122-S126.
51. Severini C, Improta G, Falconieri-Erspamer G, Salvadori S, Erspamer V (2002) The tachykinin peptide family. Pharmacol Rev 54:285-322.
52. Shen KZ, North RA (1992) Substance P opens cation channels and closes potassium channels in rat locus coeruleus neurons. Neuroscience 50:345-353.
53. 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.
54. Shvarev YN, Lagercrantz H, Yamamoto Y (2003) Two types of rhythm in the respiratory network output in the isolated ventrolateral medulla in the neonatal rats. Neurosci Lett 347:53-56.
55. 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.
56. Soejima T, Endoh T, Suzuki T (1999) Tachykinin-induced responses via neurokinin-1 and -3 receptors in hamster submandibular ganglion neurones. Arch Oral Biol 44:455-463.
57. Spigelman I, Puil E (1990) Ionic mechanism of substance P actions on neurons in trigeminal root ganglia. J Neurophysiol 64:273-281.
58. Stanfield PR, Nakajima Y, Yamaguchi K (1985) Substance P raises neuronal membrane excitability by reducing inward rectification. Nature 315:498-501.
59. Straub VA, Benjamin PR (2001) Extrinsic modulation and motor pattern generation in a feeding network: a cellular study. J Neurosci 21:1767-1778.
60. Telgkamp P, Ramirez JM (1999) Differential responses of respiratory nuclei to anoxia in rhythmic brain stem slices of mice. J Neurophysiol 82:2163-2170.
61. Telgkamp P, Cao YQ, Basbaum AI, Ramirez JM (2002) Long-term deprivation of substance P in PPT-A mutant mice alters the anoxic response of the isolated respiratory network. J Neurophysiol 88:206-213.
62. Thoby-Brisson M, Ramirez JM (2001) Identification of two types of inspiratory pacemaker neurons in the isolated respiratory neural network of mice. J Neurophysiol 86:104-112.
63. Thoby-Brisson M, Simmers J (2002) Long-term neuromodulatory regulation of a motor pattern-generating network: maintenance of synaptic efficacy and oscillatory properties. J Neurophysiol 88:2942-2953.
64. Tryba A, Pena F, Ramirez JM (2003) Stabilization of bursting in respiratory pacemaker neurons. J Neurosci 23:3838-3846.
65. Viemari JC, Burnet H, Bevengut M, Hilaire G (2003) Perinatal maturation of the mouse respiratory rhythm-generator: in vivo and in vitro studies. Eur J Neurosci 17:1233-1244.
66. Wang X, Robertson D (1998) Substance P-induced inward current in identified auditory efferent neurons in rat brain stem slices. J Neurophysiol 80:218-229.
67. Wang YY, Aghajanian GK (1987) Excitation of locus coeruleus neurons by an adenosine 3′,5′-cyclic monophosphate-activated inward current: extracellular and intracellular studies in rat brain slices. Synapse 1:481-487.
68. Weinreich D, Moore KA, Taylor GE (1997) Allergic inflammation in isolated vagal sensory ganglia unmasks silent NK-2 tachykinin receptors. J Neurosci 17:7683-7693.
69. Yamamoto Y, Onimaru H, Homma I (1992) Effect of substance P on respiratory rhythm and pre-inspiratory neurons in the ventrolateral structure of rostral medulla oblongata: an in vitro study. Brain Res 599:272-276.
70. Yasuda K, Robinson DM, Selvaratnam SR, Walsh CW, McMorland AJ, Funk GD (2001) Modulation of hypoglossal motoneuron excitability by NK1 receptor activation in neonatal mice in vitro. J Physiol (Lond) 534:447-464.