Formation and maintenance of ventilatory long-term facilitation require NMDA but not non-NMDA receptors in awake rats

Journal of Applied Physiology

Volumn 105, Issue 3, 2008, Pages 942-950

  McGuire, Michelle ^a   Liu, Chun ^a   Cao, Ying ^a   Ling, Liming ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

( ) 2 amino 5 phosphonovaleric acid; 6 cyano 7 nitroquinoxaline 2,3 dione; Intermittent hypoxia; N methyl D aspartate; Plasticity; Respiratory control

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; 2 AMINO 5 PHOSPHOPENTANOIC ACID; 2-AMINO-5-PHOSPHOPENTANOIC ACID; AMINO ACID RECEPTOR BLOCKING AGENT; DRUG DERIVATIVE; VALINE;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; FACILITATION; HYPOXIA; LUNG CAPACITY; LUNG VENTILATION; MALE; NONHUMAN; PLETHYSMOGRAPHY; PRIORITY JOURNAL; RAT; RESPIRATORY FUNCTION; SPRAGUE DAWLEY RAT; WAKEFULNESS; ANIMAL; ANOXIA; BREATHING MECHANICS; BREATHING MUSCLE; DISEASE MODEL; DRUG ANTAGONISM; HEART RATE; INNERVATION; LONG TERM POTENTIATION; METABOLISM; MOTONEURON; NERVE TRACT; PATHOPHYSIOLOGY; TIDAL VOLUME; TIME;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ANIMALS; ANOXIA; DISEASE MODELS, ANIMAL; EXCITATORY AMINO ACID ANTAGONISTS; HEART RATE; LONG-TERM POTENTIATION; MALE; MOTOR NEURONS; NEURAL PATHWAYS; PULMONARY VENTILATION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; RESPIRATORY MECHANICS; RESPIRATORY MUSCLES; TIDAL VOLUME; TIME FACTORS; VALINE; WAKEFULNESS;

EID: 53049105678     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.01274.2006     Document Type: Article

References (49)

1. Aboubakr SE, Taylor A, Ford R, Siddiqi S, Badr MS. Long-term facilitation in obstructive sleep apnea patients during NREM sleep. J Appl Physiol 91: 2751-2757, 2001.
2. Babcock MA, Badr MS. Long-term facilitation of ventilation in humans during NREM sleep. Sleep 21: 709-716, 1998.
3. Bach KB, Mitchell GS. Hypoxia-induced long-term facilitation of respiratory activity is serotonin dependent. Respir Physiol 104: 251-260, 1996.
4. Baker-Herman TL, Fuller DD, Bavis RW, Zabka AG, Golder FJ, Doperalski NJ, Johnson RA, Watters JJ, Mitchell GS. BDNF is necessary and sufficient for spinal respiratory plasticity following intermittent hypoxia. Nat Neurosci 7: 48-55, 2004.
5. Baker-Herman TL, Mitchell GS. Phrenic long-term facilitation requires spinal serotonin receptor activation and protein synthesis. J Neurosci 22: 6239-6246, 2002.
6. Blitz DM, Ramirez JM. Long-term modulation of respiratory network activity following anoxia in vitro. J Neurophysiol 87: 2964-2971, 2002.
7. Bocchiaro CM, Feldman JL. Synaptic activity-independent persistent plasticity in endogenously active mammalian motoneurons. Proc Natl Acad Sci USA 101: 4292-4295, 2004.
8. Cao KY, Zwillich CW, Berthon-Jones M, Sullivan CE. Increased normoxic ventilation induced by repetitive hypoxia in conscious dogs. J Appl Physiol 73: 2083-2088, 1992.
9. Castellano C, Cestari V, Ciamei A. NMDA receptors and learning and memory processes. Curr Drug Targets 2: 273-283, 2001.
10. Chitravanshi VC, Sapru HN. NMDA as well as non-NMDA receptors mediate the neurotransmission of inspiratory drive to phrenic motoneurons in the adult rat. Brain Res 715: 104-112, 1996.
11. Chowdhuri S, Pierchala L, Aboubakr SE, Shkoukani M, Badr MS. Long-term facilitation of genioglossus activity is present in normal humans during NREM sleep. Respir Physiol Neurobiol 160: 65-75, 2008.
12. Coles SK, Ernsberger P, Dick TE. A role for NMDA receptors in posthypoxic frequency decline in the rat. Am J Physiol Regul Integr Comp Physiol 274: R1546-R1555, 1998.
13. Eldridge F, Millhorn D. Oscillation, gating and memory in the respiratory control system. In: Handbook of Physiology. The Respiratory System. Control of Breathing. Bethesda, MD: Am. Physiol. Soc, 1986, sect. 3, vol. II, pt. I, chapt. 3, p. 93-114.
14. Feldman JL, Mitchell GS, Nattie. Breathing: rhythmicity EE, plasticity, chemosensitivity. Annu Rev Neurosci 26: 239-266, 2003.
15. Foutz AS, Champagnat J, Denavit-Saubie M. Respiratory effects of the N-methyl-D-aspartate (NMDA) antagonist, MK-801, in intact and vagotomized chronic cats. Eur J Pharmacol 154: 179-184, 1988.
16. Fregosi RF, Mitchell GS. Long-term facilitation of inspiratory intercostal nerve activity following carotid sinus nerve stimulation in cats. J Physiol 477: 469-479, 1994.
17. Fuller DD, Bach KB, Baker TL, Kinkead R, Mitchell GS. Long term facilitation of phrenic motor output. Respir Physiol 121: 135-146, 2000.
18. Fuller DD, Zabka AG, Baker TL, Mitchell GS. Phrenic long-term facilitation requires 5-HT receptor activation during but not following episodic hypoxia. J Appl Physiol 90: 2001-2006, 2001.
19. Harris DP, Balasubramaniam A, Badr MS, Mateika JH. Long-term facilitation of ventilation and genioglossus muscle activity is evident in the presence of elevated levels of carbon dioxide in awake humans. Am J Physiol Regul Integr Comp Physiol 291: R1111-R1119, 2006.
20. Hayashi F, Coles SK, Bach KB, Mitchell GS, McCrimmon DR. Time-dependent phrenic nerve responses to carotid afferent activation: intact vs. decerebellate rats. Am J Physiol Regul Integr Comp Physiol 265: R811-R819, 1993.
21. Jordan AS, Catcheside PG, O'Donoghue FJ, McEvoy RD. Long-term facilitation of ventilation is not present during wakefulness in healthy men or women. J Appl Physiol 93: 2129-2136, 2002.
22. Kandel ER. Cellular mechanisms of learning and the biological basis of individuality. In: Principles of Neural Science. New York: McGraw-Hill, 2000, p. 1247-1279.
23. Kent S, Kernahan SD, Levine S. Effects of excitatory amino acids on the hypothalamic-pituitary-adrenal axis of the neonatal rat. Brain Res Dev Brain Res 94: 1-13, 1996.
24. Kinkead R, Zhan WZ, Prakash YS, Bach KB, Sieck GC, Mitchell GS. Cervical dorsal rhizotomy enhances serotonergic innervation of phrenic motoneurons and serotonin-dependent long-term facilitation of respiratory motor output in rats. J Neurosci 18: 8436-8443, 1998.
25. Koyuncuoglu H, Kara I, Gunel MA, Nurten A, Yamanturk P. N-methyl-D-aspartate antagonists, glutamate release inhibitors, 4-aminopyridine at neuromuscular transmission. Pharmacol Res 37: 485-491, 1998.
26. Ling L, Fuller DD, Bach KB, Kinkead R, Olson EB Jr, Mitchell GS. Chronic intermittent hypoxia elicits serotonin-dependent plasticity in the central neural control of breathing. J Neurosci 21: 5381-5388, 2001.
27. Ling L, Karius DR, Speck DF. Role of N-methyl-D-aspartate receptors in the pontine pneumotaxic mechanism in the cat. J Appl Physiol 76: 1138-1143, 1994.
28. Ling L, Olson EB Jr, Vidruk EH, Mitchell GS. Integrated phrenic responses to carotid afferent stimulation in adult rats following perinatal hyperoxia. J Physiol 500: 787-796, 1997.
29. Malenka RC, Nicoll RA. Long-term potentiation-a decade of progress? Science 285: 1870-1874, 1999.
30. Mateika JH, Fregosi RF. Long-term facilitation of upper airway muscle activities in vagotomized and vagally intact cats. J Appl Physiol 82: 419-425, 1997.
31. McCrimmon DR, Smith JC, Feldman JL. Involvement of excitatory amino acids in neurotransmission of inspiratory drive to spinal respiratory motoneurons. J Neurosci 9: 1910-1921, 1989.
32. McGuire M, Ling L. Ventilatory long-term facilitation is greater in 1- vs. 2-mo-old awake rats. J Appl Physiol 98: 1195-1201, 2005.
33. McGuire M, Zhang Y, White DP, Ling L. Chronic intermittent hypoxia enhances ventilatory long-term facilitation in awake rats. J Appl Physiol 95: 1499-1508, 2003.
34. McGuire M, Zhang Y, White DP, Ling L. Effect of hypoxic episode number and severity on ventilatory long-term facilitation in awake rats. J Appl Physiol 93: 2155-2161, 2002.
35. McGuire M, Zhang Y, White DP, Ling L. Phrenic long-term facilitation requires NMDA receptors in the phrenic motonucleus in rats. J Physiol 567: 599-611, 2005.
36. McGuire M, Zhang Y, White DP, Ling L. Serotonin receptor subtypes required for ventilatory long-term facilitation and its enhancement after chronic intermittent hypoxia in awake rats. Am J Physiol Regul Integr Comp Physiol 286: R334-R341, 2004.
37. McKay LC, Janczewski WA, Feldman JL. Episodic hypoxia evokes long-term facilitation of genioglossus muscle activity in neonatal rats. J Physiol 557: 13-18, 2004.
38. Millhorn DE, Eldridge FL, Waldrop TG. Prolonged stimulation of respiration by a new central neural mechanism. Respir Physiol 41: 87-103, 1980.
39. Mitchell GS, Baker TL, Nanda SA, Fuller DD, Zabka AG, Hodgeman BA, Bavis RW, Mack KJ, Olson EB Jr. Invited review: Intermittent hypoxia and respiratory plasticity. J Appl Physiol 90: 2466-2475, 2001.
40. Mizusawa A, Ogawa H, Kikuchi Y, Hida W, Kurosawa H, Okabe S, Takishima T, Shirato K. In vivo release of glutamate in nucleus tractus solitarii of the rat during hypoxia. J Physiol 478: 55-66, 1994.
41. Monteau R, Gauthier P, Rega P, Hilaire G. Effects of N-methyl-D-aspartate (NMDA) antagonist MK-801 on breathing pattern in rats. Neurosci Lett 109: 134-139, 1990.
42. Morgado-Valle C, Feldman JL. NMDA receptors in preBotzinger complex neurons can drive respiratory rhythm independent of AMPA receptors. J Physiol 582: 359-368, 2007.
43. Morris KF, Shannon R, Lindsey BG. Changes in cat medullary neurone firing rates and synchrony following induction of respiratory long-term facilitation. J Physiol 532: 483-497, 2001.
44. Ohtake PJ, Torres JE, Gozal YM, Graff GR, Gozal D. NMDA receptors mediate peripheral chemoreceptor afferent input in the conscious rat. J Appl Physiol 84: 853-861, 1998.
45. Olson EB Jr, Bohne CJ, Dwinell MR, Podolsky A, Vidruk EH, Fuller DD, Powell FL, Mitchel GS. Ventilatory long-term facilitation in unanesthetized rats. J Appl Physiol 91: 709-716, 2001.
46. Steenland HW, Liu H, Sood S, Liu X, Horner RL. Respiratory activation of the genioglossus muscle involves both non-NMDA and NMDA glutamate receptors at the hypoglossal motor nucleus in vivo. Neuroscience 138: 1407-1424, 2006.
47. Swartzwelder HS, Ferrari C, Anderson WW, Wilson WA. The drug MK-801 attenuates the development, but not the expression, of long-term potentiation and stimulus train-induced bursting in hippocampal slices. Neuropharmacology 28: 441-445, 1989.
48. Tonegawa S. Mammalian learning and memory studied by gene targeting. Ann NY Acad Sci 758: 213-217, 1995.
49. Turner DL, Mitchell GS. Long-term facilitation of ventilation following repeated hypoxic episodes in awake goats. J Physiol 499: 543-550, 1997.