Determinants of frequency long-term facilitation following acute intermittent hypoxia in vagotomized rats

Respiratory Physiology and Neurobiology

Volumn 162, Issue 1, 2008, Pages 8-17

  Baker Herman, Tracy L ^a   Mitchell, Gordon S ^a,b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Intermittent hypoxia; LTF; Meta analysis; Phrenic nerve; Rat; Respiratory frequency; Respiratory plasticity; Sustained hypoxia; Ventilatory control

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BREATHING; CARBON DIOXIDE TENSION; CONTROLLED STUDY; FACILITATION; HYPOXIA; MALE; MULTIPLE REGRESSION; NERVE CELL PLASTICITY; NONHUMAN; PHRENIC NERVE; PRIORITY JOURNAL; RAT; VAGOTOMY;

ANIMALS; ANOXIA; LONG-TERM POTENTIATION; MALE; PHRENIC NERVE; RATS; RATS, SPRAGUE-DAWLEY; REGRESSION ANALYSIS; TIME FACTORS; VAGOTOMY;

EID: 44849138769     PISSN: 15699048     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.resp.2008.03.005     Document Type: Article

References (82)

1. Aston-Jones G., and Bloom F.E. Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle. J. Neurosci. 1 (1981) 876-886
2. Bach K.B., and Mitchell G.S. Hypoxia-induced long-term facilitation of respiratory activity is serotonin dependent. Respir. Physiol. 104 (1996) 251-260
3. Bach K.B., and Mitchell G.S. Effects of phenicotomy and exercise on hypoxia-induced changes in respiratory output. J. Appl. Physiol. 89 (2000) 1884-1891
4. Baker T.L., and Mitchell G.S. Episodic but not continuous hypoxia elicits long-term facilitation of phrenic motor output in rats. J. Physiol. 529 (2000) 215-219
5. Baker T.L., Fuller D.D., Zabka A.G., and Mitchell G.S. Respiratory plasticity: differential actions of continuous and episodic hypoxia and hypercapnia. Respir. Physiol. 129 (2001) 25-35
6. Baker-Herman T.L., and Mitchell G.S. Phrenic long-term facilitation requires spinal serotonin receptor activation and protein synthesis. J. Neurosci. 22 (2002) 6239-6244
7. Baker-Herman T.L., Fuller D.D., Bavis R.W., Zabka A.G., Golder F.J., Doperalski N.J., Johnson R.A., Watters J.J., and Mitchell G.S. BDNF is necessary and sufficient for spinal respiratory plasticity following intermittent hypoxia. Nat. Neurosci. 7 (2004) 48-55
8. Bavis R.W., and Mitchell G.S. Intermittent hypoxia induces phrenic long-term facilitation in carotid-denervated rats. J. Appl. Physiol. 94 (2003) 399-409
9. Behan M., Zabka A.G., Thomas C.F., and Mitchell G.S. Sex steroid hormones and the neural control of breathing. Respir. Physiol. Neurobiol. 136 (2003) 249-263
10. Berner J., Shvarev Y., Lagercrantz H., Bilkei-Gorzo A., Hokfelt T., and Wickstrom R. Altered respiratory pattern and hypoxic response in transgenic newborn mice lacking the tachykinin-1 gene. J. Appl. Physiol. 103 (2007) 552-559
11. Bicego K.C., Barros R.C., and Branco L.G. Physiology of temperature regulation: comparative aspects. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 147 July (3) (2007) 616-639
12. Blitz D.M., and Ramirez J.M. Long-term modulation of respiratory network activity following anoxia in vitro. J. Neurophysiol. 87 (2002) 2964-2971
13. Bocchiaro C.M., and Feldman J.L. Synaptic activity-independent persistent plasticity in endogenously active mammalian motoneurons. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 4292-4295
14. Dick T.E., Hsieh Y.H., Wang N., and Prabhakar N. Acute intermittent hypoxia increases both phrenic and sympathetic nerve activities in the rat. Exp. Physiol. 92 (2007) 87-97
15. Doperalski N.J., and Fuller D.D. Long-term facilitation of ipsilateral but not contralateral phrenic output after cervical spinal cord hemisection. Exp. Neurol. 200 (2006) 74-81
16. Dwinell M.R., Janssen P.L., and Bisgard G.E. Lack of long-term facilitation of ventilation after exposure to hypoxia in goats. Respir. Physiol. 108 (1997) 1-9
17. Eldridge F.L., and Millhorn D.E. Oscillation, gating, and memory in the respiratory control system. In: Fishman A.P., and Fisher A.B. (Eds). Handbook of Physiology. Section 3: The Respiratory System. Circulation and Nonrespiratory Functions, vol. 1 (1986), American Physiological Society, Washington DC 93-114
18. Feldman J.L., Mitchell G.S., and Nattie E.E. Breathing: rhythmicity, plasticity, chemosensitivity. Annu. Rev. Neurosci. 26 (2003) 239-266
19. Fuller D.D., Bach K.B., Baker T.L., Kinkead R., and Mitchell G.S. Long term facilitation of phrenic motor output. Respir. Physiol. 121 (2000) 135-146
20. Fuller D.D., Zabka A.G., Baker T.L., and Mitchell G.S. Phrenic long-term facilitation requires 5-HT receptor activation during but not following episodic hypoxia. J. Appl. Physiol. 90 (2001) 2001-2006
21. Fuller D.D., Baker T.L., Behan M., and Mitchell G.S. Expression of hypoglossal long-term facilitation differs between substrains of Sprague-Dawley rat. Physiol. Genomics 4 (2001) 175-181
22. Fuller D.D. Episodic hypoxia induces long-term facilitation of neural drive to tongue protrudor and retractor muscles. J. Appl. Physiol. 98 (2005) 1761-1767
23. Golder F.J., and Mitchell G.S. Spinal synaptic enhancement with acute intermittent hypoxia improves respiratory function after chronic cervical spinal cord injury. J. Neurosci. 25 (2005) 2925-2932
24. Golder F.J., Ranganathan L., Satriotomo I., Hoffman M., Lovett-Barr M.R., Watters J.J., Baker-Herman T.L., and Mitchell G.S. Spinal adenosine A2a receptor activation elicits long-lasting phrenic motor facilitation. J. Neurosci. 28 9 (2008) 2033-2042
25. Grunstein M.M., Fisk W.M., Leiter L.A., and Milic-Emili J. Effect of body temperature on respiratory frequency in anesthetized cats. J. Appl. Physiol. 34 (1973) 154-159
26. Hayashi F., Coles S.K., Bach K.B., Mitchell G.S., and McCrimmon D.R. Time-dependent phrenic nerve responses to carotid afferent activation: intact vs. decerebellate rats. Am. J. Physiol. 265 (1993) R811-R819
27. Horner R.L. Respiratory motor activity: influence of neuromodulators and implications for sleep disordered breathing. Can. J. Physiol. Pharmacol. 85 (2007) 155-165
28. Hsieh Y.H., Dick T.E., and Siegel R.E. Adaptation to hypobaric hypoxia involves GABA A receptors in the pons. Am. J. Physiol. Regul. Integr. Comp. Physiol. 294 (2008) R549-R557
29. Huey K.A., Szewczak J.M., and Powell F.L. Dopaminergic mechanisms of neural plasticity in respiratory control: transgenic approaches. Respir. Physiol. Neurobiol. 135 (2003) 133-144
30. Jacobs B.L., and Fornal C.A. Activity of serotonergic neurons in behaving animals. Neuropsychopharmacology 21 (1999) 9S-15S
31. Janssen P.L., and Fregosi R.F. No evidence for long-term facilitation after episodic hypoxia in spontaneously breathing, anesthetized rats. J. Appl. Physiol. 89 (2000) 1345-1351
32. Julien C., Bairam A., and Joseph V. Chronic intermittent hypoxia reduces ventilatory long-term facilitation and enhances apnea frequency in newborn rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. (February 2008) (Epub ahead of print) PMID: 18287216
33. Kushikata T., Hirota K., Kotani N., Yoshida H., Kudo M., and Matsuki A. Isoflurane increases norepinephrine release in the rat preoptic area and the posterior hypothalamus in vivo and in vitro: relevance to thermoregulation during anesthesia. Neuroscience 131 (2005) 79-86
34. Kinkead R., Zhan W.Z., Prakash Y.S., Bach K.B., Sieck G.C., and Mitchell G.S. Cervical dorsal rhizotomy enhances serotonergic innervation of phrenic motoneurons and serotonin-dependent long-term facilitation of respiratory motor output in rats. J. Neurosci. 18 (1998) 8436-8443
35. Kinkead R., and Mitchell G.S. Time-dependent hypoxic ventilatory responses in rats: effects of ketanserin and 5-carboxamidotryptamine. Am. J. Physiol. 277 (1999) R658-R666
36. Kline D.D., Overholt J.L., and Prabhakar N.R. Mutant mice deficient in NOS-1 exhibit attenuated long-term facilitation and short-term potentiation in breathing. J. Physiol. 539 (2002) 309-315
37. Ling L., Fuller D.D., Bach K.B., Kinkead R., Olson Jr. E.B., Behan M., and Mitchell G.S. Chronic intermittent hypoxia elicits serotonin-dependent plasticity in the central neural control of breathing. J. Neurosci. 21: (2001) 5381-5388
38. Lovett-Barr M.R., Mitchell G.S., Satriotomo I., and Johnson S.M. Serotonin-induced in vitro long-term facilitation exhibits differential pattern sensitivity in cervical and thoracic inspiratory motor output. Neuroscience 142 (2006) 885-892
39. MacFarlane P.M., and Mitchell G.S. Serotonin-induced phrenic long-term facilitation requires reactive oxygen species signaling via the NADPH oxidase complex. Soc. Neurosci. Abst. (2007)
40. MacFarlane P.M., and Mitchell G.S. Respiratory long-term facilitation following intermittent hypoxia requires reactive oxygen species formation. Neuroscience (2007) (Epub ahead of print) PMID: 18207649
41. Mahamed S., and Mitchell G.S. Is there a link between intermittent hypoxia-induced respiratory plasticity and obstructive sleep apnoea?. Exp. Physiol. 92 (2006) 27-37
42. Mahamed S., and Mitchell G.S. Simulated apneas induce serotonin dependent respiratory long term facilitation in rats. J. Physiol. (2008) (Epub ahead of print) PMID: 18292130
43. Mateika J.H., and Fregosi R.F. Long-term facilitation of upper airway muscle activities in vagotomized and vagally intact cats. J. Appl. Physiol. 82 (1997) 419-425
44. McGuire M., Zhang Y., White D.P., and Ling L. Effect of hypoxic episode number and severity on ventilatory long-term facilitation in awake rats. J. Appl. Physiol. 93 (2002) 2155-2161
45. McGuire M., Zhang Y., White D.P., and Ling L. Chronic intermittent hypoxia enhances ventilatory long-term facilitation in awake rats. J. Appl. Physiol. 95 (2003) 1499-1508
46. McGuire M., Zhang Y., White D.P., and 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 (2004) R334-R341
47. McGuire M., and Ling L. Ventilatory long-term facilitation is greater in 1- vs. 2-mo-old awake rats. J. Appl. Physiol. 98 (2005) 1195-1201
48. McGuire M., Zhang Y., White D.P., and Ling L. Phrenic long-term facilitation requires NMDA receptors in the phrenic motonucleus in rats. J. Physiol. 567 (2005) 599-611
49. McGuire M., MacDonald S.M., Song G., and Poon C.S. Phrenic long-term facilitation is robust to hypercapnia and hypocapnia but not hyperventilatory hypotension under PEEP. Respir. Physiol. Neurobiol. 158 (2007) 107-111
50. McKay L.C., Janczewski W.A., and Feldman J.L. Episodic hypoxia evokes long-term facilitation of genioglossus muscle activity in neonatal rats. J. Physiol. 557 (2004) 13-18
51. Millhorn D.E., Eldridge F.L., and Waldrop T.G. Prolonged stimulation of respiration by endogenous central serotonin. Respir. Physiol. 42 (1980) 171-188
52. Millhorn D.E., Eldridge F.L., and Waldrop T.G. Prolonged stimulation of respiration by a new central neural mechanism. Respir. Physiol. 41 (1980) 87-103
53. Mitchell G.S., and Johnson S.M. Neuroplasticity in respiratory motor control. J. Appl. Physiol. 94 (2003) 358-374
54. Mitchell G.S., Baker T.L., Nanda S.A., Fuller D.D., Zabka A.G., Hodgeman B.A., Bavis R.W., Mack K.J., and Olson Jr. E.B. Invited review: intermittent hypoxia and respiratory plasticity. J. Appl. Physiol. 90 (2001) 2466-2475
55. Mitchell G.S., Powell F.L., Hopkins S.R., and Milsom W.K. Time domains of the hypoxic ventilatory response in awake ducks: episodic and continuous hypoxia. Respir. Physiol. 124 2 (2001) 117-128
56. Morris K.F., Arata A., Shannon R., and Lindsey B.G. Long-term facilitation of phrenic nerve activity in cats: responses and short time scale correlations of medullary neurones. J. Physiol. 490 (1996) 463-480
57. Morris K.F., Shannon R., and Lindsey B.G. Changes in cat medullary neurone firing rates and synchrony following induction of respiratory long-term facilitation. J. Physiol. 532 (2001) 483-497
58. Mukaida K., Shichino T., Koyanagi S., Himukashi S., and Fukuda K. Activity of the serotonergic system during isoflurane anesthesia. Anesth. Analg. 104 (2007) 836-839
59. Nakamura A., Wenninger J.M., Olson Jr. E.B., Bisgard G.E., and Mitchell G.S. Ventilatory long-term facilitation following intermittent hypoxia is state-dependent in rats. J. Physiol. Sci. 56 (2006) S75
60. Neverova N.V., Saywell S.A., Nashold L.J., Mitchell G.S., and Feldman J.L. Episodic stimulation of alpha1-adrenoreceptors induces protein kinase C-dependent persistent changes in motoneuronal excitability. J. Neurosci. 27 (2007) 4435-4442
61. Olson Jr. E.B., Bohne C.J., Dwinell M.R., Podolsky A., Vidruk E.H., Fuller D.D., Powell F.L., and Mitchel G.S. Ventilatory long-term facilitation in unanesthetized rats. J. Appl. Physiol. 91 (2001) 709-716
62. Onimaru H., Shamoto A., and Homma I. Modulation of respiratory rhythm by 5-HT in the brainstem-spinal cord preparation from newborn rat. Pflugers Arch. 435 (1998) 485-494
63. Peng Y.J., and Prabhakar N.R. Reactive oxygen species in the plasticity of respiratory behavior elicited by chronic intermittent hypoxia. J. Appl. Physiol. 94 (2003) 2342-2349
64. Pierchala L.A., Mohammed A.S., Grullon K., Mateika J.H., and Badr M.S. Ventilatory long-term facilitation in non-snoring subjects during NREM sleep. Respir. Physiol. Neurobiol. (October 2007) (Epub ahead of print)
65. Powell F.L., Milsom W.K., and Mitchell G.S. Time domains of the hypoxic ventilatory response. Respir. Physiol. 112 (1998) 123-134
66. Prabhakar N.R., Peng Y.J., Kumar G.K., and Pawar A. Altered carotid body function by intermittent hypoxia in neonates and adults: relevance to recurrent apneas. Respir. Physiol. Neurobiol. 157 (2007) 148-153
67. Reeves S.R., Mitchell G.S., and Gozal D. Early postnatal chronic intermittent hypoxia modifies hypoxic respiratory responses and long-term phrenic facilitation in adult rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290 (2006) R1664-R1671
68. Reeves S.R., and Gozal D. Protein kinase C activity in the nucleus tractus solitarii is critically involved in the acute hypoxic ventilatory response, but is not required for intermittent hypoxia-induced phrenic long-term facilitation in adult rats. Exp. Physiol. 92 (2007) 1057-1066
69. Shimokawa A., Jin Q.H., Ishizuka Y., Kunitake T., Takasaki M., and Kannan H. Effects of anesthetics on norepinephrine release in the hypothalamic paraventricular nucleus region of awake rats. Neurosci. Lett. 244 (1998) 21-24
70. Tadjalli A., Duffin J., Li Y.M., Hong H., and Peever J.H. Inspiratory activation is not required for episodic hypoxia-induced respiratory long-term facilitation in postnatal rats. J. Physiol. 585 (2007) 593-606
71. Terada J., Nakamura A., Zhang W., Yanagisawa M., Kuriyama T., Fukuda Y., and Kuwaki T. Ventilatory long-term facilitation in mice can be observed both during sleep and wake periods and depends on orexin. J. Appl. Physiol. 104 (2008) 499-507
72. Turner D.L., and Mitchell G.S. Long-term facilitation of ventilation following repeated hypoxic episodes in awake goats. J. Physiol. (Lond.) 499 (1997) 543-550
73. Veasey S.C., Fornal C.A., Metzler C.W., and Jacobs B.L. Response of serotonergic caudal raphe neurons in relation to specific motor activities in freely moving cats. J. Neurosci. 15 (1995) 5346-5359
74. Wilkerson J.E.R., MacFarlane P.M., Hoffman M.S., and Mitchell G.S. Respiratory plasticity following intermittent hypoxia: roles of protein phosphatases and reactive oxygen species. Biochem. Soc. Trans. 35 (2007) 1269-1272
75. Wilkerson J.E.R., MacFarlane P.M., Hoffman M., Satriotomo I., Baker-Herman T.L., Watters J.J., and Mitchell G.S. Okadaic acid-sensitive protein phosphatases constrain phrenic long-term facilitation following sustained hypoxia. J. Neurosci. 28 (2008) 2949-2958
76. Zabka A.G., Behan M., and Mitchell G.S. Long term facilitation of respiratory motor output decreases with age in male rats. J. Physiol. 531 (2001) 509-514
77. Zabka A.G., Behan M., and Mitchell G.S. Selected contribution: time-dependent hypoxic respiratory responses in female rats are influenced by age and by the estrus cycle. J. Appl. Physiol. 91 (2001) 2831-2838
78. Zabka A.G., Mitchell G.S., Olson Jr. E.B., and Behan M. Selected contribution: chronic intermittent hypoxia enhances respiratory long-term facilitation in geriatric female rats. J. Appl. Physiol. 95 (2003) 2614-2623
79. Zabka A.G., Mitchell G.S., and Behan M. Ageing and gonadectomy have similar effects on hypoglossal long-term facilitation in male Fischer rats. J. Physiol. 563 (2005) 557-568
80. Zabka A.G., Behan M., and Mitchell G.S. Conversion from testosterone to oestradiol is required to modulate respiratory long-term facilitation in male rats. J. Physiol. 576 (2006) 903-912
81. Zhou M. Silent glutamatergic synapses and long-term facilitation in spinal dorsal horn neurons. Prog. Brain Res. 129 (2000) 101-113
82. Zimmer M.B., Nantwi K., and Goshgarian H.G. Effect of spinal cord injury on the respiratory system: basic research and current clinical treatment options. J. Spinal Cord Med. 30 (2007) 319-330