Diaphragm long-term facilitation following acute intermittent hypoxia during wakefulness and sleep

Journal of Applied Physiology

Volumn 110, Issue 5, 2011, Pages 1299-1310

  Terada, J ^a   Mitchell, G S ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Breathing; Metaplasticity; Respiratory muscle; Respiratory plasticity; Vigilance state

Indexed keywords

ANIMAL; ANOXIA; ARTICLE; BREATHING MECHANICS; DIAPHRAGM; INNERVATION; LONG TERM POTENTIATION; MALE; PATHOPHYSIOLOGY; RAT; SLEEP; SPRAGUE DAWLEY RAT; WAKEFULNESS;

ANIMALS; ANOXIA; DIAPHRAGM; LONG-TERM POTENTIATION; MALE; RATS; RATS, SPRAGUE-DAWLEY; RESPIRATORY MECHANICS; SLEEP; WAKEFULNESS;

EID: 79956083355     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00055.2011     Document Type: Article

References (64)

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. (Pubitemid 33108042)
2. Babcock M, Shkoukani M, Aboubakr SE, Badr MS. Determinants of long-term facilitation in humans during NREM sleep. J Appl Physiol 94: 53-59, 2003. (Pubitemid 36014295)
3. Babcock MA, Badr MS. Long-term facilitation of ventilation in humans during NREM sleep. Sleep 21: 709-716, 1998. (Pubitemid 28516162)
4. Baker-Herman TL, Bavis RW, Dahlberg JM, Mitchell AZ, Wilkerson JE, Golder FJ, Macfarlane PM, Watters JJ, Behan M, Mitchell GS. Differential expression of respiratory long-term facilitation among inbred rat strains. Respir Physiol Neurobiol 170: 260-267, 2010.
5. 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. (Pubitemid 38032167)
6. Baker-Herman TL, Mitchell GS. Determinants of frequency long-term facilitation following acute intermittent hypoxia in vagotomized rats. Respir Physiol Neurobiol 162: 8-17, 2008. (Pubitemid 351794578)
7. Baker-Herman TL, Mitchell GS. Phrenic long-term facilitation requires spinal serotonin receptor activation and protein synthesis. J Neurosci 22: 6239-6246, 2002. (Pubitemid 35387664)
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. Dale-Nagle EA, Hoffman MS, MacFarlane PM, Mitchell GS. Multiple pathways to long-lasting phrenic motor facilitation. Adv Exp Med Biol 669: 225-230, 2010.
10. Dale-Nagle EA, Hoffman MS, MacFarlane PM, Satriotomo I, Lovett-Barr MR, Vinit S, Mitchell GS. Spinal plasticity following intermittent hypoxia: implications for spinal injury. Ann NY Acad Sci 1198: 252-259, 2010.
11. Eldridge FL. Relationship between phrenic nerve activity and ventilation. Am J Physiol 221: 535-543, 1971.
12. Feldman JL, Mitchell GS, Nattie EE. Breathing: rhythmicity, plasticity, chemosensitivity. Annu Rev Neurosci 26: 239-266, 2003. (Pubitemid 37064934)
13. Fletcher EC, Lesske J, Qian W, Miller CC, 3rd, Unger T. Repetitive, episodic hypoxia causes diurnal elevation of blood pressure in rats. Hypertension 19: 555-561, 1992.
14. Frappell P, Lanthier C, Baudinette RV, Mortola JP. Metabolism and ventilation in acute hypoxia: a comparative analysis in small mammalian species. Am J Physiol Regul Integr Comp Physiol 262: R1040-R1046, 1992.
15. Fregosi RF, Mitchell GS. Long-term facilitation of inspiratory intercostals nerve activity following carotid sinus nerve stimulation in cats. J Physiol 477 (Pt 3): 469-479, 1994.
16. Fuller DD, Baker TL, Behan M, Mitchell GS. Expression of hypoglossal long-term facilitation differs between substrains of Sprague-Dawley rat. Physiol Genomics 4: 175-181, 2001. (Pubitemid 33676693)
17. Fuller DD, Johnson SM, Olson EB Jr., Mitchell GS. Synaptic pathways to phrenic motoneurons are enhanced by chronic intermittent hypoxia after cervical spinal cord injury. J Neurosci 23: 2993-3000, 2003. (Pubitemid 36418635)
18. Gerst DG, 3rd Yokhana SS, Carney LM, Lee DS, Badr MS, Qureshi T, Anthouard MN, Mateika JH. The hypoxic ventilatory response and ventilatory long term facilitation are altered by time of day and repeated daily exposure to intermittent hypoxia. J Appl Physiol 2010.
19. Golder FJ, Ranganathan L, Satriotomo I, Hoffman M, Lovett-Barr MR, Watters JJ, Baker-Herman TL, Mitchell GS. Spinal adenosine A2a receptor activation elicits long-lasting phrenic motor facilitation. J Neurosci 28: 2033-2042, 2008. (Pubitemid 351317619)
20. Gordon CJ, Fogelson L. Comparative effects of hypoxia on behavioral thermoregulation in rats, hamsters, and mice. Am J Physiol Regul Integr Comp Physiol 260: R120-R125, 1991.
21. Gozal D, Daniel JM, Dohanich GP. Behavioral and anatomical correlates of chronic episodic hypoxia during sleep in the rat. J Neurosci 21: 2442-2450, 2001. (Pubitemid 32240541)
22. 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. (Pubitemid 44498453)
23. Hoffman MS, Golder FJ, Mahamed S, Mitchell GS. Spinal adenosine A2(A) receptor inhibition enhances phrenic long term facilitation following acute intermittent hypoxia. J Physiol 588: 255-266, 2010.
24. Horner RL. Neuromodulation of hypoglossal motoneurons during sleep. Respir Physiol Neurobiol 164: 179-196, 2008.
25. 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. (Pubitemid 35379340)
26. Kline DD, Overholt JL, Prabhakar NR. Mutant mice deficient in NOS-1 exhibit attenuated long-term facilitation and short-term potentiation in breathing. J Physiol 539: 309-315, 2002. (Pubitemid 35190117)
27. Kuwaki T. Orexinergic modulation of breathing across vigilance states. Respir Physiol Neurobiol 164: 204-212, 2008.
28. 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. (Pubitemid 32622965)
29. Lovett-Barr MR, Mitchell GS, Satriotomo I, Johnson SM. Serotonininduced in vitro long-term facilitation exhibits differential pattern sensitivity in cervical and thoracic inspiratory motor output. Neuroscience 142: 885-892, 2006. (Pubitemid 44488661)
30. MacFarlane PM, Mitchell GS. Respiratory long-term facilitation following intermittent hypoxia requires reactive oxygen species formation. Neuroscience 152: 189-197, 2008.
31. Mahamed S, Mitchell GS. Is there a link between intermittent hypoxiainduced respiratory plasticity and obstructive sleep apnoea? Exp Physiol 92: 27-37, 2007. (Pubitemid 46096251)
32. Mahamed S, Mitchell GS. Respiratory long-term facilitation: too much or too little of a good thing? Adv Exp Med Biol 605: 224-227, 2008.
33. Mantilla CB, Seven YB, Zhan WZ, Sieck GC. Diaphragm motor unit recruitment in rats. Respir Physiol Neurobiol 173: 101-106, 2010.
34. Mateika JH, Narwani G. Intermittent hypoxia and respiratory plasticity in humans and other animals: does exposure to intermittent hypoxia promote or mitigate sleep apnoea? Exp Physiol 94: 279-296, 2009.
35. McEvoy RD, Popovic RM, Saunders NA, White DP. Effects of sustained and repetitive isocapnic hypoxia on ventilation and genioglossal and diaphragmatic EMGs. J Appl Physiol 81: 866-875, 1996. (Pubitemid 26303243)
36. McGuire M, Tartar JL, Cao Y, McCarley RW, White DP, Strecker RE, Ling L. Sleep fragmentation impairs ventilatory long-term facilitation via adenosine A1 receptors. J Physiol 586: 5215-5229, 2008.
37. 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. (Pubitemid 37169294)
38. 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. (Pubitemid 35379343)
39. Mitchell GS. Respiratory plasticity following intermittent hypoxia: guide for novel therapeutic approaches to ventilatory control disorders. In Genetic Basis for Respiratory Control Disorders, edited by Gaultier C. New York: Springer, 2007.
40. 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.
41. Mitchell GS, Johnson SM. Neuroplasticity in respiratory motor control. J Appl Physiol 94: 358-374, 2003.
42. Mitchell GS, Powell FL, Hopkins SR, Milsom WK. Time domains of the hypoxic ventilatory response in awake ducks: episodic and continuous hypoxia. Respir Physiol 124: 117-128, 2001. (Pubitemid 32042486)
43. Nakamura A, Fukuda Y, Kuwaki T. Sleep apnea and effect of chemostimulation on breathing instability in mice. J Appl Physiol 94: 525-532, 2003. (Pubitemid 36158227)
44. Nakamura A, Olson EB Jr., Terada J, Wenninger JM, Bisgard GE, Mitchell GS. Sleep state dependence of ventilatory long-term facilitation following acute intermittent hypoxia in Lewis rats. J Appl Physiol 109: 323-331, 2010.
45. Neverova NV, Saywell SA, Nashold LJ, Mitchell GS, Feldman JL. Episodic stimulation of α1-adrenoreceptors induces protein kinase C-dependent persistent changes in motoneuronal excitability. J Neurosci 27: 4435-4442, 2007. (Pubitemid 46640704)
46. 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. (Pubitemid 32681102)
47. Pierchala LA, Mohammed AS, Grullon K, Mateika JH, Badr MS. Ventilatory long-term facilitation in nonsnoring subjects during NREM sleep. Respir Physiol Neurobiol 160: 259-266, 2008. (Pubitemid 351754796)
48. Polotsky VY, Rubin AE, Balbir A, Dean T, Smith PL, Schwartz AR, O'Donnell CP. Intermittent hypoxia causes REM sleep deficits and decreases EEG delta power in NREM sleep in the C57BL/6J mouse. Sleep Med 7: 7-16, 2006. (Pubitemid 43033539)
49. Powell FL, Milsom WK, Mitchell GS. Time domains of the hypoxic ventilatory response. Respir Physiol 112: 123-134, 1998. (Pubitemid 28310754)
50. Row BW, Liu R, Xu W, Kheirandish L, Gozal D. Intermittent hypoxia is associated with oxidative stress and spatial learning deficits in the rat. Am J Respir Crit Care Med 167: 1548-1553, 2003. (Pubitemid 37363366)
51. Saiki C, Matsuoka T, Mortola JP. Metabolic-ventilatory interaction in conscious rats: effect of hypoxia and ambient temperature. J Appl Physiol 76: 1594-1599, 1994. (Pubitemid 24125678)
52. Sood S, Morrison JL, Liu H, Horner RL. Role of endogenous serotonin in modulating genioglossus muscle activity in awake and sleeping rats. Am J Respir Crit Care Med 172: 1338-1347, 2005. (Pubitemid 43076574)
53. Tartar JL, Ward CP, McKenna JT, Thakkar M, Arrigoni E, Mc-Carley RW, Brown RE, Strecker RE. Hippocampal synaptic plasticity and spatial learning are impaired in a rat model of sleep fragmentation. Eur J Neurosci 23: 2739-2748, 2006. (Pubitemid 43801466)
54. Tasali E, Ip MS. Obstructive sleep apnea and metabolic syndrome: alterations in glucose metabolism and inflammation. Proc Am Thorac Soc 5: 207-217, 2008. (Pubitemid 351237880)
55. Terada J, Nakamura A, Zhang W, Yanagisawa M, Kuriyama T, Fukuda Y, Kuwaki T. Ventilatory long-term facilitation in mice can be observed during both sleep and wake periods and depends on orexin. J Appl Physiol 104: 499-507, 2008. (Pubitemid 351231495)
56. Thakkar MM, Winston S, McCarley RW. A1 receptor and adenosinergic homeostatic regulation of sleep-wakefulness: effects of antisense to the A1 receptor in the cholinergic basal forebrain. J Neurosci 23: 4278-4287, 2003. (Pubitemid 36958448)
57. Turner DL, Mitchell GS. Long-term facilitation of ventilation following repeated hypoxic episodes in awake goats. J Physiol 499 (Pt 2): 543-550, 1997.
58. Veasey SC, Davis CW, Fenik P, Zhan G, Hsu YJ, Pratico D, Gow A. Long-term intermittent hypoxia in mice: protracted hypersomnolence with oxidative injury to sleep-wake brain regions. Sleep 27: 194-201, 2004. (Pubitemid 44138826)
59. Vecchio LM, Grace KP, Liu H, Harding S, Le AD, Horner RL. State-dependent vs. central motor effects of ethanol on breathing. J Appl Physiol 108: 387-400, 2010.
60. Vinit S, Lovett-Barr MR, Mitchell GS. Intermittent hypoxia induces functional recovery following cervical spinal injury. Respir Physiol Neurobiol 169: 210-217, 2009.
61. Wenninger JM, Olson EB, Wang Z, Keith IM, Mitchell GS, Bisgard GE. Carotid sinus nerve responses and ventilatory acclimatization to hypoxia in adult rats following 2 wk of postnatal hyperoxia. Respir Physiol Neurobiol 150: 155-164, 2006. (Pubitemid 43227454)
62. Wilkerson JE, Mitchell GS. Daily intermittent hypoxia augments spinal BDNF levels, ERK phosphorylation and respiratory long-term facilitation. Exp Neurol 217: 116-123, 2009.
63. Zabka AG, Behan M, Mitchell GS. Selected contribution: Time-dependent hypoxic respiratory responses in female rats are influenced by age and by the estrus cycle. J Appl Physiol 91: 2831-2838, 2001. (Pubitemid 33108051)
64. Zabka AG, Mitchell GS, Olson EB Jr., Behan M. Selected contribution: chronic intermittent hypoxia enhances respiratory long-term facilitation in geriatric female rats. J Appl Physiol 95: 2614-2623; discussion 2604, 2003. (Pubitemid 37445011)