Spinal metaplasticity in respiratory motor control

Frontiers in Neural Circuits

Volumn 9, Issue FEB, 2015, Pages

  Fields, Daryl P ^a   Mitchell, Gordon S ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Intermittent hypoxia; Metaplasticity; Motor neuron; Phrenic motor neuron; Respiratory control; Respiratory plasticity; Spinal cord

Indexed keywords

ADENOSINE A2 RECEPTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; PROTEIN KINASE C; SEROTONIN; SEROTONIN 2 RECEPTOR; SEROTONIN 7 RECEPTOR; SUBSTANCE P;

AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CAROTID BODY CHEMORECEPTOR; CAROTID SINUS NERVE; CERVICAL SPINAL CORD INJURY; DORSAL RHIZOTOMY; FACILITATION; HUMAN; INTERMITTENT HYPOXIA; LIMB MOVEMENT; MOTOR CONTROL; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; PHRENIC LONG TERM FACILITATION; PHRENIC NERVE; RESPIRATION CONTROL; RESPIRATORY NERVE CELL; SEROTONIN RELEASE; SLEEP DISORDERED BREATHING; SOLITARY TRACT NUCLEUS; SPINAL METAPLASTICITY; ANIMAL; BREATHING; PHYSIOLOGY; SPINAL CORD;

ANIMALS; HUMANS; NEURONAL PLASTICITY; RESPIRATION; SPINAL CORD;

EID: 84923276042     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2015.00002     Document Type: Article

References (99)

1. Abraham, W. C. (2008). Metaplasticity: Tuning synapses and networks for plasticity.Nat. Rev. Neurosci. 9:387.doi: 10.1038/nrn2356
2. Abraham, W. C., and Bear, M. F. (1996). Metaplasticity: The plasticity of synaptic plasticity. Trends Neurosci. 19, 126-130.doi: 10.1016/s0166-2236(96)80018-x
3. Alberini, C. M. (2008). The role of protein synthesis during the labile phases of memory: Revisiting the skepticism. Neurobiol. Learn. Mem. 89, 234-246.doi: 10.1016/j.nlm.2007.08.007
4. Bach, K. B., and Mitchell, G. S. (1996). Hypoxia-induced long-term facilitation of respiratoryactivityis serotonin dependent. Respir. Physiol. 104, 251-260.doi: 10.1016/0034-5687(96)00017-5
5. Baker, T. L., and Mitchell, G. S. (2000). Episodic but not continuous hypoxia elicits long-term facilitation of phrenic motor output in rats. J. Physiol. 529, 215-219.doi: 10.1111/j.1469-7793.2000.00215.x
6. Baker-Herman, T. L., Fuller, D. D., Bavis, R. W., Zabka, A. G., Golder, F. J., Doperalski, N. J., et al. (2004). BDNF is necessary and sufficient for spinal respiratory plasticity following intermittent hypoxia. Nat. Neurosci. 7, 48-55.doi: 10.1038/nn1166
7. Baker-Herman, T. L., and Mitchell, G. S. (2002). Phrenic long-term facilitation requires spinal serotonin receptor activation and protein synthesis. J. Neurosci. 22, 6239-6246.
8. Bavis, R. W., and Mitchell, G. S. (2003). Intermittent hypoxia induces phrenic longterm facilitation in carotid-denervated rats. J. Appl. Physiol. (1985) 94, 399-409.doi: 10.1152/japplphysiol.00374.2002
9. Bisgard, G. E. (2000). Carotid body mechanisms in acclimatization to hypoxia. Respir. Physiol. 121, 237-246.doi: 10.1016/s0034-5687(00)00131-6
10. Blitz, D. M., and Ramirez, J. M. (2002). Long-term modulation of respiratory network activity following anoxia in vitro. J. Neurophysiol. 87, 2964-2971.doi: 10.1152/jn.00515.2001
11. Byrne, J. H. (1997). Synapses. Plastic plasticity. Nature 389, 791-792.doi: 10.1038/39746
12. Dale, E. A., Ben Mabrouk, F., and Mitchell, G. S. (2014). Unexpected benefits of intermittent hypoxia: Enhanced respiratory and nonrespiratory motor function. Physiology (Bethesda) 29, 39-48.doi: 10.1152/physiol.00012.2013
13. Dale, E. A., Satriotomo, I., and Mitchell, G. S. (2012). Cervical spinal erythropoietin induces phrenic motor facilitation via extracellular signal-regulated protein kinase and Akt signaling. J. Neurosci. 32, 5973-5983.doi: 10.1523/JNEUROSCI.3873-11.2012
14. Dale-Nagle, E. A., Hoffman, M. S., MacFarlane, P. M., Satriotomo, I., Lovett-Barr, M. R., Vinit, S., et al. (2010). Spinal plasticity following intermittent hypoxia: Implications for spinal injury. Ann. NY Acad. Sci. 1198, 252-259.doi: 10.1111/j.1749-6632.2010.05499.x
15. Dale-Nagle, E. A., Satriotomo, I., and Mitchell, G. S. (2011). Spinal vascular endothelial growth factor induces phrenic motor facilitation via extracellular signal-regulated kinase and Akt signaling. J. Neurosci. 31, 7682-7690.doi: 10.1523/JNEUROSCI.0239-11.2011
16. Devinney, M. J., Huxtable, A. G., Nichols, N. L., and Mitchell, G. S. (2013). Hypoxia-induced phrenic long-term facilitation: Emergent properties. Ann. N YAcad. Sci. 1279, 143-153.doi: 10.1111/nyas.12085
17. Feldman, J. L., Mitchell, G. S., and Nattie, E. E. (2003). Breathing: Rhythmicity, plasticity, chemosensitivity. Annu. Rev. Neurosci. 26, 239-266.doi: 10.1146/annurev.neuro.26.041002.131103
18. Feldman, J. L., Neverova, N. V., and Saywell, S. A. (2005). Modulation of hypoglossal motoneuron excitability by intracellular signal transduction cascades. Respir. Physiol. Neurobiol. 147, 131-143.doi: 10.1016/j.resp.2005.03.014
19. Feldman, J. L., and Smith, J. C. (1989). Cellular mechanisms underlying modulation of breathing pattern in mammals. Ann. N Y Acad. Sci. 563, 114-130.doi: 10.1111/j.1749-6632.1989.tb42194.x
20. Fletcher, E. C., Lesske, J., Behm, R., Miller, C. C. 3rd, Stauss, H., and Unger, T. (1992). Carotid chemoreceptors, systemic blood pressure and chronic episodic hypoxia mimicking sleep apnea. J. Appl. Physiol. (1985) 72, 1978-1984.
21. Forsythe, J. A., Jiang, B. H., Iyer, N. V., Agani, F., Leung, S. W., Koos, R. D., et al. (1996). Activation of vascular endothelial growth factor gene expression by hypoxia-inducible factor 1. Mol. Cell. Biol. 16, 4601-4613.
22. Fuller, D. D., Johnson, S. M., Johnson, R. A., and Mitchell, G. S. (2002). Chronic cervical spinal sensory denervation reveals ineffective spinal pathways to phrenic motoneurons in the rat. Neurosci. Lett. 323, 25-28.doi: 10.1016/s0304-3940(02)00121-0
23. Fuller, D. D., Johnson, S. M., Olson, E. B. Jr., and Mitchell, G. S. (2003). Synaptic pathways to phrenic motoneurons are enhanced bychronic intermittent hypoxia after cervical spinal cord injury. J. Neurosci. 23, 2993-3000.
24. Fuller, D. D., Zabka, A. G., Baker, T. L., and Mitchell, G. S. (2001). Phrenic longterm facilitation requires 5-HT receptor activation during but not following episodic hypoxia. J. Appl. Physiol. (1985) 90, 2001-2006.
25. Golder, F.J., and Mitchell, G. S. (2005). Spinal synaptic enhancement with acute intermittent hypoxia improves respiratory function after chronic cervical spinal cord injury. J. Neurosci. 25, 2925-2932.doi: 10.1523/jneurosci.0148-05.2005
26. Golder, F. J., Ranganathan, L., Satriotomo, I., Hoffman, M., Lovett-Barr, M. R., Watters, J. J., et al. (2008). Spinal adenosine A2a receptor activation elicits long-lasting phrenic motor facilitation. J. Neurosci. 28, 2033-2042.doi: 10.1523/JNEUROSCI.3570-07.2008
27. Golder, F. J., Zabka, A. G., Bavis, R. W., Baker-Herman, T., Fuller, D. D., and Mitchell, G. S. (2005). Differences in time-dependent hypoxia phreinc responses among inbred rat strains. J. Appl. Physiol. (1985) 98, 838-844.doi: 10.1152/japplphysiol.00984.2004
28. Grau, J. W., Huie, J. R., Lee, K. H., Hoy, K. C., Huang, Y. J., Turtle, J. D., et al. (2014). Metaplasticity and behavior: How training and inflammation affect plastic potential within the spinal cord and recovery after injury. Front. Neural Circuits 8:100.doi: 10.3389/fncir.2014.00100
29. Hakim, F., Gozal, D., and Kheirandish-Gozal, L. (2012). Sympathetic and catecholaminergic alterations in sleep apnea with particular emphasis on children. Front. Neurol. 3:7.doi: 10.3389/fneur.2012.00007
30. Hayashi, F., Coles, S. K., Bach, K. B., Mitchell, G. S., and Mccrimmon, D. R. (1993). Time-dependent phrenic nerve responses to carotid afferent activation: Intact vs. decerebellate rats. Am. J. Physiol. 265, R811-R819.
31. Hayes, H.B., Jayaraman, A., Herrmann, M., Mitchell, G. S., Rymer, W. Z., and Trumbower, R. D. (2014). Daily intermittent hypoxia enhances walking after chronic spinal cord injury: A randomized trial. Neurology 82, 104-113.doi: 10.1212/01.wnl.0000437416.34298.43
32. Hoffman, M. S., Golder, F. J., Mahamed, S., and Mitchell, G. S. (2010). Spinal adenosine A2(A) receptor inhibition enhances phrenic long term facilitation following acute intermittent hypoxia. J. Physiol. 588, 255-266.doi: 10.1113/jphysiol.2009.180075
33. Hoffman, M. S., and Mitchell, G. S. (2011). Spinal 5-HT7 receptor activation induces long-lasting phrenic motor facilitation. J. Physiol. 589, 1397-1407.doi: 10.1113/jphysiol.2010.201657
34. Hoffman, M. S., and Mitchell, G. S. (2013). Spinal 5-HT7 receptors and protein kinase A constrain intermittent hypoxia-induced phrenic long-term facilitation. Neuroscience 250, 632-643.doi: 10.1016/j.neuroscience.2013.06.068
35. Hoffman, M. S., Nichols, N. L., Macfarlane, P. M., and Mitchell, G. S. (2012). Phrenic long-term facilitation after acute intermittent hypoxia requires spinal ERK activation but not TrkB synthesis. J. Appl. Physiol. (1985) 113, 1184-1193.doi: 10.1152/japplphysiol.00098.2012
36. Huxtable, A. G., Macfarlane, P. M., Vinit, S., Nichols, N. L., Dale, E. A., and Mitchell, G. S. (2014). Adrenergic alpha1 receptor activation is sufficient, but not necessary for phrenic long-term facilitation. J. Appl. Physiol. (1985) 116, 1345-1352.doi: 10.1152/japplphysiol.00904.2013
37. Huxtable, A. G., Smith, S. M., Vinit, S., Watters, J. J., and Mitchell, G. S. (2013). Systemic LPS induces spinal inflammatory gene expression and impairs phrenic long-term facilitation following acute intermittent hypoxia. J. Appl. Physiol. (1985) 114, 879-887.doi: 10.1152/japplphysiol.01347.2012
38. Jacquin, T., Denavit-Saubie, M., and Champagnat, J. (1989). Substance P and serotonin mutually reverse their excitatory effects in the rat nucleus tractus solitarius. Brain Res. 502, 214-222.doi: 10.1016/0006-8993(89)90616-1
39. Johnson, R. A., Okragly, A. J., Haak-Frendscho, M., and Mitchell, G. S. (2000). Cervical dorsal rhizotomy increases brain-derived neurotrophic factor and neurotrophin-3 expression in the ventral spinal cord. J. Neurosci. 20:RC77.
40. Katz, P.S., and Edwards, D. H. (1999). Beyond Neurotransmission. New York: Oxford University Press.
41. Kinkead, R., Bach, K. B., Johnson, S. M., Hodgeman, B. A., and Mitchell, G. S. (2001). Plasticity in respiratory motor control: Intermittent hypoxia and hypercapnia activate opposing serotonergic and noradrenergic modulatory systems. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 130, 207-218.doi: 10.1016/S1095-6433(01)00393-2
42. Kinkead, R., Zhan, W. Z., Prakash, Y. S., Bach, K. B., Sieck, G. C., and Mitchell, G. S. (1998). 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.
43. Kline, D.D., Hendricks, G., Hermann, G., Rogers, R. C., and Kunze, D. L. (2009). Dopamine inhibits N-type channels in visceral afferents to reduce synaptic transmitter release under normoxic and chronic intermittent hypoxic conditions. J. Neurophysiol. 101, 2270-2278.doi: 10.1152/jn.91304.2008
44. Kline, D. D., Ramirez-Navarro, A., and Kunze, D. L. (2007). Adaptive depression in synaptic transmission in the nucleus of the solitary tract after in vivo chronic intermittent hypoxia: Evidence for homeostatic plasticity. J. Neurosci. 27, 4663-4673.doi: 10.1523/jneurosci.4946-06.2007
45. Kulik, T. B., Aronhime, S. N., Echeverry, G., Beylin, A., and Winn, H. R. (2010). The relationship between oxygen and adenosine in astrocyte cultures. Glia 58, 1335-1344.doi: 10.1002/glia.21011
46. Kumar, P., and Prabhakar, N. R. (2012). Peripheral chemoreceptors: Function and plasticity of the carotid body. Compr. Physiol. 2, 141-219.doi: 10.1002/cphy.c100069
47. Lee, E. J., Woodske, M. E., Zou, B., and O’donnell, C. P. (2009). Dynamic arterial blood gas analysis in conscious, unrestrained C57BL/6J mice during exposure to intermittent hypoxia. J. Appl. Physiol. (1985) 107, 290-294.doi: 10.1152/japplphysiol.91255.2008
48. Li, J., Grigoryev, D. N., Ye, S. Q., Thorne, L., Schwartz, A. R., Smith, P. L., et al. (2005). Chronic intermittent hypoxia upregulates genes of lipid biosynthesis in obese mice. J. Appl. Physiol. (1985) 99, 1643-1648.doi: 10.1152/japplphysiol.00522.2005
49. Li, Z., Morris, K. F., Baekey, D. M., Shannon, R., and Lindsey, B. G. (1999). Multimodal medullary neurons and correlational linkages of the respiratory network. J. Neurophysiol. 82, 188-201.
50. Ling, L., Fuller, D. D., Bach, K. B., Kinkead, R., and Olson, E. B. Jr. (2001). Chronic intermittent hypoxia elicits serotonin-dependent plasticity in the central neural control of breathing. J. Neurosci. 21, 5381-5388.
51. Lovett-Barr, M. R., Satriotomo, I., Muir, G. D., Wilkerson, J. E., Hoffman, M. S., Vinit, S., et al. (2012). Repetitive intermittent hypoxia induces respiratory and somatic motor recovery after chronic cervical spinal injury. J. Neurosci. 32, 3591-3600.doi: 10.1523/jneurosci.2908-11.2012
52. MacFarlane, P. M., and Mitchell, G. S. (2009). Episodic spinal serotonin receptor activation elicits long-lasting phrenic motor facilitation by an NADPH oxidase-dependent mechanism. J. Physiol. 587, 5469-5481.doi: 10.1113/jphysiol.2009.176982
53. MacFarlane, P. M., Vinit, S., and Mitchell, G. S. (2011). Serotonin 2A and 2B receptor-induced phrenic motor facilitation: Differential requirement for spinal NADPH oxidase activity. Neuroscience 178, 45-55.doi: 10.1016/j.neuroscience.2011.01.011
54. MacFarlane, P. M., Vinit, S., and Mitchell, G. S. (2014). Spinal nNOS regulates phrenic motor facilitation by a 5-HT2B receptor and NADPH oxidase dependent mechanism. Neuroscience 269, 67-78.doi: 10.1016/j.neuroscience.2014.03.014
55. MacFarlane, P. M., Vinit, S., Roopra, A., and Mitchell, G. S. (2010). Enhanced phrenic long-term facilitation following repetitive acute intermittent hypoxia: Role of glycolytic flux. FASEB J. 24, 799.15.
56. Mahamed, S., and Mitchell, G. S. (2007). Is there a link between intermittent hypoxia-induced respiratory plasticity and obstructive sleep apnoea? Exp. Physiol. 92, 27-37.doi: 10.1113/expphysiol.2006.033720
57. Malinow, R., and Malenka, R. C. (2002). AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25, 103-126.doi: 10.1146/annurev.neuro.25.112701.142758
58. Manahan-Vaughan, D., Kulla, A., and Frey, J. U. (2000). Requirement oftranslation but not transcription for the maintenance of long-term depression in the CA1 region of freely moving rats. J. Neurosci. 20, 8572-8576.
59. McCrimmon, D. R., Mitchell, G. S., and Dekin, D. K. (1995). Glutamate, GABA and Serotonin in Ventilatory Control. New York: Marcel-Dekker.
60. McGuire, M., Tartar, J. L., Cao, Y., McCarley, R. W., White, D. P., Strecker, R. E., et al. (2008). Sleep fragmentation impairs ventilatory long-term facilitation via adenosine A1 receptors. J. Physiol. 586, 5215-5229.doi: 10.1113/jphysiol.2008.158121
61. McGuire, M., Zhang, Y., White, D. P., and Ling, L. (2003). Chronic intermittent hypoxia enhances ventilatory long-term facilitation in awake rats. J. Appl. Physiol. (1985) 95, 1499-1508.doi: 10.1152/japplphysiol.00044.2003
62. McGuire, M., Zhang, Y., White, D. P., and Ling, L. (2004). 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.doi: 10.1152/ajpregu.00463.2003
63. Mesce, K. A. (2002). Metamodulation of the biogenic amines: Second-order modulation by steroid hormones and amine cocktails. Brain Behav. Evol. 60, 339-349.doi: 10.1159/000067793
64. Mitchell, G.S. (2007). “Respiratory plasticity following intermittent hypoxia: A guide for novel therapeutic approaches to ventilatory control disorders," in Genetic Basis for Respiratory Control Disorders, ed C. Gaultier (New York: Springer Publishing Company), 291-311.
65. Mitchell, G. S., Baker, T. L., Nanda, S. A., Fuller, D. D., Zabka, A. G., Hodgeman, B. A., et al. (2001). Invited review: Intermittent hypoxia and respiratory plasticity. J. Appl. Physiol. (1985) 90, 2466-2475.
66. Mitchell, G. S., Douse, M. A., and Foley, K. T. (1990). Receptor interactions in modulating ventilatory activity. Am. J. Physiol. 259, R911-R920.
67. Mitchell, G.S., and Johnson, S. M. (2003). Neuroplasticity in respiratory motor control. J. Appl. Physiol. (1985) 94, 358-374.doi: 10.1152/japplphysiol.00523.2002
68. Moraes, D.J., Zoccal, D. B., and Machado, B. H. (2012). Medullary respiratory network drive sympathetic overactivity and hypertensions in rats submitted to chronic intermittent hypoxia. Hypertension 60, 1374-1380.doi: 10.1161/HYPERTENSIONAHA.111.189332
69. Morris, K. F., Arata, A., Shannon, R., and Lindsey, B. G. (1996). Long-term facilitation of phrenic nerve activity in cats: Responses and short term scale correlations of medullary neurones. J. Physiol. 490, 463-480.doi: 10.1113?jphysiol.1996.sp021158
70. Navarette-Opazo, A. A., and Mitchell, G. S. (2014). Therapeutic potential of intermittent hypoxia: A matter of dose. Am. J. Physiol. Regul. Integr. Comp. Physiol. 307, R1181-R1197.doi: 10.1152/ajpregu.00208.2014
71. Nichols, N. L., Dale, E. A., and Mitchell, G. S. (2012). Severe acute intermittent hypoxia elicits phrenic long-term facilitation by a novel adenosine-dependent mechanism. J. Appl. Physiol. (1985) 112, 1678-1688.doi: 10.1152/japplphysiol.00060.2012
72. Nichols, N.L., and Mitchell, G. S. (2014). Enhanced phrenic long-term facilitation in rats with motor neuron death from intrapleural CTB-saporin injections. FASEB J. 28, 713.1.
73. Nichols, N. L., Van Dyke, J., Nashold, L., Satriotomo, I., Suzuki, M., and Mitchell, S. (2013). Ventilatory control in ALS. Respir. Physiol. Neurobiol. 189, 429-437.doi: 10.1016/j.resp.2013.05.016
74. Peng, Y. J., and Prabhakar, N. R. (2003). Reactive oxygen species in the plasticity of respiratory behavior elicited by chronic intermittent hypoxia. J. Appl. Physiol. (1985) 94, 2342-2349.doi: 10.1152/japplphysiol.00613.2002
75. Peng, Y. J., and Prabhakar, N. R. (2004). Effect of two paradigms of chronic intermittent hypoxia on carotid body sensory activity. J. Appl. Physiol. (1985) 96, 1236-1242.doi: 10.1152/japplphysiol.00820.2003
76. Philips, G. T., Kopec, A. M., and Carew, T. J. (2013). Pattern and predicitability in memory formation: From molecular mechanisms to clinical relevance. Neurobiol. Learn. Mem. 105, 117-124.doi: 10.1016/j.nlm.2013.05.003
77. Prabhakar, N. R., and Semenza, G. L. (2012). Adaptive and maladaptive cardiorespiratory responses to continuous and intermittent hypoxia mediated by hypoxia-inducible factors 1 and 2. Physiol. Rev. 92, 967-1003.doi: 10.1152/physrev.00030.2011
78. Ramirez, J. M., Doi, A., Garcia, A. J. 3rd, Elsen, F. P., Koch, H., and Wei, A. D. (2012). The cellular building blocks of breathing. Compr. Physiol. 4, 2683-2731.doi: 10.1002/cphy.c110033
79. Reeves, S.R., and Gozal, D. (2006). Respiratory and metabolic responses to early postnatal chronic intermittent hypoxia and sustained hypoxia in the developing rat. Peditr. Res. 60, 680-686.doi: 10.1203/01.pdr.0000246073.95911.18
80. Ribeiro, J. A., and Sebastiao, A. M. (2010). Modulation and metamodulation of synapses by adenosine. Acta Physiol. (Oxf.) 199, 161-169.doi: 10.1111/j.1748-1716.2010.02115.x
81. Row, B. W. (2007). Intermittent hypoxia and cognitive function: Implications from chronic animal models. Adv. Exp. Med. Biol. 618, 51-67.doi: 10.1007/978-0-387-75434-5_5
82. Row, B. W., Kheirandish, L., Cheng, Y., Rowell, P. P., and Gozal, D. (2007). Impaired spatial working memory and altered choline acetyltransferase (CHAT) immunoreactivity and nicotinic receptor binding in rats exposed to intermittent hypoxia during sleep. Behav. Brain Res. 177, 308-314.doi: 10.1016/j.bbr.2006.11.028
83. Sankari, A., Bascom, A., Oomman, S., and Badr, M. S. (2014). Sleep disordered breathing in chronic spinal cord injury. J. Clin. Sleep Med. 10, 65-72.doi: 10.5664/jcsm.3362
84. Satriotomo, I., Dale, E. A., Dahlberg, J. M., and Mitchell, G. S. (2012). Repetitive acute intermittent hypoxia increases expression of proteins associated with plasticity in the phrenic motor nucleus. Exp. Neurol. 237, 103-115.doi: 10.1016/j.expneurol.2012.05.020
85. Satriotomo, I., Nashold, L. J., Svendsen, C. N., and Mitchel, G. S. (2006). Enhancement of BDNF and serotonin terminal density in phreic and hypoglossal motor nuclei in a rat model of amyotrophic lateral sclerosis. FASEB J. 20, A1212.
86. Semenza, G. L., Nejfelt, M. K., Chi, S. M., and Antonarakis, S. E. (1991). Hypoxia-inducible nuclear factors bind to an enhancer element located 3?to the human erythropoietin gene. Proc. Natl. Acad. Sci. USA 88, 5680-5684.doi: 10.1073/pnas.88.13.5680
87. Sherff, C. M., and Carew, T. J. (2002). Coincident induction of long-term facilitation at sensory-motor synapses in Aplysia: Presynaptic and postsynaptic factors. Neurobiol. Learn. Mem. 78, 498-507.doi: 10.1006/nlme.2002.4092
88. Small, A., Nikodemova, M., Doughtery, B., Mitchell, G. S., and Watters, J. J. (2014). Repetitive acute intermittent hypoxia differentially affects CD11b+ cell phenotypes after C2 spinal hemisection. FASEB J. 28, 713.6.
89. Strey, K. A., Baertsch, N. A., and Baker-Herman, T. L. (2013). Inactivity-induced respiratory plasticity: Protecting the drive to breathe in disorders that reduce respiratory neural activity. Respir. Physiol. Neurobiol. 189, 384-394.doi: 10.1016/j.resp.2013.06.023
90. Tasali, E., and Ip, M. S. (2008). Obstructive sleep apnea and metabolic syndrome: Alterations in glucose metabolism and inflammation. Proc. Am. Thorac. Soc. 5, 207-217.doi: 10.1513/pats.200708-139mg
91. Trumbower, R. D., Jayaraman, A., Mitchell, G. S., and Rymer, W. Z. (2012). Exposure to acute intermittent hypoxia augments somatic motor function in humans with incomplete spinal cord injury. Neurorehabil. Neural Repair 26, 163-172.doi: 10.1177/1545968311412055
92. Vinit, S., Lovett-Barr, M. R., and Mitchell, G. S. (2009). Intermittent hypoxia induces functional recovery following cervical spinal injury. Respir. Physiol. Neurobiol. 169, 210-217.doi: 10.1016/j.resp.2009.07.023
93. Vinit, S., Satriotomo, I., Macfarlane, P. M., and Mitchell, G. S. (2010). Enhanced phrenic long-term facilitation following repetitive (pLTF) acute intermittent hypoxia. FASEB J. 799.15.
94. Vinit, S., Windelborn, J. A., and Mitchell, G. S. (2011). Lipopolysaccharide attenuates phrenic long-term facilitation following acute intermittent hypoxia. Respir. Physiol. Neurobiol. 176, 130-135.doi: 10.1016/j.resp.2011.02.008
95. Wiegert, J. S., and Bading, H. (2011). Activity-dependent calcium signaling and ERK-MAP kinases in neurons: A link to structural plasticity of the nucleus and gene transcription regulation. Cell Calcium 49, 296-305.doi: 10.1016/j.ceca.2010.11.009
96. Wilkerson, J. E., and Mitchell, G. S. (2009). Daily intermittent hypoxia augments spinal BDNF levels, ERK phosphorylation and respiratory long-term facilitation. Exp. Neurol. 217, 116-123.doi: 10.1016/j.expneurol.2009.01.017
97. Zabka, A. G., Behan, M., and Mitchell, G. S. (2001). Long term facilitation of respiratory motor output decreases with age in male rats. J. Physiol. 531, 509-514.doi: 10.1111/j.1469-7793.2001.0509i.x
98. Zabka, A. G., Mitchell, G. S., and Behan, M. (2006). Conversion from testosterone to oestradiol is required to modulate respiratory long-term facilitation in male rats. J. Physiol. 576, 903-912.doi: 10.1113/jphysiol.2006.114850
99. Zhang, S. X., Wang, Y., and Gozal, D. (2012). Pathological consequences of intermittent hypoxia in the central nervous system. Compr. Physiol. 2, 1767-1777.doi: 10.1002/cphy.c100060