Spinal respiratory motoneurons and interneurons

Respiratory Physiology and Neurobiology

Volumn 179, Issue 1, 2011, Pages 3-13

  Lane, Michael A ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

Central nervous system; Neural components; Neuroanatomical tracing techniques; Phrenic motor system

Indexed keywords

ABDOMINAL MOTONEURON; BREATHING; BREATHING MUSCLE; CENTRAL NERVOUS SYSTEM DISEASE; HUMAN; IN VITRO STUDY; INTERCOSTAL MUSCLE; INTERNEURON; MORPHOLOGICAL TRAIT; MOTONEURON; MOTOR SYSTEM; NERVOUS SYSTEM INJURY; NEUROANATOMY; NEUROPATHOLOGY; NONHUMAN; PHRENIC NERVE; PRIORITY JOURNAL; RESPIRATORY FAILURE; RESPIRATORY FUNCTION; RESPIRATORY NERVE CELL; REVIEW; SPINAL CORD INJURY; SPINAL CORD MOTONEURON; SPINAL RESPIRATORY INTERNEURON; SUPRASPINAL RESPIRATORY MOTONEURON;

ANIMALS; HUMANS; INTERNEURONS; MOTOR NEURONS; NEURAL PATHWAYS; RESPIRATORY MECHANICS; RESPIRATORY MUSCLES; SPINAL CORD;

EID: 80053251196     PISSN: 15699048     EISSN: 18781519     Source Type: Journal    
DOI: 10.1016/j.resp.2011.07.004     Document Type: Review

References (192)

1. Aboussouan L.S., Lewis R.A., Shy M.E. Disorders of pulmonary function, sleep, and the upper airway in Charcot-Marie-Tooth disease. Lung 2007, 185:1-7.
2. Alheid G.F., McCrimmon D.R. The chemical neuroanatomy of breathing. Respir. Physiol. Neurobiol. 2008, 164:3-11.
3. Alilain W.J., Horn K.P., Hu H., Dick T.E., Silver J. Functional regeneration of respiratory pathways after spinal cord injury. Nature 2011, 475:196-200.
4. Alilain W.J., Li X., Horn K.P., Dhingra R., Dick T.E., Herlitze S., Silver J. Light-induced rescue of breathing after spinal cord injury. J. Neurosci. 2008, 28:11862-11870.
5. Aminoff M.J., Sears T.A. Spinal integration of segmental, cortical and breathing inputs to thoracic respiratory motoneurones. J. Physiol. 1971, 215:557-575.
6. Anker A.R., Sadacca B.F., Yates B.J. Vestibular inputs to propriospinal interneurons in the feline C1-C2 spinal cord projecting to the C5-C6 ventral horn. Exp. Brain Res. 2006, 170:39-51.
7. Aoki M., Mori S., Kawahara K., Watanabe H., Ebata N. Generation of spontaneous respiratory rhythm in high spinal cats. Brain Res. 1980, 202:51-63.
8. Bareyre F.M., Kerschensteiner M., Raineteau O., Mettenleiter T.C., Weinmann O., Schwab M.E. The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats. Nat. Neurosci. 2004, 7:269-277.
9. Barker A.J., Ullian E.M. Astrocytes and synaptic plasticity. Neuroscientist 2010, 16:40-50.
10. Baussart B., Stamegna J.C., Polentes J., Tadie M., Gauthier P. A new model of upper cervical spinal contusion inducing a persistent unilateral diaphragmatic deficit in the adult rat. Neurobiol. Dis. 2006, 22:562-574.
11. Bellingham M.C. Synaptic inhibition of cat phrenic motoneurons by internal intercostal nerve stimulation. J. Neurophysiol. 1999, 82:1224-1232.
12. Bellingham M.C., Lipski J. Respiratory interneurons in the C5 segment of the spinal cord of the cat. Brain Res. 1990, 533:141-146.
13. Ben Achour S., Pascual O. Glia: the many ways to modulate synaptic plasticity. Neurochem. Int. 2010, 57:440-445.
14. Berger A.J. Dorsal respiratory group neurons in the medulla of cat: spinal projections, responses to lung inflation and superior laryngeal nerve stimulation. Brain Res. 1977, 135:231-254.
15. Berger A.J., Cameron W.E., Averill D.B., Kramis R.C., Binder M.D. Spatial distributions of phrenic and medial gastrocnemius motoneurons in the cat spinal cord. Exp. Neurol. 1984, 86:559-575.
16. Billig I., Foris J.M., Card J.P., Yates B.J. Transneuronal tracing of neural pathways controlling an abdominal muscle, rectus abdominis, in the ferret. Brain Res. 1999, 820:31-44.
17. Billig I., Foris J.M., Enquist L.W., Card J.P., Yates B.J. Definition of neuronal circuitry controlling the activity of phrenic and abdominal motoneurons in the ferret using recombinant strains of pseudorabies virus. J. Neurosci. 2000, 20:7446-7454.
18. Billig I., Hartge K., Card J.P., Yates B.J. Transneuronal tracing of neural pathways controlling abdominal musculature in the ferret. Brain Res. 2001, 912:24-32.
19. Bolser D.C., Jefferson S.C., Rose M.J., Tester N.J., Reier P.J., Fuller D.D., Davenport P.W., Howland D.R. Recovery of airway protective behaviors after spinal cord injury. Respir. Physiol. Neurobiol. 2009, 169:150-156.
20. Boulenguez P., Gestreau C., Vinit S., Stamegna J.C., Kastner A., Gauthier P. Specific and artifactual labeling in the rat spinal cord and medulla after injection of monosynaptic retrograde tracers into the diaphragm. Neurosci. Lett. 2007, 417:206-211.
21. Butler J.E. Drive to the human respiratory muscles. Respir. Physiol. Neurobiol. 2007, 159:115-126.
22. Cameron W.E., Averill D.B., Berger A.J. Quantitative analysis of the dendrites of cat phrenic motoneurons stained intracellularly with horseradish peroxidase. J. Comp. Neurol. 1985, 231:91-101.
23. Card J.P., Enquist L.W. Transneuronal circuit analysis with pseudorabies viruses. Current Protocols in Neuroscience/Editorial Board 1999, 1.5.1-1.5.28. J.N. Crawley (Ed.).
24. Chandler M.J., Zhang J., Foreman R.D. Phrenic nerve inputs to upper cervical (C1-C3) spinothalamic tract neurons in monkeys. Brain Res. 1998, 798:93-100.
25. Choi H., Liao W.-L., Newton K.M., Onario R.C., King A.M., Desilets F.C., Woodard E.J., Eichler M.E., Frontera W.R., Sabharwal S., Teng Y.D. Respiratory abnormalities resulting from midcervical spinal cord injury and their reversal by serotonin 1A agonists in conscious rats. J. Neurosci. 2005, 25:4550-4559.
26. Cleland C.L., Getting P.A. Respiratory-modulated and phrenic afferent-driven neurons in the cervical spinal cord (C4-C6) of the fluorocarbon-perfused guinea pig. Exp. Brain Res. 1993, 93:307-311.
27. Coglianese C.J., Peiss C.N., Wurster R.D. Rhythmic phrenic nerve activity and respiratory activity in spinal dogs. Respir. Physiol. 1977, 29:247-254.
28. Courtine G., Gerasimenko Y., van den Brand R., Yew A., Musienko P., Zhong H., Song B., Ao Y., Ichiyama R.M., Lavrov I., Roy R.R., Sofroniew M.V., Edgerton V.R. Transformation of nonfunctional spinal circuits into functional states after the loss of brain input. Nat. Neurosci. 2009, 12:1333-1342.
29. Courtine G., Song B., Roy R.R., Zhong H., Herrmann J.E., Ao Y., Qi J., Edgerton V.R., Sofroniew M.V. Recovery of supraspinal control of stepping via indirect propriospinal relay connections after spinal cord injury. Nat. Med. 2008, 14:69-74.
30. Davies J.G., Kirkwood P.A., Sears T.A. The detection of monosynaptic connexions from inspiratory bulbospinal neurones to inspiratory motoneurones in the cat. J. Physiol. 1985, 368:33-62.
31. Davies J.G., Kirkwood P.A., Sears T.A. The distribution of monosynaptic connexions from inspiratory bulbospinal neurones to inspiratory motoneurones in the cat. J. Physiol. 1985, 368:63-87.
32. Dawkins M.A., Foreman R.D., Farber J.P. Short latency excitation of upper cervical respiratory neurons by vagal stimulation in the rat. Brain Res. 1992, 594:319-322.
33. de Castro D., Lipski J., Kanjhan R. Electrophysiological study of dorsal respiratory neurons in the medulla oblongata of the rat. Brain Res. 1994, 639:49-56.
34. De Troyer A., Kirkwood P.A., Wilson T.A. Respiratory action of the intercostal muscles. Physiol. Rev. 2005, 85:717-756.
35. Decherchi P., Gauthier P. Regeneration of acutely and chronically injured descending respiratory pathways within post-traumatic nerve grafts. Neuroscience 2002, 112:141-152.
36. Dekker J.J., Lawrence D.G., Kuypers H.G. The location of longitudinally running dendrites in the ventral horn of the cat spinal cord. Brain Res. 1973, 51:319-325.
37. Del Negro C.A., Morgado-Valle C., Feldman J.L. Respiratory rhythm: an emergent network property?. Neuron 2002, 34:821-830.
38. DeRuisseau L.R., Fuller D.D., Qiu K., DeRuisseau K.C., Donnelly W.H., Mah C., Reier P.J., Byrne B.J. Neural deficits contribute to respiratory insufficiency in Pompe disease. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:9419-9424.
39. DeVries K.L., Goshgarian H.G. Spinal cord localization and characterization of the neurons which give rise to the accessory phrenic nerve in the adult rat. Exp. Neurol. 1989, 104:88-90.
40. Dobbins E.G., Feldman J.L. Brainstem network controlling descending drive to phrenic motoneurons in rat. J. Comp. Neurol. 1994, 347:64-86.
41. Douse M.A., Duffin J. Axonal projections and synaptic connections of C5 segment expiratory interneurones in the cat. J. Physiol. 1993, 470:431-444.
42. Douse M.A., Duffin J., Brooks D., Fedorko L. Role of upper cervical inspiratory neurons studied by cross-correlation in the cat. Exp. Brain Res. 1992, 90:153-162.
43. Downman C.B. Skeletal muscle reflexes of splanchnic and intercostal nerve origin in acute spinal and decerebrate cats. J. Neurophysiol. 1955, 18:217-235.
44. Duffin J., Douse M.A., van Alphen J. Excitation of upper cervical inspiratory neurones by vagal stimulation in the cat. Neuroreport 1994, 5:1133-1136.
45. Duffin J., Hung S. Respiratory rhythm generation. Can. Anaesth. Soc. J. 1985, 32:124-137.
46. Duffin J., Lipski J. Monosynaptic excitation of thoracic motoneurones by inspiratory neurones of the nucleus tractus solitarius in the cat. J. Physiol. 1987, 390:415-431.
47. Eccles R.M., Sears T.A., Shealy C.N. Intracellular recording from respiratory motoneurones of the thoracic spinal cord of the cat. Nature 1962, 193:844-846.
48. El-Bohy A.A., Schrimsher G.W., Reier P.J., Goshgarian H.G. Quantitative assessment of respiratory function following contusion injury of the cervical spinal cord. Exp. Neurol. 1998, 150:143-152.
49. Ellenberger H.H., Feldman J.L. Monosynaptic transmission of respiratory drive to phrenic motoneurons from brainstem bulbospinal neurons in rats. J. Comp. Neurol. 1988, 269:47-57.
50. Ellenberger H.H., Feldman J.L., Goshgarian H.G. Ventral respiratory group projections to phrenic motoneurons: electron microscopic evidence for monosynaptic connections. J. Comp. Neurol. 1990, 302:707-714.
51. Ellenberger H.H., Vera P.L., Haselton J.R., Haselton C.L., Schneiderman N. Brainstem projections to the phrenic nucleus: an anterograde and retrograde HRP study in the rabbit. Brain Res. Bull. 1990, 24:163-174.
52. 2 chemosensitivity and respiratory control. J. Appl. Physiol. 2010, 108:1803-1811.
53. Erlichman J.S., Leiter J.C., Gourine A.V. ATP, glia and central respiratory control. Respir. Physiol. Neurobiol. 2010, 173:305-311.
54. Eugenin J., Nicholls J.G., Cohen L.B., Muller K.J. Optical recording from respiratory pattern generator of fetal mouse brainstem reveals a distributed network. Neuroscience 2006, 137:1221-1227.
55. Ezure K., Manabe M., Yamada H. Distribution of medullary respiratory neurons in the rat. Brain Res. 1988, 455:262-270.
56. Ezure K., Tanaka I. Distribution and medullary projection of respiratory neurons in the dorsolateral pons of the rat. Neuroscience 2006, 141:1011-1023.
57. Fedorko, L., 1982. Localization of the respiratory motoneurone pools in the cat's thoracic spinal cord. J. Physiol. 332(Suppl): 28P.
58. Fedorko L., Hoskin R.W., Duffin J. Projections from inspiratory neurons of the nucleus retroambigualis to phrenic motoneurons in the cat. Exp. Neurol. 1989, 105:306-310.
59. Fedorko L., Merrill E.G., Lipski J. Two descending medullary inspiratory pathways to phrenic motoneurones. Neurosci. Lett. 1983, 43:285-291.
60. Feldman J.L. Neurophysiology of breathing in mammals. Handbook of Physiology - The Nervous System 1986, vol. IV. pp. 463-524.
61. Feldman J.L., Del Negro C.A. Looking for inspiration: new perspectives on respiratory rhythm. Nat. Rev. Neurosci. 2006, 7:232-242.
62. Feldman J.L., Mitchell G.S., Nattie E.E. Breathing: rhythmicity, plasticity, chemosensitivity. Annu. Rev. Neurosci. 2003, 26:239-266.
63. Flourens M. Nouveaux détails sur le noeud vital. Comp. Rend. Acad. Sci. 1858, 47:803-806.
64. Fuller D.D., Bavis R.W., Mitchell G.S. Respiratory neuroplasticity: respiratory gases, development, and spinal injury. Pharmacology and Pathophysiology of the Control of Breathing 2005, 155-223. Taylor & Francis, Boca Raton. D.S. Ward, A. Dahan, L. Teppema (Eds.).
65. Fuller D.D., Doperalski N.J., Dougherty B.J., Sandhu M.S., Bolser D.C., Reier P.J. Modest spontaneous recovery of ventilation following chronic high cervical hemisection in rats. Exp. Neurol. 2008, 211:97-106.
66. Fuller D.D., Sandhu M.S., Doperalski N.J., Lane M.A., White T.E., Bishop M.D., Reier P.J. Graded unilateral cervical spinal cord injury and respiratory motor recovery. Respir. Physiol. Neurobiol. 2009, 165:245-253.
67. Furley D.J., Wilkie J.S. Galen on Respiration and the Arteries 1984, Princeton University Press, Princeton, NJ.
68. Gaytan S.P., Pasaro R., Coulon P., Bevengut M., Hilaire G. Identification of central nervous system neurons innervating the respiratory muscles of the mouse: a transneuronal tracing study. Brain Res. Bull. 2002, 57:335-339.
69. Geser F., Brandmeir N.J., Kwong L.K., Martinez-Lage M., Elman L., McCluskey L., Xie S.X., Lee V.M., Trojanowski J.Q. Evidence of multisystem disorder in whole-brain map of pathological TDP-43 in amyotrophic lateral sclerosis. Arch. Neurol. 2008, 65:636-641.
70. Gilchrist J.M. Overview of neuromuscular disorders affecting respiratory function. Semin. Respir. Crit Care Med. 2002, 23:191-200.
71. Golder F.J., Fuller D.D., Lovett-Barr M.R., Vinit S., Resnick D.K., Mitchell G.S. Breathing patterns after mid-cervical spinal contusion in rats. Exp. Neurol. 2011.
72. Golder F.J., Reier P.J., Bolser D.C. Altered respiratory motor drive after spinal cord injury: supraspinal and bilateral effects of a unilateral lesion. J. Neurosci. 2001, 21:8680-8689.
73. Gordon P.H., Cheng B., Katz I.B., Mitsumoto H., Rowland L.P. Clinical features that distinguish PLS, upper motor neuron-dominant ALS, and typical ALS. Neurology 2009, 72:1948-1952.
74. Goridis C., Dubreuil V., Thoby-Brisson M., Fortin G., Brunet J.F. Phox2b, congenital central hypoventilation syndrome and the control of respiration. Semin. Cell Dev. Biol. 2010, 21:814-822.
75. Goshgarian H.G. The crossed phrenic phenomenon: a model for plasticity in the respiratory pathways following spinal cord injury. J. Appl. Physiol. 2003, 94:795-810.
76. Goshgarian H.G. The crossed phrenic phenomenon and recovery of function following spinal cord injury. Respir. Physiol. Neurobiol. 2009.
77. Goshgarian H.G., Ellenberger H.H., Feldman J.L. Decussation of bulbospinal respiratory axons at the level of the phrenic nuclei in adult rats: a possible substrate for the crossed phrenic phenomenon. Exp. Neurol. 1991, 111:135-139.
78. Goshgarian H.G., Ellenberger H.H., Feldman J.L. Bulbospinal respiratory neurons are a source of double synapses onto phrenic motoneurons following cervical spinal cord hemisection in adult rats. Brain Res. 1993, 600:169-173.
79. Goshgarian H.G., Rafols J.A. The phrenic nucleus of the albino rat: a correlative HRP and Golgi study. J. Comp. Neurol. 1981, 201:441-456.
80. Goshgarian H.G., Rafols J.A. The ultrastructure and synaptic architecture of phrenic motor neurons in the spinal cord of the adult rat. J. Neurocytol. 1984, 13:85-109.
81. Goshgarian H.G., Roubal P.J. Origin and distribution of phrenic primary afferent nerve fibers in the spinal cord of the adult rat. Exp. Neurol. 1986, 92:624-638.
82. Goshgarian H.G., Yu X.J., Rafols J.A. Neuronal and glial changes in the rat phrenic nucleus occurring within hours after spinal cord injury. J. Comp. Neurol. 1989, 284:519-533.
83. Gosselink R., Kovacs L., Decramer M. Respiratory muscle involvement in multiple sclerosis. Eur. Respir. J. 1999, 13:449-454.
84. Gottschall J. The diaphragm of the rat and its innervation. Muscle fiber composition; perikarya and axons of efferent and afferent neurons. Anat. Embryol. (Berl.) 1981, 161:405-417.
85. Gould D.J., Goshgarian H.G. Glial changes in the phrenic nucleus following superimposed cervical spinal cord hemisection and peripheral chronic phrenicotomy injuries in adult rats. Exp. Neurol. 1997, 148:1-9.
86. Grelot L., Milano S., Portillo F., Miller A.D. Respiratory interneurons of the lower cervical (C4-C5) cord: membrane potential changes during fictive coughing, vomiting, and swallowing in the decerebrate cat. Pflugers Arch. 1993, 425:313-320.
87. Guth L. Functional plasticity in the respiratory pathway of the mammalian spinal cord. Exp. Neurol. 1976, 51:414-420.
88. Hadjikoutis S., Wiles C.M. Respiratory complications related to bulbar dysfunction in motor neuron disease. Acta Neurol. Scand. 2001, 103:207-213.
89. Hadley S.D., Goshgarian H.G. Altered immunoreactivity for glial fibrillary acidic protein in astrocytes within 1h after cervical spinal cord injury. Exp. Neurol. 1997, 146:380-387.
90. Hadley S.D., Walker P.D., Goshgarian H.G. Effects of serotonin inhibition on neuronal and astrocyte plasticity in the phrenic nucleus 4h following C2 spinal cord hemisection. Exp. Neurol. 1999, 160:433-445.
91. Hayashi F., Hinrichsen C.F., McCrimmon D.R. Short-term plasticity of descending synaptic input to phrenic motoneurons in rats. J. Appl. Physiol. 2003, 94:1421-1430.
92. Hilaire G., Bou C., Monteau R. Rostral ventrolateral medulla and respiratory rhythmogenesis in mice. Neurosci. Lett. 1997, 224:13-16.
93. Hilaire G., Monteau R. Connections between inspiratory medullary neurons and phrenic or intercostal motoneurones. J. Physiol. (Paris) 1976, 72:987-1000. (Author's transl.).
94. Hilaire G., Monteau R. Brainstem and spinal control of respiratory muscles during breathing. Neural Control of the Respiratory Muscles 1997, 91-105. CRC, New York. A.D. Miller, A.L. Bianchi, B.P. Bishop (Eds.).
95. Holstege G., van Neerven J., Evertse F. Spinal cord location of the motoneurons innervating the abdominal, cutaneous maximus, latissimus dorsi and longissimus dorsi muscles in the cat. Exp. Brain Res. 1987, 67:179-194.
96. Hoskin R., Duffin J. Excitation of upper cervical inspiratory neurons by inspiratory neurons of the nucleus tractus solitarius in the cat. Exp. Neurol. 1987, 95:126-141.
97. Hoskin R.W., Fedorko L.M., Duffin J. Projections from upper cervical inspiratory neurons to thoracic and lumbar expiratory motor nuclei in the cat. Exp. Neurol. 1988, 99:544-555.
98. Iizuka M. Respiration-related control of abdominal motoneurons. Respir. Physiol. Neurobiol. 2010.
99. Iizuka M. Respiration-related control of abdominal motoneurons. Respir. Physiol. Neurobiol. 2011.
100. Imhotep, 2650BC. Edwin Smith Egyptian Papyrus.
101. Iscoe S. Control of abdominal muscles. Prog. Neurobiol. 1998, 56:433-506.
102. Iscoe S. Segmental responses of abdominal motoneurons in decerebrate cats. Respir. Physiol. 2000, 122:27-34.
103. Iscoe S., Duffin J. Effects of stimulation of phrenic afferents on cervical respiratory interneurones and phrenic motoneurones in cats. J. Physiol. 1996, 497(Pt 3):803-812.
104. Jefferson S.C., Tester N.J., Rose M., Blum A.E., Howland B.G., Bolser D.C., Howland D.R. Cough following low thoracic hemisection in the cat. Exp. Neurol. 2010, 222:165-170.
105. Johnson S.M., Getting P.A. Phrenic motor nucleus of the guinea pig: dendrites are bundled without clustering of cell somas. Exp. Neurol. 1988, 101:208-220.
106. Kajana S., Goshgarian H.G. Administration of phosphodiesterase inhibitors and an adenosine A1 receptor antagonist induces phrenic nerve recovery in high cervical spinal cord injured rats. Exp. Neurol. 2008, 210:671-680.
107. Keswani N.H., Hollinshead W.H. Localization of the phrenic nucleus in the spinal cord of man. Anat. Rec. 1956, 125:683-699.
108. Kirkwood P.A., Munson J.B., Sears T.A., Westgaard R.H. Respiratory interneurones in the thoracic spinal cord of the cat. J. Physiol. 1988, 395:161-192.
109. Kirkwood P.A., Schmid K., Sears T.A. Functional identities of thoracic respiratory interneurones in the cat. J. Physiol. 1993, 461:667-687.
110. Kuzuhara S., Chou S.M. Localization of the phrenic nucleus in the rat: a HRP study. Neurosci. Lett. 1980, 16:119-124.
111. Lane M.A., Fuller D.D., White T.E., Reier P.J. Respiratory neuroplasticity and cervical spinal cord injury: translational perspectives. Trends Neurosci. 2008, 31:538-547.
112. Lane M.A., Lee K.Z., Fuller D.D., Reier P.J. Spinal circuitry and respiratory recovery following spinal cord injury. Respir. Physiol. Neurobiol. 2009, 169:123-132.
113. Lane M.A., Salazar K., Vavrousek J.C., Mercier L.M., O'Steen B.E., Fuller D.D., Reier P.J. Plasticity in the phrenic motor system following cervical contusion in adult rat spinal cord. Neurorehabil. Neural Repair 2009, 23:974.
114. Lane M.A., White T.E., Coutts M.A., Jones A.L., Sandhu M.S., Bloom D.C., Bolser D.C., Yates B.J., Fuller D.D., Reier P.J. Cervical prephrenic interneurons in the normal and lesioned spinal cord of the adult rat. J. Comp. Neurol. 2008, 511:692-709.
115. Larnicol N., Rose D., Marlot D., Duron B. Spinal localization of the intercostal motoneurones innervating the upper thoracic spaces. Neurosci. Lett. 1982, 31:13-18.
116. Laskowski M.B., Sanes J.R. Topographic mapping of motor pools onto skeletal muscles. J. Neurosci. 1987, 7:252-260.
117. Le Forestier N., Maisonobe T., Piquard A., Rivaud S., Crevier-Buchman L., Salachas F., Pradat P.F., Lacomblez L., Meininger V. Does primary lateral sclerosis exist? A study of 20 patients and a review of the literature. Brain 2001, 124:1989-1999.
118. Lee K.Z., Qiu K., Sandhu M.S., Elmallah M.K., Falk D.J., Lane M.A., Reier P.J., Byrne B.J., Fuller D.D. Hypoglossal neuropathology and respiratory activity in pompe mice. Front. Physiol. 2011, 2:31.
119. Liou W.W., Goshgarian H.G. The superimposed effects of chronic phrenicotomy and cervical spinal cord hemisection on glial cytoarchitecture in the rat phrenic nucleus. J. Spinal Cord Med. 1996, 19:58-70.
120. Lipski J. Is there electrical coupling between phrenic motoneurons in cats. Neurosci. Lett. 1984, 46:229-234.
121. Lipski J., Duffin J. An electrophysiological investigation of propriospinal inspiratory neurons in the upper cervical cord of the cat. Exp. Brain Res. 1986, 61:625-637.
122. Lipski J., Duffin J., Kruszewska B., Zhang X. Upper cervical inspiratory neurons in the rat: an electrophysiological and morphological study. Exp. Brain Res. 1993, 95:477-487.
123. Lipski J., Martin-Body R.L. Morphological properties of respiratory intercostal motoneurons in cats as revealed by intracellular injection of horseradish peroxidase. J. Comp. Neurol. 1987, 260:423-434.
124. Lipski J., Zhang X., Kruszewska B., Kanjhan R. Morphological study of long axonal projections of ventral medullary inspiratory neurons in the rat. Brain Res. 1994, 640:171-184.
125. Lois J.H., Rice C.D., Yates B.J. Neural circuits controlling diaphragm function in the cat revealed by transneuronal tracing. J. Appl. Physiol. 2009, 106:138-152.
126. Lu F., Qin C., Foreman R.D., Farber J.P. Chemical activation of C1-C2 spinal neurons modulates intercostal and phrenic nerve activity in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2004, 286:R1069-R1076.
127. Lyall R.A., Donaldson N., Polkey M.I., Leigh P.N., Moxham J. Respiratory muscle strength and ventilatory failure in amyotrophic lateral sclerosis. Brain 2001, 124:2000-2013.
128. Mantilla C.B., Zhan W.Z., Sieck G.C. Retrograde labeling of phrenic motoneurons by intrapleural injection. J. Neurosci. Methods 2009, 182:244-249.
129. Mateika J.H., Duffin J. The connections from botzinger expiratory neurons to upper cervical inspiratory neurons in the cat. Exp. Neurol. 1989, 104:138-146.
130. McCrimmon D.R., Monnier A., Hayashi F., Zuperku E.J. Pattern formation and rhythm generation in the ventral respiratory group. Clin. Exp. Pharmacol. Physiol. 2000, 27:126-131.
131. Mehta S. Neuromuscular disease causing acute respiratory failure. Respir. Care 2006, 51:1016-1021. (discussion 1021-1013).
132. Mellins R.B., Balfour H.H., Turino G.M., Winters R.W. Failure of automatic control of ventilation (Ondine's curse), Report of an infant born with this syndrome and review of the literature. Medicine (Baltimore). 1970, 49:487-504.
133. Merrill E.G., Lipski J. Inputs to intercostal motoneurons from ventrolateral medullary respiratory neurons in the cat. J. Neurophysiol. 1987, 57:1837-1853.
134. Miller A.D. Localization of motoneurons innervating individual abdominal muscles of the cat. J. Comp. Neurol. 1987, 256:600-606.
135. Mironov S.L., Skorova E., Hartelt N., Mironova L.A., Hasan M.T., Kugler S. Remodelling of the respiratory network in a mouse model of Rett syndrome depends on brain-derived neurotrophic factor regulated slow calcium buffering. J. Physiol. 2009, 587:2473-2485.
136. Mitchell R.A., Berger A.J. Neural regulation of respiration. Am. Rev. Respir. Dis. 1975, 111:206-224.
137. Monteau R., Hilaire G. Spinal respiratory motoneurons. Prog. Neurobiol. 1991, 37:83-144.
138. Moreno D.E., Yu X.J., Goshgarian H.G. Identification of the axon pathways which mediate functional recovery of a paralyzed hemidiaphragm following spinal cord hemisection in the adult rat. Exp. Neurol. 1992, 116:219-228.
139. Nakazono Y., Aoki M. Excitatory connections between upper cervical inspiratory neurons and phrenic motoneurons in cats. J. Appl. Physiol. 1994, 77:679-683.
140. Nantwi K.D., El-Bohy A.A., Schrimsher G.W., Reier P.J., Goshgarian H. Spontaneous functional recovery in a paralyzed hemidiaphragm following upper cervical spinal cord injury in adult rats. Neurorehab. Neural Repair 1999, 13:225-234.
141. Nicholls J.G., Paton J.F. Brainstem: neural networks vital for life. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2009, 364:2447-2451.
142. Nonaka S., Miller A.D. Behavior of upper cervical inspiratory propriospinal neurons during fictive vomiting. J. Neurophysiol. 1991, 65:1492-1500.
143. NSCISC Spinal Cord Injury Facts and Figures at a Glance 2011, National Spinal Cord Injury Statistical Center, Birmingham, Alabama. https://www.nscisc.uab.edu/.
144. Oku Y., Okabe A., Hayakawa T., Okada Y. Respiratory neuron group in the high cervical spinal cord discovered by optical imaging. Neuroreport 2008, 19:1739-1743.
145. Palisses R., Persegol L., Viala D. Evidence for respiratory interneurones in the C3-C5 cervical spinal cord in the decorticate rabbit. Exp. Brain Res. 1989, 78:624-632.
146. Palisses R., Viala D. Existence of respiratory interneurons in the cervical spinal cord of the rabbit. Comptes Rendus l'Acad. Sci. 1987, 305:321-324.
147. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 1998, Academic Press, San Diego.
148. Polentes J., Stamegna J.C., Nieto-Sampedro M., Gauthier P. Phrenic rehabilitation and diaphragm recovery after cervical injury and transplantation of olfactory ensheathing cells. Neurobiol. Dis. 2004, 16:638-653.
149. Porter W.T. The path of the respiratory impulse from the bulb to the phrenic nuclei. J. Physiol. 1895, 17:455-485.
150. Prakash Y.S., Mantilla C.B., Zhan W.Z., Smithson K.G., Sieck G.C. Phrenic motoneuron morphology during rapid diaphragm muscle growth. J. Appl. Physiol. 2000, 89:563-572.
151. Qin C., Chandler M.J., Foreman R.D., Farber J.P. Upper thoracic respiratory interneurons integrate noxious somatic and visceral information in rats. J. Neurophysiol. 2002, 88:2215-2223.
152. Qin C., Farber J.P., Chandler M.J., Foreman R.D. Chemical activation of C(1)-C(2) spinal neurons modulates activity of thoracic respiratory interneurons in rats. Am J. Physiol. Regul. Integr. Comp. Physiol. 2002, 283:R843-R852.
153. Qiu K., Lane M.A., Lee K.Z., Reier P.J., Fuller D.D. The phrenic motor nucleus in the adult mouse. Exp. Neurol. 2010, 226:254-258.
154. Ramirez J.M., Richter D.W. The neuronal mechanisms of respiratory rhythm generation. Curr. Opin. Neurobiol. 1996, 6:817-825.
155. Ramirez J.M., Schwarzacher S.W., Pierrefiche O., Olivera B.M., Richter D.W. Selective lesioning of the cat pre-Botzinger complex in vivo eliminates breathing but not gasping. J. Physiol. 1998, 507(Pt 3):895-907.
156. Rekling J.C., Feldman J.L. PreBotzinger complex and pacemaker neurons: hypothesized site and kernel for respiratory rhythm generation. Annu. Rev. Physiol. 1998, 60:385-405.
157. Richter D.W. Generation and maintenance of the respiratory rhythm. J. Exp. Biol. 1982, 100:93-107.
158. Rikard-Bell G.C., Bystrzycka E.K. Localization of phrenic motor nucleus in the cat and rabbit studied with horseradish peroxidase. Brain Res. 1980, 194:479-483.
159. Rikard-Bell G.C., Bystrzycka E.K., Nail B.S. Brainstem projections to the phrenic nucleus: a HRP study in the cat. Brain Res. Bull. 1984, 12:469-477.
160. Rikard-Bell G.C., Bystrzycka E.K., Nail B.S. The identification of brainstem neurones projecting to thoracic respiratory motoneurones in the cat as demonstrated by retrograde transport of HRP. Brain Res. Bull. 1985, 14:25-37.
161. Rochester D.F. Respiratory muscles and ventilatory failure: 1993 perspective. Am. J. Med. Sci. 1993, 305:394-402.
162. Rosenbaum H., Renshaw B. Descending respiratory pathways in the cervical spinal cord. Am. J. Physiol. 1949, 157:468-476.
163. Routal R.V., Pal G.P. Location of the phrenic nucleus in the human spinal cord. J. Anat. 1999, 195(Pt 4):617-621.
164. Saether K., Hilaire G., Monteau R. Dorsal and ventral respiratory groups of neurons in the medulla of the rat. Brain Res. 1987, 419:87-96.
165. Samuel E.P., Warwick R. The origin of the phrenic nerve in the Rhesus monkey. J. Comp. Neurol. 1955, 102:557-563.
166. Sandhu M.S., Dougherty B.J., Lane M.A., Bolser D.C., Kirkwood P.A., Reier P.J., Fuller D.D. Respiratory recovery following high cervical hemisection. Respir. Physiol. Neurobiol. 2009, 169:94-101.
167. Schriever S., Jurgens U. Location of respiratory motoneurons involved in phonation. An HRP study in the squirrel monkey. J. Hirnforsch. 1989, 30:521-527.
168. Sidman R.L., Taksir T., Fidler J., Zhao M., Dodge J.C., Passini M.A., Raben N., Thurberg B.L., Cheng S.H., Shihabuddin L.S. Temporal neuropathologic and behavioral phenotype of 6neo/6neo Pompe disease mice. J. Neuropathol. Exp. Neurol. 2008, 67:803-818.
169. Smith J.C., Ellenberger H.H., Ballanyi K., Richter D.W., Feldman J.L. Pre-Botzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science 1991, 254:726-729.
170. Sperry M.A., Goshgarian H.G. Ultrastructural changes in the rat phrenic nucleus developing within 2h after cervical spinal cord hemisection. Exp. Neurol. 1993, 120:233-244.
171. St John W.M. Noeud vital for breathing in the brainstem: gasping - yes, eupnoea - doubtful. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2009, 364:2625-2633.
172. Sumi T. Organization of spinal respiratory neurons. Ann. N. Y. Acad. Sci. 1963, 109:561-570.
173. Sun Q.J., Goodchild A.K., Chalmers J.P., Pilowsky P.M. The pre-Botzinger complex and phase-spanning neurons in the adult rat. Brain Res. 1998, 809:204-213.
174. Takahashi K., Ninomiya T. Observations on the fine structure of the phrenic nucleus in the cervical spinal cord of the cat with special reference to its dendritic bundles. J. Anat. 1985, 140(Pt 3):491-498.
175. Takahashi K., Satomi H., Ise H., Yamamoto T. Identification of the phrenic nucleus in the cat as studied by horseradish peroxidase bathing of the transected intrathoracal phrenic nerve. Anat. Anz. 1980, 148:49-54.
176. Taneja P., Ogier M., Brooks-Harris G., Schmid D.A., Katz D.M., Nelson S.B. Pathophysiology of locus ceruleus neurons in a mouse model of Rett syndrome. J. Neurosci. 2009, 29:12187-12195.
177. Tani M., Kida M.Y., Akita K. Relationship between the arrangement of motoneuron pools in the ventral horn and ramification pattern of the spinal nerve innervating trunk muscles in the cat (Felis domestica). Exp. Neurol. 1994, 128:290-300.
178. Tekgul H., Serdaroglu G., Tutuncuoglu S. Outcome of axonal and demyelinating forms of Guillain-Barre syndrome in children. Pediatr. Neurol. 2003, 28:295-299.
179. Teng Y.T., Su W.J., Hou J.W., Huang S.F. Infantile-onset glycogen storage disease type II (Pompe disease): report of a case with genetic diagnosis and pathological findings. Chang Gung Med. J. 2004, 27:379-384.
180. Tian G.F., Duffin J. Connections from upper cervical inspiratory neurons to phrenic and intercostal motoneurons studied with cross-correlation in the decerebrate rat. Exp. Brain Res. 1996, 110:196-204.
181. Ullah M. Localization of the phrenic nucleus in the spinal cord of the rabbit. J. Anat. 1978, 125:377-386.
182. Vinit S., Darlot F., Stamegna J.C., Sanchez P., Gauthier P., Kastner A. Long-term reorganization of respiratory pathways after partial cervical spinal cord injury. Eur. J. Neurosci. 2008, 27:897-908.
183. Vinit S., Kastner A. Descending bulbospinal pathways and recovery of respiratory motor function following SCI. Respir. Physiol. Neurobiol. 2009.
184. Vinit S., Lovett-Barr M.R., Mitchell G.S. Intermittent hypoxia induces functional recovery following cervical spinal injury. Respir. Physiol. Neurobiol. 2009, 169:210-217.
185. Warwick R., Mitchell G.A. The phrenic nucleus of the macaque. J. Comp. Neurol. 1956, 105:553-585.
186. Webber C.L., Pleschka K. Structural and functional characteristics of individual phrenic motoneurons. Pflugers Arch. 1976, 364:113-121.
187. Webber C.L., Wurster R.D., Chung J.M. Cat phrenic nucleus architecture as revealed by horseradish peroxidase mapping. Exp. Brain Res. 1979, 35:395-406.
188. Yamada H., Ezure K., Manabe M. Efferent projections of inspiratory neurons of the ventral respiratory group. A dual labeling study in the rat. Brain Res. 1988, 455:283-294.
189. Yates B.J., Smail J.A., Stocker S.D., Card J.P. Transneuronal tracing of neural pathways controlling activity of diaphragm motoneurons in the ferret. Neuroscience 1999, 90:1501-1513.
190. Zhou S.-Y., Castro-Moure F., Goshgarian H.G. Activation of a latent respiratory motor pathway by stimulation of neurons in the medullary chemoreceptor area of the rat. Exp. Neurol. 2001, 171:176-184.
191. Zimmer M.B., Nantwi K., Goshgarian H.G. Effect of spinal cord injury on the respiratory system: basic research and current clinical treatment options. J. Spinal Cord Med. 2007, 30:319-330.
192. Zimmer M.B., Nantwi K., Goshgarian H.G. Effect of spinal cord injury on the neural regulation of respiratory function. Exp. Neurol. 2008, 209:399-406.