Phrenic motoneuron discharge patterns following chronic cervical spinal cord injury

Experimental Neurology

Volumn 249, Issue , 2013, Pages 20-32

  Lee, Kun Ze ^a,b   Dougherty, Brendan J ^b,c   Sandhu, Milapjit S ^b   Lane, Michael A ^c   Reier, Paul J ^c   Fuller, David D ^b  

^a NATIONAL SUN YAT SEN UNIVERSITY   (Taiwan)

^b UNIVERSITY OF FLORIDA   (United States)

^c UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Motoneuron; Phrenic; Spinal cord injury

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APNEA; ARTICLE; CELLULAR DISTRIBUTION; CERVICAL SPINAL CORD INJURY; CONTROLLED STUDY; END TIDAL CARBON DIOXIDE TENSION; HYPOCAPNIA; INSPIRATORY CAPACITY; MALE; MOTONEURON; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL PLASTICITY; NONHUMAN; PHRENIC MOTONEURON; PHRENIC NERVE; PRIORITY JOURNAL; RAT;

C2 SPINAL CORD HEMISECTION; C2HX; EARLY-I; EARLY-INSPIRATORY; END-TIDAL CO(2) PARTIAL PRESSURE; EXPIRATORY DURATION; INSPIRATORY DURATION; LATE-I; LATE-INSPIRATORY; MOTONEURON; P(ET)CO(2); PERSISTENT INWARD CURRENTS; PHMNS; PHRENIC; PHRENIC MOTONEURONS; PICS; SCI; SPINAL CORD INJURY; T(E); T(I);

ACTION POTENTIALS; ANIMALS; CERVICAL VERTEBRAE; CHRONIC DISEASE; MALE; PHRENIC NERVE; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; RESPIRATORY MECHANICS; SPINAL CORD INJURIES;

EID: 84883365371     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2013.08.003     Document Type: Article

References (70)

1. Alilain W.J., Goshgarian H.G. Glutamate receptor plasticity and activity-regulated cytoskeletal associated protein regulation in the phrenic motor nucleus may mediate spontaneous recovery of the hemidiaphragm following chronic cervical spinal cord injury. Exp. Neurol. 2008, 212:348-357.
2. 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.
3. 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.
4. Basura G.J., Zhou S.Y., Walker P.D., Goshgarian H.G. Distribution of serotonin 2A and 2C receptor mRNA expression in the cervical ventral horn and phrenic motoneurons following spinal cord hemisection. Exp. Neurol. 2001, 169:255-263.
5. Bellingham M.C. Synaptic inhibition of cat phrenic motoneurons by internal intercostal nerve stimulation. J. Neurophysiol. 1999, 82:1224-1232.
6. Bellingham M.C., Lipski J. Respiratory interneurons in the C5 segment of the spinal cord of the cat. Brain Res. 1990, 533:141-146.
7. Berger A.J. Phrenic motoneurons in the cat: subpopulations and nature of respiratory drive potentials. J. Neurophysiol. 1979, 42:76-90.
8. Costa T., Herz A. Antagonists with negative intrinsic activity at delta opioid receptors coupled to GTP-binding proteins. Proc. Natl. Acad. Sci. U. S. A. 1989, 86:7321-7325.
9. 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.
10. 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.
11. Dick T.E., Kong F.J., Berger A.J. Correlation of recruitment order with axonal conduction velocity for supraspinally driven diaphragmatic motor units. J. Neurophysiol. 1987, 57:245-259.
12. Dimitrijevic M.R. Motor control in human spinal cord injury. Spinal Cord Monitoring 1998, 409-420. Springer, New York. E. Stalberg, H.S. Sharma, Y. Olsson (Eds.).
13. Dougherty B.J., Lee K.Z., Lane M.A., Reier P.J., Fuller D.D. Contribution of the spontaneous crossed-phrenic phenomenon to inspiratory tidal volume in spontaneously breathing rats. J. Appl. Physiol. 2012, 112:96-105.
14. Duffin J., Iscoe S. The possible role of C5 segment inspiratory interneurons investigated by cross-correlation with phrenic motoneurons in decerebrate cats. Exp. Brain Res. 1996, 112:35-40.
15. Edgerton V.R., Leon R.D., Harkema S.J., Hodgson J.A., London N., Reinkensmeyer D.J., Roy R.R., Talmadge R.J., Tillakaratne N.J., Timoszyk W., Tobin A. Retraining the injured spinal cord. J. Physiol. 2001, 533:15-22.
16. El-Bohy A.A., Goshgarian H.G. The use of single phrenic axon recordings to assess diaphragm recovery after cervical spinal cord injury. Exp. Neurol. 1999, 156:172-179.
17. 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.
18. 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.
19. Enriquez Denton M., Wienecke J., Zhang M., Hultborn H., Kirkwood P.A. Voltage-dependent amplification of synaptic inputs in respiratory motoneurones. J. Physiol. 2012, 590:3067-3090.
20. Flynn J.R., Graham B.A., Galea M.P., Callister R.J. The role of propriospinal interneurons in recovery from spinal cord injury. Neuropharmacology 2011, 60:809-822.
21. Fuller D.D., Baker-Herman T.L., Golder F.J., Doperalski N.J., Watters J.J., Mitchell G.S. Cervical spinal cord injury upregulates ventral spinal 5-HT2A receptors. J. Neurotrauma 2005, 22:203-213.
22. 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.
23. Fuller D.D., Johnson S.M., Olson E.B., Mitchell G.S. Synaptic pathways to phrenic motoneurons are enhanced by chronic intermittent hypoxia after cervical spinal cord injury. J. Neurosci. 2003, 23:2993-3000.
24. 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.
25. Golder F.J., Mitchell G.S. Spinal synaptic enhancement with acute intermittent hypoxia improves respiratory function after chronic cervical spinal cord injury. J. Neurosci. 2005, 25:2925-2932.
26. 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.
27. Goshgarian H.G. The role of cervical afferent nerve fiber inhibition of the crossed phrenic phenomenon. Exp. Neurol. 1981, 72:211-225.
28. 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.
29. Goshgarian H.G. The crossed phrenic phenomenon and recovery of function following spinal cord injury. Respir. Physiol. Neurobiol. 2009, 169:85-93.
30. 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.
31. Harkema S.J. Plasticity of interneuronal networks of the functionally isolated human spinal cord. Brain Res. Rev. 2008, 57:255-264.
32. 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.
33. Henneman E. Relation between size of neurons and their susceptibility to discharge. Science 1957, 126:1345-1347.
34. Henneman E., Somjen G., Carpenter D.O. Functional significance of cell size in spinal motoneurons. J. Neurophysiol. 1965, 28:560-580.
35. Kong F.J., Berger A.J. Firing properties and hypercapnic responses of single phrenic motor axons in the rat. J. Appl. Physiol. 1986, 61:1999-2004.
36. Lane M.A. Spinal respiratory motoneurons and interneurons. Respir. Physiol. Neurobiol. 2011, 179:3-13.
37. 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.
38. 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.
39. Lane M.A., Lee K.Z., Salazar K., O'Steen B.E., Bloom D.C., Fuller D.D., Reier P.J. Respiratory function following bilateral mid-cervical contusion injury in the adult rat. Exp. Neurol. 2012, 235:197-210.
40. 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.
41. Lee K.Z., Fuller D.D. Neural control of phrenic motoneuron discharge. Respir. Physiol. Neurobiol. 2011, 179:71-79.
42. Lee K.Z., Reier P.J., Fuller D.D. Phrenic motoneuron discharge patterns during hypoxia-induced short-term potentiation in rats. J. Neurophysiol. 2009, 102:2184-2193.
43. Lee K.Z., Sandhu M.S., Dougherty B.J., Reier P.J., Fuller D.D. Influence of vagal afferents on supraspinal and spinal respiratory activity following cervical spinal cord injury in rats. J. Appl. Physiol. 2010, 109:377-387.
44. Li Y., Gorassini M.A., Bennett D.J. Role of persistent sodium and calcium currents in motoneuron firing and spasticity in chronic spinal rats. J. Neurophysiol. 2004, 91:767-783.
45. 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.
46. Mantilla C.B., Bailey J.P., Zhan W.Z., Sieck G.C. Phrenic motoneuron expression of serotonergic and glutamatergic receptors following upper cervical spinal cord injury. Exp. Neurol. 2012, 234:191-199.
47. Mantilla C.B., Sieck G.C. Invited review: mechanisms underlying motor unit plasticity in the respiratory system. J. Appl. Physiol. 2003, 94:1230-1241.
48. Mantilla C.B., Sieck G.C. Neuromuscular adaptations to respiratory muscle inactivity. Respir. Physiol. Neurobiol. 2009, 169:133-140.
49. Mantilla C.B., Sieck G.C. Phrenic motor unit recruitment during ventilatory and non-ventilatory behaviors. Respir. Physiol. Neurobiol. 2011, 179:57-63.
50. Monteau R., Khatib M., Hilaire G. Central determination of recruitment order: intracellular study of phrenic motoneurons. Neurosci. Lett. 1985, 56:341-346.
51. Murray K.C., Nakae A., Stephens M.J., Rank M., D'Amico J., Harvey P.J., Li X., Harris R.L., Ballou E.W., Anelli R., Heckman C.J., Mashimo T., Vavrek R., Sanelli L., Gorassini M.A., Bennett D.J., Fouad K. Recovery of motoneuron and locomotor function after spinal cord injury depends on constitutive activity in 5-HT2C receptors. Nat. Med. 2010, 16:694-700.
52. Murray K.C., Stephens M.J., Ballou E.W., Heckman C.J., Bennett D.J. Motoneuron excitability and muscle spasms are regulated by 5-HT2B and 5-HT2C receptor activity. J Neurophysiol 2011, 105:731-748.
53. Olson E.B., Bohne C.J., Dwinell M.R., Podolsky A., Vidruk E.H., Fuller D.D., Powell F.L., Mitchel G.S. Ventilatory long-term facilitation in unanesthetized rats. J. Appl. Physiol. 2001, 91:709-716.
54. Rowley K.L., Mantilla C.B., Sieck G.C. Respiratory muscle plasticity. Respir. Physiol. Neurobiol. 2005, 147:235-251.
55. 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.
56. Sieck G.C., Mantilla C.B. Role of neurotrophins in recovery of phrenic motor function following spinal cord injury. Respir. Physiol. Neurobiol. 2009, 169:218-225.
57. 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.
58. St John W.M., Bartlett D. Comparison of phrenic motoneuron responses to hypercapnia and isocapnic hypoxia. J. Appl. Physiol. 1979, 46:1096-1102.
59. St John W.M., Bartlett D. Comparison of phrenic motoneuron activity during eupnea and gasping. J. Appl. Physiol. 1981, 50:994-998.
60. St John W.M., Bartlett D. Comparison of phrenic motoneuron activity in eupnea and apneusis. Respir. Physiol. 1985, 60:347-355.
61. Stornetta R.L., Sevigny C.P., Guyenet P.G. Inspiratory augmenting bulbospinal neurons express both glutamatergic and enkephalinergic phenotypes. J. Comp. Neurol. 2003, 455:113-124.
62. Sukiasyan N., Hultborn H., Zhang M. Distribution of calcium channel Ca(V)1.3 immunoreactivity in the rat spinal cord and brain stem. Neuroscience 2009, 159:217-235.
63. Tai Q., Palazzolo K., Mautes A., Nacimiento W., Kuhtz-Buschbeck J.P., Nacimiento A.C., Goshgarian H.G. Ultrastructural characteristics of glutamatergic and GABAergic terminals in cat lamina IX before and after spinal cord injury. J. Spinal Cord Med. 1997, 20:311-318.
64. Tai Q., Palazzolo K.L., Goshgarian H.G. Synaptic plasticity of 5-hydroxytryptamine-immunoreactive terminals in the phrenic nucleus following spinal cord injury: a quantitative electron microscopic analysis. J. Comp. Neurol. 1997, 386:613-624.
65. Tian G.F., Peever J.H., Duffin J. Synaptic connections to phrenic motoneurons in the decerebrate rat. Adv. Exp. Med. Biol. 1998, 450:51-59.
66. Vinit S., Stamegna J.C., Boulenguez P., Gauthier P., Kastner A. Restorative respiratory pathways after partial cervical spinal cord injury: role of ipsilateral phrenic afferents. Eur. J. Neurosci. 2007, 25:3551-3560.
67. Webber C.L., Pleschka K. Structural and functional characteristics of individual phrenic motoneurons. Pflugers Arch. 1976, 364:113-121.
68. Zhang M., Moller M., Broman J., Sukiasyan N., Wienecke J., Hultborn H. Expression of calcium channel CaV1.3 in cat spinal cord: light and electron microscopic immunohistochemical study. J. Comp. Neurol. 2008, 507:1109-1127.
69. Zimmer M.B., Goshgarian H.G. Spinal cord injury in neonates alters respiratory motor output via supraspinal mechanisms. Exp. Neurol. 2007, 206:137-145.
70. 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.