Influence of vagal afferents on supraspinal and spinal respiratory activity following cervical spinal cord injury in rats

Journal of Applied Physiology

Volumn 109, Issue 2, 2010, Pages 377-387

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

^a UNIVERSITY OF FLORIDA   (United States)

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

Author keywords

Crossed phrenic phenomenon; Hypoglossal nerve; Plasticity; Positive end expired pressure; Vagotomy

Indexed keywords

ANIMAL; BLOOD PRESSURE; BREATHING; BREATHING MECHANICS; CERVICAL SPINE; DISEASE MODEL; HEART RATE; HYPOGLOSSAL NERVE; INNERVATION; LUNG; MALE; NERVE CELL INHIBITION; PATHOLOGY; PATHOPHYSIOLOGY; PHRENIC NERVE; POSITIVE END EXPIRATORY PRESSURE; RAT; SENSORY NERVE CELL; SPINAL CORD INJURY; SPRAGUE DAWLEY RAT; SURGERY; TIME; VAGOTOMY; VAGUS NERVE;

ANIMALS; BLOOD PRESSURE; CERVICAL VERTEBRAE; DISEASE MODELS, ANIMAL; HEART RATE; HYPOGLOSSAL NERVE; LUNG; MALE; NEURAL INHIBITION; NEURONS, AFFERENT; PHRENIC NERVE; POSITIVE-PRESSURE RESPIRATION; RATS; RATS, SPRAGUE-DAWLEY; RESPIRATION; RESPIRATORY MECHANICS; SPINAL CORD INJURIES; TIME FACTORS; VAGOTOMY; VAGUS NERVE;

EID: 77955641548     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.01429.2009     Document Type: Article

References (59)

1. Alilain WJ, Goshgarian HG. Glutamate receptor plasticity and activityregulated cytoskeletal associated protein regulation in the phrenic motor nucleus may mediate spontaneous recovery of the hemidiaphragm following chronic cervical spinal cord injury. Exp Neurol 212: 348-357, 2008.
2. Bae H, Nantwi KD, Goshgarian H. Effects of carotid body excision on recovery of respiratory function in C2 hemisected adult rats. Exp Neurol 195: 140-147, 2005.
3. Bailey EF, Fregosi RF. Modulation of upper airway muscle activities by bronchopulmonary afferents. J Appl Physiol 101: 609-617, 2006.
4. Bonham AC, Chen CY, Sekizawa S, Joad JP. Plasticity in the nucleus tractus solitarius and its influence on lung and airway reflexes. J Appl Physiol 101: 322-327, 2006.
5. Boulenguez P, Gauthier P, Kastner A. Respiratory neuron subpopulations and pathways potentially involved in the reactivation of phrenic motoneurons after C2 hemisection. Brain Res 1148: 96-104, 2007.
6. Brown R, DiMarco AF, Hoit JD, Garshick E. Respiratory dysfunction and management in spinal cord injury. Respir Care 51: 853-868, 2006.
7. Chatfield PO, Mead S. The role of the vagi in the crossed phrenic phenomenon. Fed Proc 7: 20, 1948.
8. Cherniack NS, von Euler C, Glogowska M, Homma I. Characteristics and rate of occurrence of spontaneous and provoked augmented breaths. Acta Physiol Scand 111: 349-360, 1981.
9. Coleridge HM, Coleridge JCG. Reflexes evoked from tracheobronchial tree and lungs. In: Handbook of Physiology. The Respiratory System. Control of Breathing. Bethesda, MD: Am. Physiol. Soc., 1986, sect. 3, vol. II, p. 395-429.
10. Doperalski NJ, Fuller DD. Long-term facilitation of ipsilateral but not contralateral phrenic output after cervical spinal cord hemisection. Exp Neurol 200: 74-81, 2006.
11. Doperalski NJ, Sandhu MS, Bavis RW, Reier PJ, Fuller DD. Ventilation and phrenic output following high cervical spinal hemisection in male vs. female rats. Respir Physiol Neurobiol 162: 160-167, 2008.
12. El-Bohy AA, Goshgarian HG. The use of single phrenic axon recordings to assess diaphragm recovery after cervical spinal cord injury. Exp Neurol 156: 172-179, 1999.
13. Ezure K, Tanaka I, Saito Y. Activity of brainstem respiratory neurones just before the expiration-inspiration transition in the rat. J Physiol 547: 629-640, 2003.
14. Fuller DD, Doperalski NJ, Dougherty BJ, Sandhu MS, Bolser DC, Reier PJ. Modest spontaneous recovery of ventilation following chronic high cervical hemisection in rats. Exp Neurol 211: 97-106, 2008.
15. Fuller DD, Johnson SM, Johnson RA, Mitchell GS. Chronic cervical spinal sensory denervation reveals ineffective spinal pathways to phrenic motoneurons in the rat. Neurosci Lett 323: 25-28, 2002.
16. 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.
17. Golder FJ, Davenport PW, Johnson RD, Reier PJ, Bolser DC. Augmented breath phase volume and timing relationships in the anesthetized rat. Neurosci Lett 373: 89-93, 2005.
18. Golder FJ, Fuller DD, Davenport PW, Johnson RD, Reier PJ, Bolser DC. Respiratory motor recovery after unilateral spinal cord injury: eliminating crossed phrenic activity decreases tidal volume and increases contralateral respiratory motor output. J Neurosci 23: 2494-2501, 2003.
19. Golder FJ, Mitchell GS. Spinal synaptic enhancement with acute intermittent hypoxia improves respiratory function after chronic cervical spinal cord injury. J Neurosci 25: 2925-2932, 2005.
20. Golder FJ, Reier PJ, Bolser DC. Altered respiratory motor drive after spinal cord injury: supraspinal and bilateral effects of a unilateral lesion. J Neurosci 21: 8680-8689, 2001.
21. Golder FJ, Reier PJ, Davenport PW, Bolser DC. Cervical spinal cord injury alters the pattern of breathing in anesthetized rats. J Appl Physiol 91: 2451-2458, 2001.
22. Goshgarian HG. The crossed phrenic phenomenon and recovery of function following spinal cord injury. Respir Physiol Neurobiol 169: 85-93, 2009.
23. Goshgarian HG. The crossed phrenic phenomenon: a model for plasticity in the respiratory pathways following spinal cord injury. J Appl Physiol 94: 795-810, 2003.
24. Goshgarian HG. The role of cervical afferent nerve fiber inhibition of the crossed phrenic phenomenon. Exp Neurol 72: 211-225, 1981.
25. Goshgarian HG, Moran MF, Prcevski P. Effect of cervical spinal cord hemisection and hemidiaphragm paralysis on arterial blood gases, pH, and respiratory rate in the adult rat. Exp Neurol 93: 440-445, 1986.
26. Hwang JC, St John WM, Bartlett D, Jr. Influence of pulmonary inflations on discharge patterns of phrenic motoneurons. J Appl Physiol 63: 1421-1427, 1987.
27. James E, Nantwi KD. Involvement of peripheral adenosine A2 receptors in adenosine A1 receptor-mediated recovery of respiratory motor function after upper cervical spinal cord hemisection. J Spinal Cord Med 29: 57-66, 2006.
28. Janssen PL, Fregosi RF. No evidence for long-term facilitation after episodic hypoxia in spontaneously breathing, anesthetized rats. J Appl Physiol 89: 1345-1351, 2000.
29. Kline DD. Plasticity in glutamatergic NTS neurotransmission. Respir Physiol Neurobiol 164: 105-111, 2008.
30. Kong FJ, Berger AJ. Firing properties and hypercapnic responses of single phrenic motor axons in the rat. J Appl Physiol 61: 1999-2004, 1986.
31. Kubin L, Alheid GF, Zuperku EJ, McCrimmon DR. Central pathways of pulmonary and lower airway vagal afferents. J Appl Physiol 101: 618-627, 2006.
32. Lane MA, Fuller DD, White TE, Reier PJ. Respiratory neuroplasticity and cervical spinal cord injury: translational perspectives. Trends Neurosci 31: 538-547, 2008.
33. Lane MA, White TE, Coutts MA, Jones AL, Sandhu MS, Bloom DC, Bolser DC, Yates BJ, Fuller DD, Reier PJ. Cervical prephrenic interneurons in the normal and lesioned spinal cord of the adult rat. J Comp Neurol 511: 692-709, 2008.
34. Lee KZ, Fuller DD. Preinspiratory and inspiratory hypoglossal motor output during hypoxia-induced plasticity in the rat. J Appl Physiol 108: 1187-1198, 2010.
35. Lee KZ, Fuller DD, Lu IJ, Ku LC, Hwang JC. Pulmonary C-fiber receptor activation abolishes uncoupled facial nerve activity from phrenic bursting during positive end-expired pressure in the rat. J Appl Physiol 104: 119-129, 2008.
36. Lee KZ, Fuller DD, Lu IJ, Lin JT, Hwang JC. Neural drive to tongue protrudor and retractor muscles following pulmonary C-fiber activation. J Appl Physiol 102: 434-444, 2007.
37. Lee KZ, Fuller DD, Tung LC, Lu IJ, Ku LC, Hwang JC. Uncoupling of upper airway motor activity from phrenic bursting by positive endexpired pressure in the rat. J Appl Physiol 102: 878-889, 2007.
38. Lee KZ, Reier PJ, Fuller DD. Phrenic motoneuron discharge patterns during hypoxia-induced short-term potentiation in rats. J Neurophysiol 102: 2184-2193, 2009.
39. Lewis LJ, Brookhart JM. Significance of the crossed phrenic phenomenon. Am J Physiol 166: 241-254, 1951.
40. Ma A, Bravo M, Kappagoda CT. Responses of bronchial C-fiber afferents of the rabbit to changes in lung compliance. Respir Physiol Neurobiol 138: 155-163, 2003.
41. Mantilla CB, Sieck GC. Neuromuscular adaptations to respiratory muscle inactivity. Respir Physiol Neurobiol 169: 133-140, 2009.
42. Miyata H, Zhan WZ, Prakash YS, Sieck GC. Myoneural interactions affect diaphragm muscle adaptations to inactivity. J Appl Physiol 79: 1640-1649, 1995.
43. Nantwi KD, El-Bohy A, Schrimsher GW, Reier PJ, Goshgarian HG. Spontaneous functional recovery in a paralyzed hemidiaphragm following upper cervical spinal cord injury in adult rats. Neurorehabil Neural Repair 13: 225-234, 1999.
44. Rosenblueth A, Ortiz T. The crossed respiratory impulses to the phrenic. Am J Physiol 117: 495-513, 1936.
45. Rowley KL, Mantilla CB, Sieck GC. Respiratory muscle plasticity. Respir Physiol Neurobiol 147: 235-251, 2005.
46. Saito Y, Ezure K, Tanaka I. Difference between hypoglossal and phrenic activities during lung inflation and swallowing in the rat. J Physiol 544: 183-193, 2002.
47. Sandhu MS, Dougherty BJ, Lane MA, Bolser DC, Kirkwood PA, Reier PJ, Fuller DD. Respiratory recovery following high cervical hemisection. Respir Physiol Neurobiol 169: 94-101, 2009.
48. Schelegle ES, Green JF. An overview of the anatomy and physiology of slowly adapting pulmonary stretch receptors. Respir Physiol 125: 17-31, 2001.
49. Schilero GJ, Spungen AM, Bauman WA, Radulovic M, Lesser M. Pulmonary function and spinal cord injury. Respir Physiol Neurobiol 166: 129-141, 2009.
50. Schreihofer AM, Stornetta RL, Guyenet PG. Evidence for glycinergic respiratory neurons: Botzinger neurons express mRNA for glycinergic transporter 2. J Comp Neurol 407: 583-597, 1999.
51. Sperry MA, Goshgarian HG. Ultrastructural changes in the rat phrenic nucleus developing within 2 h after cervical spinal cord hemisection. Exp Neurol 120: 233-244, 1993.
52. St John WM, Bartlett D, Jr. Comparison of phrenic motoneuron responses to hypercapnia and isocapnic hypoxia. J Appl Physiol 46: 1096- 1102, 1979.
53. Stornetta RL, Sevigny CP, Guyenet PG. Inspiratory augmenting bulbospinal neurons express both glutamatergic and enkephalinergic phenotypes. J Comp Neurol 455: 113-124, 2003.
54. Vinit S, Gauthier P, Stamegna JC, Kastner A. High cervical lateral spinal cord injury results in long-term ipsilateral hemidiaphragm paralysis. J Neurotrauma 23: 1137-1146, 2006.
55. Vinit S, Lovett-Barr MR, Mitchell GS. Intermittent hypoxia induces functional recovery following cervical spinal injury. Respir Physiol Neurobiol 169: 210-217, 2009.
56. Yu J, Pisarri TE, Coleridge JC, Coleridge HM. Response of slowly adapting pulmonary stretch receptors to reduced lung compliance. J Appl Physiol 71: 425-431, 1991.
57. Zhou SY, Goshgarian HG. 5-Hydroxytryptophan-induced respiratory recovery after cervical spinal cord hemisection in rats. J Appl Physiol 89: 1528-1536, 2000.
58. Zimmer MB, Goshgarian HG. Spinal cord injury in neonates alters respiratory motor output via supraspinal mechanisms. Exp Neurol 206: 137-145, 2007.
59. Zimmer MB, Nantwi K, Goshgarian HG. Effect of spinal cord injury on the neural regulation of respiratory function. Exp Neurol 209: 399-406, 2008.