Phrenic motoneuron expression of serotonergic and glutamatergic receptors following upper cervical spinal cord injury

Experimental Neurology

Volumn 234, Issue 1, 2012, Pages 191-199

  Mantilla, Carlos B ^a,b   Bailey, Jeffrey P ^a   Zhan, Wen Zhi ^a   Sieck, Gary C ^a,b  

^a MAYO GRADUATE SCHOOL   (United States)

^b MAYO CLINIC   (United States)

Author keywords

5 HTR2a; AMPA; Laser capture microdissection; Motor neuron; Neuroplasticity; Neurotransmitter; NMDA; Quantitative real time RT PCR; Spinal hemisection

Indexed keywords

AMPA RECEPTOR; GLUTAMATE RECEPTOR; MESSENGER RNA; METABOTROPIC RECEPTOR 1; METABOTROPIC RECEPTOR 5; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; SEROTONIN 1B RECEPTOR; SEROTONIN 2A RECEPTOR; SEROTONIN 2C RECEPTOR; SEROTONIN RECEPTOR;

ADULT ANIMAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CERVICAL SPINAL CORD INJURY; CONTROLLED STUDY; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHRENIC MOTONEURON; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPINAL CORD MOTONEURON;

ANIMALS; CERVICAL VERTEBRAE; CHOLERA TOXIN; DIAPHRAGM; DISEASE MODELS, ANIMAL; ELECTROMYOGRAPHY; FUNCTIONAL LATERALITY; GENE EXPRESSION REGULATION; MALE; MOTOR NEURONS; PHRENIC NERVE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GLUTAMATE; RECEPTORS, SEROTONIN; RNA, MESSENGER; SPINAL CORD INJURIES; STATISTICS AS TOPIC; TIME FACTORS;

EID: 84857506591     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2011.12.036     Document Type: Article

References (49)

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. 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.
3. Canton H., Emeson R.B., Barker E.L., Backstrom J.R., Lu J.T., Chang M.S., Sanders-Bush E. Identification, molecular cloning, and distribution of a short variant of the 5-hydroxytryptamine2C receptor produced by alternative splicing. Mol. Pharmacol. 1996, 50:799-807.
4. Chitravanshi V.C., Sapru H.N. NMDA as well as non-NMDA receptors mediate the neurotransmission of inspiratory drive to phrenic motoneurons in the adult rat. Brain Res. 1996, 715:104-112.
5. DeVivo M.J., Ivie C.S. Life expectancy of ventilator-dependent persons with spinal cord injuries. Chest 1995, 108:226-232.
6. DeVivo M.J., Black K.J., Stover S.L. Causes of death during the first 12 years after spinal cord injury. Arch. Phys. Med. Rehabil. 1993, 74:248-254.
7. Di Pasquale E., Lindsay A., Feldman J., Monteau R., Hilaire G. Serotonergic inhibition of phrenic motoneuron activity: an in vitro study in neonatal rat. Neurosci. Lett. 1997, 230:29-32.
8. Dong X.W., Feldman J.L. Distinct subtypes of metabotropic glutamate receptors mediate differential actions on excitability of spinal respiratory motoneurons. J. Neurosci. 1999, 19:5173-5184.
9. Dow D.E., Mantilla C.B., Zhan W.Z., Sieck G.C. EMG-based detection of inspiration in the rat diaphragm muscle. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2006, 1:1204-1207.
10. Dow D.E., Zhan W.Z., Sieck G.C., Mantilla C.B. Correlation of respiratory activity of contralateral diaphragm muscles for evaluation of recovery following hemiparesis. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2009, 1:404-407.
11. Fuller D.D., Bach K.B., Baker T.L., Kinkead R., Mitchell G.S. Long term facilitation of phrenic motor output. Respir. Physiol. 2000, 121:135-146.
12. Fuller D.D., Zabka A.G., Baker T.L., Mitchell G.S. Phrenic long-term facilitation requires 5-HT receptor activation during but not following episodic hypoxia. J. Appl. Physiol. 2001, 90:2001-2006.
13. 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.
14. Fuller D.D., Golder F.J., Olson E.B., Mitchell G.S. Recovery of phrenic activity and ventilation after cervical spinal hemisection in rats. J. Appl. Physiol. 2006, 100:800-806.
15. 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.
16. Golder F.J., Fuller D.D., Davenport P.W., Johnson R.D., Reier P.J., Bolser D.C. Respiratory motor recovery after unilateral spinal cord injury: eliminating crossed phrenic activity decreases tidal volume and increases contralateral respiratory motor output. J. Neurosci. 2003, 23:2494-2501.
17. Goshgarian H.G. The role of cervical afferent nerve fiber inhibition of the crossed phrenic phenomenon. Exp. Neurol. 1981, 72:211-225.
18. Greer J.J., Smith J.C., Feldman J.L. Role of excitatory amino acids in the generation and transmission of respiratory drive in neonatal rat. J. Physiol. 1991, 437:727-749.
19. Hadley S.D., Walker P.D., Goshgarian H.G. Effects of serotonin inhibition on neuronal and astrocyte plasticity in the phrenic nucleus 4 h following C2 spinal cord hemisection. Exp. Neurol. 1999, 160:433-445.
20. Kinkead R., Zhan W.Z., Prakash Y.S., Bach K.B., Sieck G.C., Mitchell G.S. Cervical dorsal rhizotomy enhances serotonergic innervation of phrenic motoneurons and serotonin-dependent long-term facilitation of respiratory motor output in rats. J. Neurosci. 1998, 18:8436-8443.
21. Liu G., Feldman J.L., Smith J.C. Excitatory amino acid-mediated transmission of inspiratory drive to phrenic motoneurons. J. Neurophysiol. 1990, 64:423-436.
22. Mantilla C.B., Sieck G.C. Neuromuscular adaptations to respiratory muscle inactivity. Respir. Physiol. Neurobiol. 2009, 169:133-140.
23. Mantilla C.B., Rowley K.L., Zhan W.Z., Fahim M.A., Sieck G.C. Synaptic vesicle pools at diaphragm neuromuscular junctions vary with motoneuron soma, not axon terminal, inactivity. Neuroscience 2007, 146:178-189.
24. Mantilla C.B., Zhan W.Z., Sieck G.C. Retrograde labeling of phrenic motoneurons by intrapleural injection. J. Neurosci. Methods 2009, 182:244-249.
25. Mantilla C.B., Seven Y.B., Hurtado-Palomino J.N., Zhan W.Z., Sieck G.C. Chronic assessment of diaphragm muscle EMG activity across motor behaviors. Respir. Physiol. Neurobiol. 2011, 177:176-182.
26. McCrimmon D.R., Smith J.C., Feldman J.L. Involvement of excitatory amino acids in neurotransmission of inspiratory drive to spinal respiratory motoneurons. J. Neurosci. 1989, 9:1910-1921.
27. McGuire M., Liu C., Cao Y., Ling L. Formation and maintenance of ventilatory long-term facilitation require NMDA but not non-NMDA receptors in awake rats. J. Appl. Physiol. 2008, 105:942-950.
28. Mitchell G.S., Sloan H.E., Jiang C., Miletic V., Hayashi F., Lipski J. 5-Hydroxytryptophan (5-HTP) augments spontaneous and evoked phrenic motoneuron discharge in spinalized rats. Neurosci. Lett. 1992, 141:75-78.
29. Miyata H., Zhan W.Z., Prakash Y.S., Sieck G.C. Myoneural interactions affect diaphragm muscle adaptations to inactivity. J. Appl. Physiol. 1995, 79:1640-1649.
30. Murphy S.M., Pilowsky P.M., Llewellyn-Smith I.J. Vesicle shape and amino acids in synaptic inputs to phrenic motoneurons: do all inputs contain either glutamate or GABA?. J. Comp. Neurol. 1996, 373:200-219.
31. 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.
32. Nantwi K.D., El-Bohy A., Schrimsher G.W., Reier P.J., Goshgarian H.G. Spontaneous functional recovery in a paralyzed hemidiaphragm following upper cervical spinal cord injury in adult rats. Neurorehabil. Neural Repair 1999, 13:225-234.
33. National Spinal Cord Injury Statistical Center Spinal Cord Injury: Facts and Figures at a Glance 2011, University of Alabama, Birmingham.
34. O'Hara T.E.J., Goshgarian H.G. Quantitative assessment of phrenic nerve functional recovery mediated by the crossed phrenic reflex at various time intervals after spinal cord injury. Exp. Neurol. 1991, 111:244-250.
35. Porter J. The path of the respiratory impulse from the bulb to the phrenic nuclei. J. Physiol. (Lond) 1895, 17:455-485.
36. Prakash Y.S., Smithson K.G., Sieck G.C. Measurements of motoneuron somal volumes using laser confocal microscopy: comparisons with shape-based stereological estimations. Neuroimage 1993, 1:95-107.
37. Prakash Y.S., Miyata H., Zhan W.Z., Sieck G.C. Inactivity-induced remodeling of neuromuscular junctions in rat diaphragmatic muscle. Muscle Nerve 1999, 22:307-319.
38. 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.
39. Rekling J.C., Funk G.D., Bayliss D.A., Dong X.W., Feldman J.L. Synaptic control of motoneuronal excitability. Physiol. Rev. 2000, 80:767-852.
40. Robinson D., Ellenberger H. Distribution of N-methyl-d-aspartate and non-N-methyl-d-aspartate glutamate receptor subunits on respiratory motor and premotor neurons in the rat. J. Comp. Neurol. 1997, 389:94-116.
41. Rosenblueth A., Klopps C.T., Simeone F.A. A further study of the crossed phrenic phenomenon. J. Neurophysiol. 1938, 1:508-520.
42. 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.
43. Tai Q., Goshgarian H.G. Ultrastructural quantitative analysis of glutamatergic and GABAergic synaptic terminals in the phrenic nucleus after spinal cord injury. J. Comp. Neurol. 1996, 372:343-355.
44. Trelease R.B., Sieck G.C., Harper R.M. A new technique for acute and chronic recording of crural diaphragm EMG in cats. Electroencephalogr. Clin. Neurophysiol. 1982, 53:459-462.
45. Twigger S.N., Shimoyama M., Bromberg S., Kwitek A.E., Jacob H.J. The Rat Genome Database, update 2007 - easing the path from disease to data and back again. Nucleic Acids Res. 2007, 35:D658-D662.
46. Vinit S., Gauthier P., Stamegna J.C., Kastner A. High cervical lateral spinal cord injury results in long-term ipsilateral hemidiaphragm paralysis. J. Neurotrauma 2006, 23:1137-1146.
47. Zhan W.Z., Ellenberger H.H., Feldman J.L. Monoaminergic and GABAergic terminations in phrenic nucleus of rat identified by immunohistochemical labeling. Neuroscience 1989, 31:105-113.
48. Zhou S.Y., Goshgarian H.G. Effects of serotonin on crossed phrenic nerve activity in cervical spinal cord hemisected rats. Exp. Neurol. 1999, 160:446-453.
49. Zhou S.Y., Basura G.J., Goshgarian H.G. Serotonin(2) receptors mediate respiratory recovery after cervical spinal cord hemisection in adult rats. J. Appl. Physiol. 2001, 91:2665-2673.