Ultrastructural quantitative analysis of glutamatergic and GABAergic synaptic terminals in the phrenic nucleus after spinal cord injury

Journal of Comparative Neurology

Volumn 372, Issue 3, 1996, Pages 343-355

  Tai, Qing ^a   Goshgarian, Harry G ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

electron microscopy; plasticity; postembedding immunochemistry; synaptogenesis

Indexed keywords

4 AMINOBUTYRIC ACID; GLUTAMIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITE; DENSE BODY; ELECTRON MICROSCOPY; FEMALE; IMMUNOCHEMISTRY; NERVE CELL PLASTICITY; NERVE ENDING; NEUROFILAMENT; NONHUMAN; PHRENIC NERVE; PRIORITY JOURNAL; RAT; SPINAL CORD HEMISECTION; SPINAL CORD INJURY; SYNAPSE; SYNAPSE VESICLE; SYNAPTIC MEMBRANE; SYNAPTOGENESIS; ULTRASTRUCTURE;

ANIMALS; FEMALE; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; IMMUNOHISTOCHEMISTRY; MICROSCOPY, ELECTRON; MOTOR NEURONS; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD INJURIES;

EID: 0029819827     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19960826)372:3<343::AID-CNE2>3.0.CO;2-2     Document Type: Article

References (43)

1. Berger, A.J. (1979) Phrenic motoneurons in the cat: subpopulations and nature of respiratory drive potentials. J. Neurophysiol. 42:76-90.
2. Chen, S., and D.E. Hillman (1990) Robust synaptic plasticity of striatal cells following partial deafferentation. Brain Res. 520(1-2):103-114.
3. Davies, J.G.M., P.A. Kirkwood, and T.A. Sears (1985) The detection of monosynaptic connections from inspiratory bulbospinal neurons to inspiratory motoneurons in the cat. J. Physiol. (Lond.) 368:33-62.
4. Ellenberger, H.H., and J.L. Feldman (1990) Subnuclear organization of the lateral tegmental field of the rat: I. Nucleus ambiguus and ventral respiratory group. J. Comp. Neurol. 294:202-211.
5. Fedorko, L., C.A. Connelly, and J.E. Remmers (1987) Neurotransmitters mediating synaptic inhibition of phrenic motoneurons. In G.C. Sieck, S.C. Gandevia, and W.E. Cameron (eds): Respiratory Muscle and their Neuromotor Control. New York: Alan R. Liss, Inc., pp. 167-173.
6. Feldman, J.L., J.C. Smith, H.H. Ellenberger, C.A. Connelly, G. Liu, J.J. Greer, A.D. Lindsay, and M.R. Otto (1990) Neurogenesis of respiratory rhythm and pattern: emerging concepts. Am. J. Physiol. 259:R579-R586.
7. Gibson, A.R., D.I. Hansma, J.C. Houk, and F.R. Robinson (1984) A sensitive low artifact TMB procedure for the demonstration of WGA-HRP in the CNS. Brain Res. 298:235-241.
8. Goshgarian, H.G. (1979) Developmental plasticity in the respiratory pathway of the adult rat. Exp. Neurol. 66:547-555.
9. Goshgarian, H.G., and L. Guth (1977) Demonstration of functionally ineffective synapses in the guinea pig spinal cord. Exp. Neurol. 57:613-621.
10. Goshgarian, H.G., and J. Rafols (1981) The phrenic nucleus of the albino rat: a correlative HRP and Golgi study. J. Comp. Neurol. 201:441-456.
11. Goshgarian, H.G., and J. Rafols (1984) The ultrastructure and synaptic architecture of phrenic motor neurons in the spinal cord of the adult rat. J. Neurocytol. 13:85-109.
12. Goshgarian, H.G., X.-J. Yu, and J.A. Rafols (1989) Neuronal and glial changes in the rat phrenic nucleus occurring within hours after spinal cord injury. J. Comp. Neurol. 284:519-533.
13. Goshgarian, H.G., H.H. Ellenberger, and J.L. Feldman (1993) Bulbospinal respiratory neurons are a source of double synapses onto phrenic motoneurons following cervical spinal cord hemisection in adult rats. Brain Res. 600:169-173.
14. Greer, J.J., J.C. Smith, and J.L. Feldman (1992) Glutamate release and presynaptic action of AP4 during inspiratory drive to phrenic motoneurons. Brain Res. 576:355-357.
15. Gundersen, H.J.G. (1977) Notes on the estimation of the numerical density of arbitrary profiles: the edge effect. J. Microsc. 111:219-223.
16. Gundersen, H.J.G., P. Bagger, T.F. Bendtsen, S.M. Evans, L. Korbo, N. Marcussen, A. Moller, K. Nielsen, J.R. Nyengaard, B. Pakkengerg, F.B. Sorensen, A. Vesterby, and M.J. West (1988) The new stereological tolls: disector, fractionator, nucleator, point sampled intercepts and their use in pathological research and diagnosis. APMIS 96:857-881.
17. Hillman, D.E., and S. Chen (1984) Reciprocal relationship between size of postsynaptic densities and their number: constancy in contact area. Brain Res. 295:325-343.
18. Hillman, D.E., and S. Chen (1985) Plasticity in the size of presynaptic and postsynaptic membrane specializations. In C.W. Cotman (ed): Synaptic Plasticity. New York: Guilford Press, pp. 39-76.
19. Hökfelt, T. (1992) Neuropeptides in perspective: the last ten years. Neuron 7:867-879.
20. Holtman, J.R., W.P. Norman, L. Skirboll, K.L. Dretchen, C. Cuello, T.J. Visser, T. Hökfelt, and R.A. Gillis (1984) Evidence for 5-hydroxytryptamine, substance P, and thyrotropin-releasing hormone in neurons innervating the phrenic motor nucleus. J. Neurosci. 4:1064-1071.
21. Holtman, J.R., D.S. Vascik, and B.E. Maley (1990) Ultrastructural evidence for serotonin-immunoreactive terminals contacting phrenic motoneurons in the cat. Exp. Neurol. 109:269-272.
22. Horn, A.K.E., and K.P. Hoffman (1987) Combined GABA-immunocytochemistry and TMB-HRP histochemistry of pretectal nuclei projecting to the inferior olive in rats, cats and monkeys. Brain Res. 409:133-138.
23. Johnson, M.D. (1994) Synaptic glutamate release by postnatal rat serotonergic neurons in microculture. Neuron 12(2):433-442.
24. Ling, L., K.B. Bach, and G.S. Mitchell (1994) Serotonin reveals ineffective spinal pathways to contralateral phrenic motoneurons in spinally hemisected rats. Exp. Brain Res. 101:35-43.
25. Liu, G.S., J.L. Feldman, and J.C. Smith (1990) Excitary amino acid-mediated transmission of inspiratory drive to phrenic motoneurons. J. Neurophysiol. 64:423-436.
26. Liu, H., M. Sheng, L.Y. Jan, Y.N. Jan, and A.I. Basbaum (1994) Evidence for presynaptic N-methyl-D-aspartate autoreceptors in the spinal cord dorsal horn. Proc. Natl. Acad. Sci. U.S.A. 91:8383-8387.
27. McCrimmon, D.R., J.C. Smith, and J.L. Feldman (1989) Involvement of excitatory amino acids in neurotransmission of inspiratory drive to spinal respiratory motoneurons. J. Neurosci. 9(6):1910-1921.
28. Moreno, D.E., X.-J. Yu, and H.G. Goshgarian (1992) Identification of axon pathways which mediate functional recovery of a paralyzed hemidiaphragm following spinal cord hemisection in the adult rat. Exp. Neurol. 116:219-228.
29. Murphy, S.M., P.M. Pilowsky, Q.-J. Sun, and I.J. Llewell-Smith (1994) Amino acid- and neuropeptide-containing synaptic inputs to rat phrenic motoneurons. Soc. Neurosci. Abstr. 20:545.
30. Onai, T., M. Saji, and M. Miura (1987) Projections of supraspinal structures to the phrenic motor nucleus in rats studied by a horseradish peroxidase microinjection method. J. Auton. Nerv. Syst. 21:233-240.
31. Peters, A., S.L. Palay, and F. Webster (1991) Synapses. In A. Peters, S.L. Palay, and F. Webster (eds): The Fine Structure of the Nervous System. New York: Oxford, pp. 138-210.
32. Pilowsky, P.M., D. de Castro, I. Liewellyn-Smity, J. Lipski, and M.D. Voss (1990) Serotonin immunoreactive boutons make synapses with feline phrenic motoneurons. J. Neurosci. 10:1091-1098.
33. Rye, D.B., C.B. Saper, and B.H. Wainer (1984) Stabilization of the tetramethyl benzidine (TMB) reaction product: application for retrograde and anterograde tracing, and combination with immunohistochemistry. J. Histochem. Cytochem. 32:1145-1153.
34. Saji, M., and M. Miura (1990) Evidence that glutamate is the transmitter mediating respiratory drive from medullary premotor neurons to phrenic motoneurons: a double labeling study in the rat. Neurosci. Lett. 115:177-182.
35. Sperry, M.A., and H.G. Goshgarian (1993) Ultrastructural changes in the rat phrenic nucleus developing within 2 hours after cervical spinal cord hemisection. Exp. Neurol. 120:233-244.
36. Tai, Q., and H.G. Goshgarian (1994) Immunocytochemical demonstration of the major neuromessengers in the phrenic nucleus. J. Am. Parapleg. Soc. 17(4):228.
37. Uchizono, K. (1965) Characteristics of excitatory and inhibitory synapses in the central nervous system of the cat. Nature 207:642-643.
38. Uchizono, K. (1968) Axon identification in the cerebellar cortex of the cat. Arch. Histol. Jpn. 29:399-424.
39. Uchizono, K. (1969) Synaptic organization of the mammalian cerebellum. In R. Llinas (ed): Neurobiology of Cerebellar Evolution and Development. Chicago: AMA-ERF Institute for Biomedical Research, pp. 549-581.
40. Vascik, D.A., B.E. Maley, and J.R. Holtman, Jr. (1988) GABA immunoreactive terminals contact phrenic motoneurons. Soc. Neurosci. Abstr. 14:936.
41. Womack, M., A. MacDermott, and T. Jessel (1988) Sensory transmitters regulate intracellular calcium in dorsal horn neurons. Nature 334:351-353.
42. Zhan, W.-Z., H.H. Ellenberger, and J.L. Feldman (1989) Monoaminergic and GABAergic terminations in phrenic nucleus of rat identified by immunohistochemical labeling. Neuroscience 31:105-113.
43. Zhang, B., M.E. Goldberger, and M. Murray (1993) Proliferation of SP- and 5HT-containing terminals in lamina II of rat spinal cord following dorsal rhizotomy: quantitative EM-immunocytochemical studies. Exp. Neurol. 123:51-63.