Ultrastructural study of glutamate- and GABA-immunoreactive terminals contacting the primary afferent fibers in frog spinal cord: A double postembedding immunocytochemical study

Brain Research

Volumn 960, Issue 1-2, 2003, Pages 267-272

  Vesselkin, N P ^a,c   Adanina, V O ^a,b   Rio, J P ^b   Reperant J ^b,c  

^a RUSSIAN ACADEMY OF SCIENCES   (Russian Federation)

^b PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^c MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

Author keywords

Axo axonic synapse; Excitable membranes and synaptic transmission; Frog; GABA; Glutamate; Presynaptic mechanisms; Primary afferent; Spinal cord

Indexed keywords

4 AMINOBUTYRIC ACID; GLUTAMIC ACID;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DORSAL ROOT; FROG; GABAERGIC SYSTEM; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; IN VITRO STUDY; MUSCLE SPINDLE AFFERENT NERVE; NONHUMAN; PRIORITY JOURNAL; SPINAL CORD; STAINING; SYNAPSE;

ANIMALS; FEMALE; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; HORSERADISH PEROXIDASE; IMMUNOHISTOCHEMISTRY; MALE; NEURONS, AFFERENT; PRESYNAPTIC TERMINALS; RANA TEMPORARIA; SPINAL CORD; TISSUE EMBEDDING;

EID: 0037449448     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(02)03795-2     Document Type: Article

References (34)

1. Adams J.C. Heavy metal intensification of DAB-based HRP reaction product. J. Histochem. Cytochem. 29:1981;775.
2. Aicher S.A., Sharma S., Cheng P.Y., Pickel V.M. The N-methyl-D-aspartate (NMDA) receptor is postsynaptic to substance P-containing axon terminals in the rat superficial dorsal horn. Brain Res. 772:1997;71-81.
3. Azkue J.J., Murga M., Fernández-Capetillo O., Mateos J.M., Elezgarai I., Benítez R., Osorio A., Díez J., Puente N., Bilbao A., Bidaurrazaga A., Kuhn R., Grandes P. Immunoreactivity for the group III metabotropic glutamate receptor subtype mGluR4a in the superficial laminae of the rat spinal dorsal horn. J. Comp. Neurol. 430:2001;448-457.
4. Barron H., Matthews B.H.C. The interpretation of potential changes in the spinal cord. J. Physiol. (Lond.). 92:1938;276-321.
5. Ben-Ari Y., Cossart R. Kainate, a double agent that generates seizures: two decades of progress. Trends Neurosci. 23:2000;580-587.
6. Carlton S.M., Hargett G.L., Coggeshall R.E. Localization of metabotropic glutamate receptors 2/3 on primary afferent axons in the rat. Neuroscience. 105:2001;957-969.
7. Cochilla A.J., Alford S. Metabotropic glutamate receptor-mediated control of neurotransmitter release. Neuron. 20:1998;1007-1016.
8. Cochilla A.J., Alford S. NMDA receptor-mediated control of presynaptic calcium and neurotransmitter release. J. Neurosci. 19:1999;193-205.
9. Curtis D.R., Lodge D., Brand S.J. GABA and spinal afferent terminal excitability in the cat. Brain Res. 130:1977;360-363.
10. Erecinska M., Silver I.A. Metabolism and role of glutamate in mammalian brain. Prog. Neurobiol. 35:1990;245-296.
11. Frerking M., Nicoll R.A. Synaptic kainate receptors. Curr. Opin. Neurobiol. 10:2000;342-351.
12. Hackman J.C., Davidoff R.A. Dorsal root potentials in the isolated frog spinal cord: amino acid neurotransmitters and magnesium ions. Neuroscience. 41:1991;61-69.
13. Hackman J.C., Holohean A.M., Davidoff R.A. Role of metabotropic glutamate receptors in the depression of GABA-mediated depolarization of frog primary afferent terminals. Neuroscience. 81:1997;1079-1090.
14. Huettner J.E. Glutamate receptor channels in rat DRG neurons: activation by kainate and quisqualate and blockade of desensitization by Con A. Neuron. 5:1990;255-266.
15. Hwang S.J., Pagliardini S., Rustioni A., Valtschanoff J.G. Presynaptic kainate receptors in primary afferents to the superficial laminae of the rat spinal cord. J. Comp. Neurol. 436:2001;275-289.
16. Kenigfest N.B., Repérant J., Rio J.P., Belekhova M.G., Ward R., Vesselkin N.P., Miceli D., Herbin M. Retinal and cortical afferents to the dorsal lateral geniculate nucleus of the turtle, Emys orbicularis: a combined axonal tracing, glutamate, and GABA immunocytochemical electron microscopic study. J. Comp. Neurol. 391:1998;470-490.
17. Kerchner G.A., Wilding T.J., Li P., Zhuo M., Huettner J.E. Presynaptic kainate receptors regulate spinal sensory transmission. J. Neurosci. 21:2001;59-66.
18. Levenes C., Daniel H., Crepel F. Retrograde modulation of transmitter release by postsynaptic subtype 1 metabotropic glutamate receptors in the rat cerebellum. J. Physiol. 537:2001;125-140.
19. Liu H., Wang H., Sheng M., Jan L.Y., Jan Y.N., Basbaum A.I. Evidence for presynaptic N-methyl-D-aspartate autoreceptors in the spinal cord dorsal horn. Proc. Natl. Acad. Sci. USA. 91:1994;8383-8387.
20. Liu H., Mantyh P.W., Basbaum A.I. NMDA-receptor regulation of substance P release from primary afferent nociceptors. Nature. 386:1997;721-724.
21. Lovinger D.M., Weight F.W. Glutamate induces a depolarization of adult rat dorsal root ganglion neurons that is mediated predominantly by NMDA receptors. Neurosci. Lett. 94:1988;314-320.
22. Ma Q.-P., Hargreaves R.J. Localization of N-methyl-D-aspartate NR2B subunits on primary sensory neurons that give rise to small-caliber sciatic nerve fibers in rats. Neuroscience. 101:2000;699-707.
23. MacDermott A.B., Role L.W., Siegelbaum S. Presynaptic ionotropic receptors and the control of transmitter release. Annu. Rev. Neurosci. 22:1999;443-485.
24. Maxwell D.J., Christie W.M., Ottersen O.P., Storm-Mathisen J. Terminals of group Ia primary afferent fibres in Clarke's column are enriched with L-glutamate-like immunoreactivity. Brain Res. 510:1990;346-350.
25. Ottersen O.P. Postembedding light and electron microscopic immunocytochemistry of amino acids: description of a new model system allowing identical conditions of specificity testing and tissue processing. Exp. Brain Res. 69:1987;167-184.
26. B receptors causes presynaptic inhibition at synapses between muscle spindle afferents and motoneurons in the spinal cord of bullfrogs. J. Neurosci. 9:1989;1502-1515.
27. A receptors causes presynaptic and postsynaptic inhibition at synapses between muscle spindle afferents and motoneurons in the spinal cord of bullfrogs. J. Neurosci. 9:1989;1516-1522.
28. Shapovalov A.I., Shiriaev B.I. Recurrent interactions between individual motoneurones and dorsal root fibres in the frog. Exp. Brain Res. 38:1980;115-116.
29. Schmitz D., Frerking M., Nicoll R.A. Synaptic activation of presynaptic kainate receptors on hippocampal mossy fiber synapses. Neuron. 27:2000;327-338.
30. Somogyi P., Halasz K., Somogyi J., Storm-Mathisen J., Ottersen O.P. Quantification of immunogold labelling reveals enrichment of glutamate in mossy and parallel fibre terminals in cat cerebellum. Neuroscience. 19:1986;1045-1050.
31. Somogyi P., Tamás G., Lujan R., Buhl E.H. Salient features of synaptic organisation in the cerebral cortex. Brain Res. Rev. 26:1998;113-135.
32. Storm-Mathisen J., Ottersen O.P. Immunocytochemistry of glutamate at the synaptic level. J. Histochem. Cytochem. 38:1990;1733-1743.
33. Vesselkin N.P., Adanina V.O., Rio J.P., Repérant J. Axo-axonic GABA-immunopositive synapses on the primary afferent fibers in frogs. J. Chem. Neuroanat. 22:2001;209-217.
34. Yang H.W., Appenteng K., Batten T.F. Ultrastructural subtypes of glutamate-immunoreactive terminals on rat trigeminal motoneurones and their relationships with GABA-immunoreactive terminals. Exp. Brain Res. 114:1997;99-116.