Hostname: page-component-848d4c4894-m9kch Total loading time: 0 Render date: 2024-05-21T04:33:27.129Z Has data issue: false hasContentIssue false
  • English
  • Français

Quantitative immunogold evidence for enrichment of glutamate but not aspartate in synaptic terminals of retino-geniculate, geniculo-cortical, and cortico-geniculate axons in the cat

Published online by Cambridge University Press:  02 June 2009

Vicente M. Montero
Vicente M. Montero
Affiliation:
Department of Neurophysiology, University of Wisconsin, Madison
Get access Rights & Permissions [Opens in a new window]

Abstract

A postembedding immunogold procedure was used on thin sections of the dorsal lateral geniculate nucleus (LGN) and perigeniculate nucleus (PGN) of the cat to estimate qualitatively and quantitatively, at the electron-microscopic (EM) level, the intensity of glutamate or aspartate immunoreactivities on identifiable synaptic terminals and other profiles of the neuropil. On sections incubated with a glutamate antibody, terminals of retinal and cortical axons in the LGN, and of collaterals of geniculo-cortical axons in the PGN, contain significantly higher density of immunogold particles than GABAergic terminals, glial cells, dendrites, and cytoplasm of geniculate cells. By contrast, in sections incubated with an aspartate antibody, terminals of retino-geniculate, cortico-geniculate, and geniculo-cortical axons did not show a selective enrichment of immunoreactivity, but instead the density of immunogold particles was generally low in the different profiles of the neuropil, with the exception of nucleoli. These results suggest that glutamate, but not aspartate, is a neurotransmitter candidate in the retino-geniculo-cortical pathways.

Keywords

NeurotransmittersSynapsesLateral geniculate nucleusRetinaVisual cortex
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 4 , July 1994 , pp. 675 - 681
Copyright
Copyright © Cambridge University Press 1994

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anderso, K.J., Borja, M.A., Cotman, C.W., Moffet, J.R., Namboodiri, M.A.A. & Neale, J.H. (1987). n-Acetylaspartyl-glutamate identified in the rat retina ganglion cells and their projections in the brain. Brain Research 411, 172–177.CrossRefGoogle Scholar
Baughman, R.W. & Gilbert, C.D. (1981). Aspartate and glutamate as possible neurotransmitters of cells in the visual cortex. Journal of Neuroscience 4, 427–439.CrossRefGoogle Scholar
Blakely, R.D., Robinson, M.B., Thompson, R.C. & Coyle, J.T. (1988). Hydrolysis of the brain dipeptide n-acetyl-l-aspartyl-l-glutamate: Subcellular and regional distribution, ontogeny, and the effect of lesions on n-acetylated-a-linked acidic dipeptidase activity. Journal of Neurochemistry 50, 1200–1209.CrossRefGoogle Scholar
Collingridge, G.L. & Lester, R.A.J. (1989). Excitatory amino acid receptors in the vertebrate central nervous system. Pharmacological Review 40, 143–210.Google Scholar
Davanger, S., Ottersen, O.P. & Storm-Mathisen, J. (1991). Glutamate, GABA, and glycine in the human retina: An immunocyto-chemical investigation. Journal of Comparative Neurology 311, 483–494.CrossRefGoogle Scholar
Davies, L.P. & Johnston, G.A.R. (1976). Uptake and release of d- and L-aspartate by rat brain slices. Journal of Neurochemistry 26, 1007–1014.CrossRefGoogle ScholarPubMed
De Biasi, S. & Rustioni, A. (1990). Ultrastructural immunocytochemical localization of excitatory amino acids in the somatosensory system. Journal of Histochemistry and Cytochemistry 38, 1745–1754.CrossRefGoogle ScholarPubMed
Ehtnger, B. (1981). [3H]-D-Aspartate accumulation in the retina of pigeon, guinea-pig, and rabbit. Experimental Eye Research 33, 381–391.CrossRefGoogle Scholar
Ffrench-Mullen, J.M.H., Roller, K.J., Zaczek, R., Coyle, J.T., Hori, N. & Carpenter, D.O. (1985). N-acetyl-aspartyl-glutamate: Possible role as the neurotransmitter of the lateral olfactory tract. Proceedings of the National Academy of Sciences of the U.S.A. 82, 3897–3900.CrossRefGoogle ScholarPubMed
Fonnum, F. (1984). Glutamate: A neurotransmitter in mammalian brain. Neurochemistry 42, 1–11.CrossRefGoogle ScholarPubMed
Forloni, G., Grzanna, R., Blakely, R.D. & Coyle, J.T. (1987). Co-localization of N-acetyl-aspartyl-glutamate in central cholinergic, noradrenergic, and serotonergic neurons. Synapse 1, 455–460.CrossRefGoogle ScholarPubMed
Funke, K., Eysel, U.T. & Frrzgibbon, T. (1991). Retinogeniculate transmission by NMDA and non-NMDA receptors in the cat. Brain Research 547, 229–238.CrossRefGoogle ScholarPubMed
Gulllery, R.W. (1969). The organization of synaptic interconnections in the laminae of the dorsal lateral geniculate nucleus of the cat. Zeitschrift fur Zellforschung 96, 1–38.CrossRefGoogle Scholar
Hagihara, K., Tsumoto, T., Sato, H. & Hata, Y. (1988). Actions of excitatory amino acid antagonists on geniculo-cortical transmission in the cat's visual cortex. Experimental Brain Research 69, 407–416.CrossRefGoogle ScholarPubMed
Hartveit, E. & Heggelund, P. (1990). Neurotransmitter receptors mediating excitatory input to cells in the cat lateral geniculate nucleus. II. Non-lagged cells. Journal of Neurophysiology 63, 1361–1372.CrossRefGoogle Scholar
Henderson, Z. & Salt, T.E. (1988). The effects of N-acetylaspartyl-glutamate like immunoreactivity in the rat somatosensory thalamus. Neuroscience 25, 899–906.CrossRefGoogle Scholar
Heggelund, P. & Hartveit, E. (1990). Neurotransmitter receptors mediating excitatory input to cells in the cat lateral geniculate nucleus, I. Lagged cells. Journal of Neurophysiology 63, 1347–1360.CrossRefGoogle ScholarPubMed
Hicks, T.P., Kaneko, T., Metherate, R., Oka, J. & Stark, C.A. (1991). Amino acids as transmitters of synaptic excitation in neo-cortical sensory processes. Canadian Journal of Physiological Pharmacology 69, 1099–1114.CrossRefGoogle Scholar
Ide, L.S. (1982). The fine structure of the perigeniculate nucleus in the cat. Journal of Comparative Neurology 210, 317–334.CrossRefGoogle ScholarPubMed
Jones, H.E. & Sillito, A.M. (1992). The action of the putative neurotransmitters N-acetylaspartylglutamate and L-homocysteate in cat dorsal lateral geniculate nucleus. Journal of Neurophysiology 68, 663–672.CrossRefGoogle ScholarPubMed
Kanai, Y., Smith, C.P. & Hediger, M.A. (1993). The elusive transporters with a high affinity for glutamate. Trends in Neuroscience 16, 365–370.CrossRefGoogle ScholarPubMed
Kemp, J.A. & Slllito, A.M. (1982). The nature of the excitatory transmitter mediating X and Y cell inputs to the cat dorsal lateral geniculate nucleus. Journal of Physiology 323, 377–391.CrossRefGoogle Scholar
Kharazia, V.N. & Weinberg, R.J. (1993). Glutamate in terminals of thalamocortical fibers in rat somatic sensory cortex. Neuroscience Letters 157, 162–166.CrossRefGoogle ScholarPubMed
Kwon, Y.H., Esguerra, M. & Sur, M. (1991). NMDA and Non-NMDA receptors mediate visual responses of neurons in the cat's lateral geniculate nucleus. Journal of Neurophysiology 66, 414–428.CrossRefGoogle ScholarPubMed
Logan, W.J. & Snyder, S.H. (1972). High-affinity uptake systems for glycine, glutamate and aspartate in synaptosomes of rat central tissues. Brain Research 42, 413–431.CrossRefGoogle Scholar
Matute, C. & Streit, P. (1985). Selective retrograde labeling with D-[3H]-aspartate in afferents to the mammalian superior colliculus. Journal of Comparative Neurology 241, 34–49.CrossRefGoogle Scholar
Maxwell, D.J., Christie, W.M., Brown, A.G., Ottersen, O.P. & Storm-Mathisen, J. (1992). Direct observations of synapses between L-glutamate-immunoreactive boutons and identified spinocervical tract neurones in the spinal cordo of the cat. Journal of Comparative Neurology 326, 485–500.CrossRefGoogle Scholar
Maxwell, D.J., Christie, W.M., Brown, A.G., Ottersen, O.P. … Storm-Mathisen, J. (1993). Identified hair follicle afferent boutons in the spinal cord of the cat are enriched with L-glutamate-like immunoreactivity. Brain Research 606, 156–161.CrossRefGoogle ScholarPubMed
McCormick, D.A. (1992). Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity. Progress in Neurobiology 39, 337–388.CrossRefGoogle ScholarPubMed
Moffett, J.R., Williamson, L.C., Neale, J.H., Palkovtts, M. & Nam-boodiri, M.A.A. (1991). Effect of optic nerve transection on n-acetylaspartylglutamate immunoreactivity in the primary and accessory optic projection systems in the rat. Brain Research 538, 86–94.CrossRefGoogle ScholarPubMed
Molinar-Rode, R. & Paslk, P. (1992). Amino acids and N-acetyl-aspartyl-glutamate as neurotransmitter candidates in the monkey retinogeniculate pathways. Experimental Brain Research 89, 40–48.CrossRefGoogle ScholarPubMed
Montero, V.M. (1986). Localization of gamma-aminobutyric acid (GABA) in type 3 cells and demonstration of their source to F2 terminals in the cat lateral geniculate nucleus: A Golgi-electron-microscopic GABA-immunocytochemical study. Journal of Comparative Neurology 254, 228–245.CrossRefGoogle ScholarPubMed
Montero, V.M. (1989). Ultrastructural identification of synaptic terminals from cortical axons and from collateral axons of geniculo-cortical relay cells in the perigeniculate nucleus of the cat. Experimental Brain Research 75, 65–72.CrossRefGoogle ScholarPubMed
Montero, V.M. (1990). Quantitative immunogold analysis reveals high glutamate levels in synaptic terminals of retino-geniculate, cortico-geniculate, and geniculo-cortical axons in the cat. Visual Neuroscience 4, 437–443.CrossRefGoogle ScholarPubMed
Montero, V.M. & Singer, W. (1984). Ultrastructure and synaptic relations of neural elements containing glutamic acid decarboxylase (GAD) in the perigeniculate nucleus of the cat: A light and electron microscopic immunocytochemical study. Experimental Brain Research 56, 115–125.CrossRefGoogle Scholar
Montero, V.M. & Wenthold, R.J. (1989). Quantitative immunogold analysis reveals high glutamate levels in retinal and cortical synaptic terminals in the lateral geniculate nucleus of the macaque. Neuroscience 31, 639–647.CrossRefGoogle ScholarPubMed
Montero, V.M. (1991). A quantitative study of synaptic contacts on interneurons and relay cells of the cat lateral geniculate nucleus. Experimental Brain Research 86, 257–270.CrossRefGoogle ScholarPubMed
Montero, V.M. & Wenthold, R.J. (1991). Quantitative immunogold evidence for high levels of glutamate but not aspartate in synaptic terminals of retino-geniculate, cortico-geniculate and geniculo-cortical axons in the cat. Society of Neuroscience Abstracts 17, 627.Google Scholar
Mosinger, J. & Altschuler, R.A. (1985). Aspartate aminotransferase-like immunoreactivity in the guinea pig and monkey retinas. Journal of Comparative Neurology 233, 255–268.CrossRefGoogle ScholarPubMed
Naito, S. & Ueda, T. (1985). Characterization of glutamate uptake into synaptic vesicles. Journal of Neurochemistry 44, 99–109.CrossRefGoogle ScholarPubMed
Nunes-Cardoso, B., Bults, R. & Vanderwant, J. (1991). Glutamate-like immunoreactivity in retinal terminals in the nucleus of the optic tract in rabbits. Journal of Comparative Neurology 309, 261–270.Google Scholar
Ottersen, O.P. (1989). Quantitative electron microscopic immunocy-tochemistry of neuroactive amino acids. Anatomy and Embryology 180, 1–15.CrossRefGoogle Scholar
Ottersen, O.P. & Storm-Mathisen, J. (1984). Glutamate- and GABA-containing neurons in the mouse and rat brain, as demonstrated with a new immunocytochemical technique. Journal of Comparative Neurology 229, 374–392.CrossRefGoogle ScholarPubMed
Pines, G., Danbolt, N.C., Bjoras, M., Zhang, Y., Bendahan, A., Eide, L., Koepsel, H., Storm-Mathisen, J., Seeberg, E. & Kan-ner, B.I. (1992). Cloning and expression of a rat brain L-glutamate transporter. Nature 360, 464–467.CrossRefGoogle ScholarPubMed
Rinvik, E. & Ottersen, O.P. (1993). Terminals of subthalamonigral fibres are enriched with glutamate-like immunoreactivity: An electron microscopic, immunogold analysis in the cat. Journal of Chemical Neuroanatomy 6, 19–30.CrossRefGoogle ScholarPubMed
Rrveros, N. & Orrego, F. (1982). A search in rat brain cortex synaptic vesicles for endogenous ligands for kainic acid receptors. Brain Research 236, 492–496.CrossRefGoogle Scholar
Riveros, N., Fiedler, J., Lagos, N., Munoz, C. & Orrego, F. (1986). Glutamate in rat brain cortex synaptic vesicles: Influence of the vesicle isolation procedure. Brain Research 386, 405–408.CrossRefGoogle ScholarPubMed
Roberts, P.J. (1974). Amino acid release from isolated rat dorsal root ganglia. Brain Research 74, 327–332.CrossRefGoogle ScholarPubMed
Robson, J.A. (1983). The morphology of corticofugal axons to the dorsal lateral geniculate nucleus in the cat. Journal of Comparative Neurology 216, 89–103.CrossRefGoogle Scholar
Robson, J.A. & Mason, C.A. (1979). The synaptic organization of terminals traced from individual labeled retino-geniculate axons in the cat. Neuroscience 4, 99–111.CrossRefGoogle ScholarPubMed
Sakurai, T. & Okada, Y. (1992). Selective reduction of glutamate in the rat superior colliculus and dorsal lateral geniculate nucleus after contralateral enucleation. Brain Research 573, 197–203.CrossRefGoogle ScholarPubMed
Sekiguchi, M., Wada, K. & Wenthold, R.J. (1992). N-Acetylaspartyl-glutamate acts as an agonist upon homomeric NMDA receptor (NMDAR1) expressed in Xenopus oocytes. Federation European Biochemistry Society 311, 285–289.CrossRefGoogle Scholar
Sillito, A.M., Murphy, P.C. & Salt, T.E. (1990 a). The contribution of the non-NMDA group of excitatory amino acid receptors to retinogeniculate transmission in the cat. Neuroscience 34, 273–280.CrossRefGoogle Scholar
Sillito, A.M., Murphy, P.C., Salt, T.E. & Moody, C.I. (1990 b). The dependence of retinogeniculate transmission in the cat on NMDA receptors. Journal of Neurophysiology 63, 347–355.CrossRefGoogle ScholarPubMed
Somogyi, J., Hamori, J. & Silakov, V.L. (1984). Synaptic reorganization in the lateral geniculate nucleus of the adult cat following chronic decortication. Experimental Brain Research 54, 485–498.CrossRefGoogle ScholarPubMed
Somogyi, P., Halasy, K., Somogyi, J., Storm-Mathisen, J. & Otter-sen, O.P. (1986). Quantification of immunogold labelling reveals enrichment of glutamate in mossy and parallel fibre terminals in cat cerebellum. Neuroscience 19, 1045–1050.CrossRefGoogle ScholarPubMed
Somogyi, P. & Soltesz, I. (1986). Immunogold demonstration of GABA in synaptic terminals of intracellularly recorded, horseradish peroxidase-filled basket cells and cluth cells in the cat's visual cortex. Neuroscience 19, 1051–1065.CrossRefGoogle Scholar
Storck, T., Schulte, S., Hofmann, K. & Stoffel, W. (1992). Structure, expression, and functional analysis of a Na+-dependent glutamate/aspartate transporter from rat brain. Proceedings of the National Academy of Sciences of the U.S.A. 89, 10955–10959.CrossRefGoogle ScholarPubMed
Storm-Mathisen, J., Leknes, A.K., Bore, A.T., Vaaland, J.L., Edminson, P., Haug, F.M.S. & Ottersen, O.P. (1983). First visualization of glutamate and GABA in neurones by immunocytochem-istry. Nature 301, 517–520.CrossRefGoogle Scholar
Szentágothai, J., Hamori, J. & Tombol, T. (1966). Degeneration and electron microscope analysis of the synaptic glomeruli in the lateral geniculate body. Experimental Brain Research 2, 283–301.CrossRefGoogle ScholarPubMed
Tamura, H., Hicks, T.P., Hata, Y., Tsumoto, T. & Yamatodani, A. (1990). Release of glutamate and aspartate from the visual cortex of the cat following activation of afferent pathways. Experimental Brain Research 80, 447–455.CrossRefGoogle ScholarPubMed
Tieman, S.B., Cangro, C.B. & Neale, J.H. (1987). N-acetylaspartyl-glutamate immunoreactivity in neurons of the cat's visual system. Brain Research 420, 188–193.CrossRefGoogle Scholar
Tieman, S.B., Moffett, J.R. & Irtenkauf, S.M. (1991). Effect of eye removal on N-acetylaspartylglutamate immunoreactivity in retinal targets of the cat. Brain Research 562, 318–322.CrossRefGoogle ScholarPubMed
Tsai, G., Stauch, B.L., Vornov, J.J., Deshpande, J.K. & Coyle, J.T. (1990). Selective release of N-acetylaspartylglutamate from the rat optic nerve terminals in vivo. Brain Research 518, 313–316.CrossRefGoogle ScholarPubMed
Tsumoto, T, Masui, H. & Sato, H. (1986). Excitatory amino acid transmitters in neuronal circuits of the cat visual cortex. Journal of Neurophysiology 55, 469–483.CrossRefGoogle ScholarPubMed
Villanueva, S. & Orrego, F. (1988). Endogenous ligands for the quisqualate receptor: Presence in rat brain cortex synaptic vesicles. Brain Research 440, 363–365.CrossRefGoogle ScholarPubMed
Watkins, J.C. & Olverman, H.J. (1987). Agonists and antagonists for excitatory amino acid receptors. Trends in Neuroscience 10, 265–272.CrossRefGoogle Scholar
Wenthold, R.J. & Altschuler, R.A. (1983). Immunocytochemistry of aspartate aminotransferase and glutaminase. In Glutamine, Glutamate, and GABA in the Central Nervous System, ed. Hertz, L., Kvamme, E., McGeer, E.G. & Schousboe, A., pp. 33–50. New York: Alan R. Liss.Google Scholar
Wenthold, R.J. & Altschuler, R.A. (1986). Immunocytochemical localization of enzymes involved in the metabolism of excitatory amino acids. In Excitatory Amino Acids, ed. Roberts, P.J., Storm-Mathisen, J. & Bradford, H.F., pp. 85–100. London, England: MacMillan Press.CrossRefGoogle Scholar
Whittemore, E.R. & Koerner, J.F. (1989). An explanation for the purported excitation of piriform cortical neurons by N-acetyl-L-aspartyl-L-glutamic acid (NAAG). Proceedings of the National Academy of Sciences of the U.S.A. 86, 9602–9605.CrossRefGoogle ScholarPubMed
Wilkin, G.P., Garthwaite, J. & Balazs, R. (1982). Putative acidic amino acid transmitters in the cerebellum. II. Electron microscopic localization of transport sites. Brain Research 244, 69–80.CrossRefGoogle ScholarPubMed
Wilkinson, R.J. & Nicholls, D.G. (1989). Compartmentation of glutamate and aspartate within cerebral cortical synaptosomes: Evidence for a non-cytoplasmic origin for the calcium-releasable pool of glutamate. Neurochemistry International 15, 191–197.CrossRefGoogle ScholarPubMed
Yaqub, A. & Eldred, W.D. (1991). Localization of aspartate-like immunoreactivity in the retina of the turtle (Pseudemys scripta). Journal of Comparative Neurology 312, 584–598.CrossRefGoogle ScholarPubMed
Yingcharoen, K., Rinvtk, E., Storm-Mathisen, J. & Ottersen, O.P. (1989). GABA, glycine, glutamate, aspartate and taurine in the peri-hypoglossal nuclei. An immunocytochemical investigation in the cat with particular reference to the issue of amino acid colocalization. Experimental Brain Research 78, 345–357.CrossRefGoogle Scholar
Zhang, N., Walberg, F., Laake, J.H., Meldrum, B.S. & Ottersen, O.P. (1990). Aspartate-like and glutamate-like immunoreactivities in the inferior olive and climbing fibre system: A light microscopic and semiquantitative electron microscopic study in rat and baboon (Papio anubis). Neuroscience 38, 61–80.CrossRefGoogle ScholarPubMed