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Quantitative immunogold analysis reveals high glutamate levels in synaptic terminals of retino-geniculate, cortico-geniculate, and geniculo-cortical axons in the cat

Published online by Cambridge University Press:  02 June 2009

Vicente M. Montero
Vicente M. Montero
Affiliation:
Department of Neurophysiology, and Waisman Center, University of Wisconsin, Madison
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Abstract

A postembedding immunogold procedure was used to estimate quantitatively, at the electron-microscopical level, the intensity of glutamate (GLU) immunoreactivity in different identifiable profiles of the lateral geniculate nucleus (LGN) and perigeniculate nucleus (PGN) of the cat. Synaptic terminals of retinal and cortical origins in the LGN, and of axon collaterals of geniculo-cortical relay cells in the PGN, were identified by previously determined ultrastructural features. Processes of interneurons or relay cells were identified by being immunoreactive or non-immunoreactive, respectively, in serial thin section reacted with a GABA antibody.

The results showed that synaptic terminals of geniculo-cortical relay cells in the PGN have significantly higher levels of GLU immunoreactivity than their parent somata or dendrites in the LGN; this suggests transmitter storage of this amino acid in these terminals. By contrast, synaptic terminals of interneurons did not show enrichment of GLU relative to their parent somata. This argues against the possibility that the relative enrichment of GLU in relay cells terminals is due to factors other than presynaptic storage. In addition, axon collateral terminals of relay cells in the PGN, as well as retinal and cortical terminals in the LGN, showed significantly higher GLU immunoreactivity than GABAergic terminals. These immunocytochemical results suggest that GLU is a neurotransmitter in the retino-geniculate, cortico-geniculate, and geniculo-cortical pathways in the cat.

Keywords

GlutamateLateral geniculate nucleusPerigeniculate nucleusRetinaPostembedding immunogold
Type
Research Articles
Information
Visual Neuroscience , Volume 4 , Issue 5 , May 1990 , pp. 437 - 443
Copyright
Copyright © Cambridge University Press 1990

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References

Ahlsen, G., Grant, K. & Lindstrom, S. (1982). Monosynaptic excitation of principal cells in the lateral geniculate nucleus by corticofugal fibers. Brain Research 234, 454–458.CrossRefGoogle ScholarPubMed
Ahlsen, G. & Lindstrom, S. (1982). Excitation of perigeniculate neurones via axon collaterals of principal cells. Brain Research 236, 477–481.CrossRefGoogle ScholarPubMed
Ahlsen, G., Lindstrom, S. & Lo, F.S. (1980). Excitatory connections from different types of principal cells to perigeniculate neurones. Acta Physiologica Scandinavica 108, 49a.Google Scholar
Baughman, R.W. & Gilbert, C.D. (1980). Aspartate and glutamate as possible neurotransmitters of cells in layer 6 of the visual cortex. Nature 287, 848–850.CrossRefGoogle ScholarPubMed
Baughman, R.W. & Gilbert, C.D. (1981). Aspartate and glutamate as possible neurotransmitters in the visual cortex. Journal of Neuroscience 1, 427–439.CrossRefGoogle ScholarPubMed
Crunelli, V., Kelly, J.S., Lereche, N. & Pirchio, M. (1987). On the excitatory postsynaptic potential evoked by stimulation of the optic tract in the rat lateral geniculate nucleus. Journal of Physiology 384, 603–618.CrossRefGoogle ScholarPubMed
Cucchiaro, J.B., Uhlrich, D.J., Hamos, J.E. & Sherman, S.M. (1985). Perigeniculate input to the cat's lateral geniculate nucleus: a light- and electron-microscopic study of single, HRP-filled cells. Neuroscience Abstracts 11, 231.Google Scholar
Cucchiaro, J.B., Uhlrich, D.J. & Sherman, S.M. (1988). Parabrachial innervation of the cat's dorsal lateral geniculate nucleus: an electron-microscopic study using the tracer Phaseolus vulgaris Leucoagglutinin (PHA-L). Journal of Neuroscience 8, 4576–4588.CrossRefGoogle ScholarPubMed
De Lima, A.D., Montero, V.M. & Singer, W. (1985). The cholinergic innervation of the visual thalamus. Experimental Brain Research 59, 206–212.CrossRefGoogle ScholarPubMed
De Lima, A.D. & Singer, W. (1987a). The serotonergic fibers in the dorsal lateral geniculate nucleus of the cat: distribution and synaptic connections demonstrated with immunocytochemistry. Journal of Comparative Neurology 258, 339–351.CrossRefGoogle Scholar
De, Lima A.D. & Singer, W. (1987b). The brain-stem projection to the lateral geniculate nucleus in the cat: identification of cholinergic and monoaminergic elements. Journal of Comparative Neurology 259, 92–121.Google Scholar
Esguerra, M., Kwon, Y.H. & Sur, M. (1989). NMDA and non NMDA receptors mediate retinogeniculate transmission in cat and ferret LGN in vitro. Neuroscience Abstracts 15, 175.Google Scholar
Fitzpatrick, D., Diamond, I.T. & Raczkowski, D. (1989). Cholinergic and monoaminergic innervation of the cat's thalamus: comparison of the lateral geniculate nucleus with other principal sensory nuclei. Journal of Comparative Neurology 288, 647–675.CrossRefGoogle ScholarPubMed
Fitzpatrick, D., Penny, G.R. & Schmechel, D.E. (1984). Glutamic acid decarboxylase-immunoreactive neurons and terminals in the lateral geniculate nucleus of the cat. Journal of Neuroscience 4, 1809–1829.CrossRefGoogle ScholarPubMed
Fonnum, F. (1984). Glutamate: a neurotransmitter in mammalian brain. Journal of Neurochemistry 42, 1–11.CrossRefGoogle ScholarPubMed
Fonnum, F., Fosse, V.M. & Paulsen, R. (1986). The compartmentation and turnover of glutamate and GABA: a better understanding by the use of drugs. In Excitatory Amino Acids, ed. Roberts, P.J., Storm-Mathisen, J. & Bradford, H.F., pp. 67–83. London, England: Macmillan Press Ltd.CrossRefGoogle Scholar
Fosse, V.M., Heggelund, P., Iversen, E. & Fonnum, F. (1984). Effects of area 17 ablation on neurotransmitter parameters in efferents to area 18, the lateral geniculate body, pulvinar and superior colliculus in the cat. Neuroscience Letters 52, 323–328.CrossRefGoogle ScholarPubMed
Graybiel, A.M. (1978). A satellite system of the superior colliculus: the parabigeminal nucleus and its projections to the superficial collicular layers. Brain Research 145, 365–374.CrossRefGoogle Scholar
Guillery, R.W. (1969a). The organization of synaptic interconnections in the laminae of the dorsal lateral geniculate nucleus of the cat. Zeitschrift fur Zellforschung 96, 1–38.CrossRefGoogle ScholarPubMed
Guillery, R.W. (1969b). A quantitative study of synaptic interconnections in the dorsal lateral geniculate nucleus of the cat. Zeitschrift fur Zellforschung 96, 39–48.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
Heggelund, P. & Hartvett, E. (1989). Lagged and non-lagged X cells in the cat lateral geniculate nucleus receive retinal input through different glutamate receptors. Neuroscience Abstracts 15, 175.Google 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, E.G. & Powell, T.P.S. (1969). An electron-microscopic study of the mode of termination of cortico-thalamic fibres within the sensory relay nuclei of the thalamus. Proceedings of the Royal Society B (London) 172, 173–185.Google ScholarPubMed
Karlsen, R.L. & Fonnum, F. (1978). Evidence for glutamate as a neu rotransmitter in the corticofugal fibers to the dorsal lateral geniculate body and the superior colliculus in rats. Brain Research 151, 457–467.CrossRefGoogle Scholar
Kemp, J.A. & Sillito, 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
Kvaie, I. & Fonnum, F. (1983). The effects of unilateral removal of visual cortex on transmitter parameters in the adult superior colliculus and lateral geniculate body. Developmental Brain Research 11, 261–266.Google Scholar
Montero, V.M. (1986). Localization of γ-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. (1987). Ultrastructural identification of synaptic terminals from the axon of type 3 interneurons in the cat lateral geniculate nucleus. Journal of Comparative Neurology 264, 268–283.CrossRefGoogle ScholarPubMed
Montero, V.M. (1989a). The GABA-immunoreactive neurons in the interlaminar regions of the cat lateral geniculate nucleus: light- and electron-microscopic observations. Experimental Brain Research 75 497–512.CrossRefGoogle ScholarPubMed
Montero, V.M. (1989b). Ultrastructural identification of synaptic terminals from cortical axons and from collateral axons of geniculocortical relay cells in the perigeniculate nucleus of the cat. Experimental Brain Research 75, 65–72.CrossRefGoogle ScholarPubMed
Montero, V.M. (1989c). Quantitative immunogold analysis reveals high glutamate levels in axon collateral terminals of geniculo-cortical relay cells in the perigeniculate nucleus of the cat. Neuroscience Abstracts 15, 1393.Google Scholar
Montero, V.M. & Scott, G.L. (1981). Synaptic terminals in the dorsal lateral geniculate nucleus from neurons of the thalamic reticular nucleus: a light and electron microscope autoradiographic study. Neuroscience 6, 2561–2577.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
Ottersen, O. P. (1989). Quantitative electron-microscopic immunocytochemistry of neuroactive amino acids. Anatomy and Embryology 180, 1–15.CrossRefGoogle ScholarPubMed
Parent, A., Pare, D., Smith, Y. & Steriade, M. (1988). Basal forebrain cholinergic and noncholinergic projections to the thalamus and brain stem in cats and monkeys. Journal of Comparative Neurology 277, 281–301.CrossRefGoogle Scholar
Pasik, P., Pasik, T. & Holstein, G.R. (1988). Serotonin immunoreactivity in the monkey lateral geniculate nucleus. Experimental Brain Research 69, 662–666.CrossRefGoogle ScholarPubMed
Raczkowski, D. & Fitzpatrick, D. (1989). Organization of cholinergic synapses in the cat's dorsal lateral geniculate and perigeniculate nuclei. Journal of Comparative Neurology 288, 676–690.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
Smith, Y., Pare, D., Deschenes, M., Parent, A. & Steriade, M. (1988). Cholinergic and non-cholinergic projections from the upper brain-stem core to the visual thalamus in the cat. Experimental Brain Research 69, 1–15.Google Scholar
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. & Ottersen, O.P. (1986). Quantification of immunogold labeling reveals enrichment of glutamate in mossy and parallel fiber terminals in cat cerebellum. Neuroscience 19, 1045–1050.CrossRefGoogle ScholarPubMed
Somogyi, P. & Hodgson, A.J. (1985). Antisera to γ-aminobutyric acid, III: Demonstration of GABA in Golgi-impregnated neurons and in conventional electron-microscopic sections of cat striate cortex. Journal of Histochemistry and Cytochemistry 33, 249–257.CrossRefGoogle ScholarPubMed
Somogyi, P. & Soltesz, I. (1986). Immunogold demonstration of GABA in synaptic terminals of intracellularly recorded, horseradish peroxidase-filled basket cells and clutch cells in the cat's visual cortex. Neuroscience 19, 1050–1065.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 immunocytochemistry. Nature 301, 517–520.CrossRefGoogle ScholarPubMed
Szentagithai, 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.Google Scholar
Tomimoto, H., Kamo, H., Kameyama, M., Mcgeer, P.L. & Kimura, H. (1987). Descending projections of the basal forebrain in the rat demonstrated by the anterograde neural tracer Phaseolus vulgaris leucoagglutinin (PHA-L). Brain Research 425, 248–255.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
Watson, A.H.D. (1988). Antibodies against GABA and glutamate label neurons with morphologically distinct synaptic vesicles in the locust central nervous system. Neuroscience 26, 33–44.CrossRefGoogle ScholarPubMed
Weber, A.J. & Kalil, R.E. (1987). Development of corticogeniculate synapses in the cat. Journal of Comparative Neurology 264, 171–192.CrossRefGoogle ScholarPubMed
Wenthold, R., Zempel, J., Parakkal, M.H., Reeks, K.A. & Altschuler, R.A. (1986). Immunocytochemical localization of GABA in the cochlear nucleus of the guinea pig. Brain Research 380, 7–18.CrossRefGoogle ScholarPubMed
Wilson, J.R. & Hendrickson, A.E. (1988). Serotonergic axons in the monkey's lateral geniculate nucleus. Visual Neuroscience 1, 125–133.CrossRefGoogle ScholarPubMed