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Glutamate-like immunoreactivity in the cat superior colliculus and visual cortex: Further evidence that glutamate is the neurotransmitter of the corticocollicular pathway

Published online by Cambridge University Press:  02 June 2009

Chang-Jin Jeon ,
Michael K. Hartman  and
R. Ranney Mize
Chang-Jin Jeon
Affiliation:
Department of Anatomy and Neurobiology, University of Tennessee, Memphis
Michael K. Hartman
Affiliation:
Department of Anatomy and Neurobiology, University of Tennessee, Memphis
R. Ranney Mize
Affiliation:
Department of Anatomy and the Neuroscience Center, Louisiana State University Medical Center, New Orleans
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Abstract

Biochemical studies provide evidence that the pathway from visual cortex to the superior colliculus (SC) utilizes glutamate as a neurotransmitter. In the present study, we have used immunocytochemistry, visual cortex lesions, and retrograde tracing to show directly by anatomical methods that glutamate or a closely related analog is contained in corticocollicular neurons and terminals. A monoclonal antibody directed against gamma-L-glutamyl-L-glutamate (gamma glu glu) was used to localize glutamate-like immunoreactivity in both the superior colliculus (SC) and visual cortex (VC). Unilateral lesions of areas 17–18 were made in four cats to determine if gamma glu glu labeling was reduced in SC by this lesion. WGA-HRP was injected into the SC of 10 additional cats in order to determine if corticocollicular neurons were also labeled by the gamma glu glu antibody. A distinctive dense band of gamma glu glu immunoreactivity was found within the deep superficial gray and upper optic layers of SC where many corticotectal axons are known to terminate. Both fibers and cells were labeled within the band. Immunoreactivity was also found in cells and fibers throughout the deep layers of SC. Measures of total immunoreactivity (i.e. optical density) in the dense band were made in sections from the SC both ipsilateral to and contralateral to the lesions of areas 17–18. A consistent reduction in optical density was found in both the neuropil and in cells within the dense band of the SC ipsilateral to the lesion. A large percentage of all corticocollicular neurons that were retrogradely labeled by WGA-HRP also contained gamma glu glu. These results provide further evidence that the corticocollicular pathway in mammals is glutamatergic. The results also suggest that visual cortex ablation alters synthesis or storage of glutamate within postsynaptic SC neurons, presumably as a result of partial deafferentation.

Keywords

ImmunocytochemistryRetrograde tracingWGA-HRPGamma-L-glutamyl-L-glutamic acidImage analysis
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 1 , January 1997 , pp. 27 - 37
Copyright
Copyright © Cambridge University Press 1997

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References

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.Google Scholar
Baughman, R.W. & Gilbert, C.D. (1981). Aspartate and glutamate as possible neurotransmitters in the visual cortex. Journal of Neuroscience 1, 427–439.Google Scholar
Behan, M. (1984). An EM-autoradiographic analysis of the projection from cortical areas 17, 18, and 19 to the superior colliculus in the cat. Journal of Comparative Neurology 225, 591–604.CrossRefGoogle Scholar
Binns, K.E. & Salt, T.E. (1994). Excitatory amino acid receptors participate in synaptic transmission of visual responses in the superficial layers of the cat superior colliculus. European Journal of Neuroscience 6, 161–169.Google Scholar
Conti, F., Rustioni, A., Petrusz, P. & Towle, A.C. (1987). Glutamate-positive neurons in the somatic sensory cortex of rats and monkeys. Journal of Neuroscience 7, 1887–1901.CrossRefGoogle ScholarPubMed
Dori, I., Dinopoulos, A., Cavanagh, M.E. & Parnavelas, J.G. (1992). Proportion of glutamate- and aspartate-immunoreactive neurons in the efferent pathways of the rat visual cortex varies according to the target. Journal of Comparative Neurology 319, 191–204.CrossRefGoogle ScholarPubMed
Fonnum, F. (1984). Glutamate: A neurotransmitter in mammalian brain. Journal of Neurochemistry 42, 1–11.CrossRefGoogle ScholarPubMed
Fosse, V.M. & Fonnum, F. (1987). Biochemical evidence for glutamate and/or aspartate as neurotransmitters in fibers from the visual cortex to the lateral posterior thalamic nucleus (pulvinar) in rats. Brain Research 400, 219–224.CrossRefGoogle ScholarPubMed
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
Fosse, V.M., Kolstad, J. & Fonnum, F. (1986). A bioluminescence method for the measurements of L-glutamate: Application to the study of changes in the release of L-glutamate from lateral geniculate nucleus and superior colliculus after visual cortex ablation in rats. Journal of Neurochemistry 47, 340–349.CrossRefGoogle Scholar
Golladay, G.J., Butler, G.D., Tigges, M. & Mize, R.R. (1993). Monocular enucleation reduces GABA immunoreactivity in the lateral geniculate nucleus (LGN) of the Rhesus monkey. Investigative Ophthalmology and Visual Science (Suppl.) 34, 1172.Google Scholar
Hofbauer, A. & Hollander, H. (1986). Synaptic connections of cortical and retinal terminals in the superior colliculus of the rabbit: An electron microscopic double labeling study. Experimental Brain Research 65, 145–155.CrossRefGoogle Scholar
Huettner, J.E. & Baughman, R.W. (1988). The pharmacology of synapses formed by identified corticocollicular neurons in primary cultures of rat visual cortex. Journal of Neuroscience 8, 160–175.CrossRefGoogle ScholarPubMed
Jeon, C.-J., Gurski, M. & Mize, R.R. (1997). Glutamate containing neurons in the cat superior colliculus revealed by immunocytochemistry. Visual Neuroscience 14 (in press).CrossRefGoogle ScholarPubMed
Kvale, I., Fosse, V.M. & Fonnum, F. (1983). Development of neurotransmitter parameters in lateral geniculate body, superior colliculus and visual cortex of the albino rat. Developmental Brain Research 7, 137–145.CrossRefGoogle Scholar
Lund-Karlsen, R. & Fonnum, F. (1978). Evidence for glutamate as a neurotransmitter in the corticofugal fibres to the lateral geniculate body and the superior colliculus in rats. Brain Research 151, 457–467.CrossRefGoogle Scholar
Madl, J.E., Larson, A.A. & Beitz, A.J. (1986). Monoclonal antibody specific for carbodiimide-fixed glutamate: Immunocytochemical localization in the rat CNS. Journal of Histochemistry and Cytochemistry 34, 317–326CrossRefGoogle ScholarPubMed
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
Mize, R.R. (1983). Patterns of convergence and divergence of retinal and cortical synaptic terminals in the cat superior colliculus. Experimental Brain Research 51, 88–96.CrossRefGoogle ScholarPubMed
Mize, R.R. (1985). A microcomputer plotter for use with light and electron microscopes. In The Microcomputer in Cell Neurobiological Research, ed. Mize, R.R., pp. 111–133. New York: Elsevier Science Publishers.Google Scholar
Mize, R.R. (1989). The analysis of immunohistochemical data. In Computer Techniques in Neuroanatomy, ed. Capowski, J.J. pp. 333–372. New York: Plenum.CrossRefGoogle Scholar
Mize, R.R. (1994). Conservation of basic synaptic circuits that mediate GABA inhibition in the subcortical visual system. Progress in Brain Research 100, 123–132.CrossRefGoogle ScholarPubMed
Mize, R.R. & Butler, G.D. (1996 a). Postembedding immunocytochemistry demonstrates directly that both retinal and cortical terminals in the superior colliculus are glutamatergic. Journal of Comparative Neurology 371, 633–648.Google Scholar
Mize, R.R. & Butler, G.D. (1996 b). The n-methyl-d-aspartate receptor subunit NMDARI is localized at synaptic sites opposite both retinal and cortical terminals in the cat superior colliculus (in preparation).Google Scholar
Mize, R.R., Holdefer, R.N. & Nabors, B.L. (1988). Quantitative immunocytochemistry using an image analyzer. I. Hardware evaluation, image processing, and data analysis. Journal of Neuroscience Methods 26, 1–24.CrossRefGoogle ScholarPubMed
Mize, R.R., Luo, Q. & Tigges, M. (1992). Monocular enucleation reduces immunoreactivity to the calcium binding protein calbindin 28kD in the Rhesus monkey lateral geniculate nucleus. Visual Neuroscience 9, 471–482.CrossRefGoogle Scholar
Molnár, E., Baude, A., Richmond, S.A., Patel, P.B., Somogyi, P. & McIlhinney, R.A.J. (1993). Biochemical and immunocytochemical characterization of antipeptide antibodies to a cloned GluRl glutamate receptor subunit: Cellular and subcellular distribution in the rat forebrain. Neuroscience 53, 307–326.CrossRefGoogle Scholar
Monaghan, D.T. & Cotman, C.W. (1985). Distribution of N-melhyl-D-aspartate sensitive L-[3H]AMPA binding sites in rat brain as determined by quantitative autoradiography. Brain Research 324, 160–164.CrossRefGoogle Scholar
Nabors, L.B. & Mize, R.R. (1991). A unique neuronal organization in the cat pretectum revealed by antibodies to the calcium binding protein calbindin-D 28K. Journal of Neuroscience 11, 2460–2476.Google 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, 374–393.CrossRefGoogle ScholarPubMed
Petralia, R.S. & Wenthold, R.J. (1992). Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the brain. Journal of Comparative Neurology 318, 329–354.CrossRefGoogle Scholar
Petralia, R.S., Yokotani, N. & Wenthold, R.J. (1994). Light and electron microscope distribution of the NMDA receptor subunit NMDARI in the rat nervous system using a selective anti-peptide antibody. Journal of Neuroscience 14, 667–696.CrossRefGoogle Scholar
Sakurai, T. & Okada, Y. (1992). Selective reduction of glutamate in the rat superior colliculus and dorsal lateral geniculate nucleus after contralateral enucleation. Brain Research 513, 197–203.CrossRefGoogle Scholar
Sakurai, T., Miyamoto, T. & Okada, Y. (1990). Reduction of glutamate content in rat superior colliculus after retino-tectal denervation. Neuroscience Letters 109, 299–303.CrossRefGoogle ScholarPubMed
Sandberg, M. & Corazzi, L. (1983). Release of endogenous amino acids from superior colliculus of the rabbit: In vitro studies after retinal ablation. Journal of Neurochemistry 40, 917–921.CrossRefGoogle ScholarPubMed
Sandberg, M., Jacobson, I. & Hamberger, A. (1982). Release of endogenous amino acids in vitro from the superior colliculus and the hippocampus. Brain Research 55, 157–166.CrossRefGoogle ScholarPubMed
Sterling, P. (1971). Receptive fields and synaptic organization of the superficial gray layer of the cat superior colliculus. Vision Research (Suppl.) 3, 309–328.CrossRefGoogle Scholar
Straschill, M. & Perwein, J. (1971). Effect of iontophoretically applied biogenic amines and of cholinomimetic substance upon the activity of neurons in the superior colliculus and mesencephalic reticular formation of cat. Pflügers Archives 324, 43–55.CrossRefGoogle ScholarPubMed
Tigges, M. & Tigges, J. (1991). Parvalbumin immunoreactivity of the lateral geniculate nucleus in adult Rhesus monkeys after monocular eye enucleation. Visual Neuroscience 6, 375–382CrossRefGoogle ScholarPubMed
Tusa, R.J., Palmer, L.A. & Rosenquist, A.C. (1978). The retinotopic organization of area 17 (striate cortex) in the cat. Journal of Comparative Neurology 177, 213–236.Google Scholar
Tusa, R.J., Rosenquist, A.C. & Palmer, L.A. (1979). Retinotopic organization of areas 18 and 19 in the cat. Journal Comparative Neurology 185, 657–678.CrossRefGoogle Scholar