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An in vitro study of retinotectal transmission in the chick: Role of glutamate and GABA in evoked field potentials

Published online by Cambridge University Press:  02 June 2009

J. C. Dye  and
H. J. Karten
J. C. Dye
Affiliation:
Department of Neurosciences, University of California-San Diego, La Jolla
H. J. Karten
Affiliation:
Department of Neurosciences, University of California-San Diego, La Jolla
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Abstract

We have developed two brain slice preparations for studying tectofugal visual pathways in the chick: conventional, 400-μm slices (“thin slices”), and “thick slices” which encompass the rostral pole of the optic tectum and the contralateral optic nerve. Stimulation was delivered with a bipolar electrode positioned in stratum opticum in thin slices and in the contralateral optic nerve in thick slices. While the latter preparation provided a means of exclusively and unambiguously activating retinal afferents, several lines of evidence also indicated that the evoked field potentials in thin slices were chiefly consequent to retinal afferent excitation: (1) the similarity of evoked field potentials in thin slices to those in thick slice preparations; (2) their precise localization in retinorecipient layers as shown by prelabeling from retina with FITC-coupled cholera toxin; (3) transmission delays appropriate for retinal afferents as established with the thick slice preparation; (4) patterns of labeled afferents resulting from applications of Dil crystals to slices fixed after recording; and (5) the similarity in transmitter pharmacology between thin and thick slice preparations. Pharmacological manipulations carried out with bath-applied antagonists indicated that glutamate is the principal retinotectal transmitter. The broadly active glutamate receptor blocker, kynurenic acid, reversibly eliminated the postsynaptic component of the field potential as confirmed with 0 Ca2+ saline. A complete block was also effected by the non-NMDA antagonists CNQX and DNQX. The specific NMDA antagonist, APS, caused a smaller and variable reduction in response amplitude. The GABA antagonist, bicuculline, caused a prolongation of the monosynaptic field epsp in retinorecipient layers and an enhancement of the long-latency, negative wave in cellular layers below, supporting a late, excitation-limiting role for this inhibitory transmitter.

Keywords

ChickOptic tectumRetinal ganglion cellSynaptic transmissionBrain sliceField potentialGlutamateGABA
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 4 , July 1996 , pp. 747 - 758
Copyright
Copyright © Cambridge University Press 1996

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References

Acheson, D.W.K., Kemplay, S.K. & Webster, K.E. (1980). Quantitative analysis of optic terminal profile distribution within the pigeon optic tectum. Neuroscience 5, 1067–1084.CrossRefGoogle ScholarPubMed
Angaut, P. & Repérant, J. (1976). Fine structure of the optic fibre termination layers in the pigeon optic tectum: A Golgi and electron microscope study. Neuroscience 1, 93–105.CrossRefGoogle ScholarPubMed
Bagnoli, P., Francesconi, W. & Magni, F. (1977). Visual Wulst influences on the optic tectum of the pigeon. Brain, Behavior, and Evolution 14, 217–237.Google ScholarPubMed
Barth, R. & Felix, D. (1974). Influence of GABA and glycine and their antagonists on inhibitory mechanisms of pigeon's optic tectum. Brain Research 80, 532–537.CrossRefGoogle ScholarPubMed
Bilge, M. (1971). Electrophysiological investigations on the pigeon optic tectum. Quarterly Journal of Experimental Physiology 56, 242–249.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 Neuroscieiice 6, 161–169.CrossRefGoogle ScholarPubMed
Bondy, S.C. & Purdy, J.L. (1977). Putative neurotransmitters of the avian visual pathway. Brain Research 119, 417–426.CrossRefGoogle ScholarPubMed
Canzek, V., Wolfensberger, M., Amsler, U. & Cuénod, M. (1981). In vivo release of glutamate and aspartate following optic nerve stimulation. Nature 293, 572–574.CrossRefGoogle ScholarPubMed
Cline, H.T., McDonald, J.W. & Constantine-Paton, M. (1994). Glutamate receptor binding in juvenile and adult Rana pipiens CNS. Journal of Neurobiology 25, 488–502.CrossRefGoogle ScholarPubMed
Cragg, B.G., Evans, D.H.L. & Hamlyn, L.H. (1954). The optic tectum of Gallus domesticus. A correlation of the electrical responses with the hislological structure. Journal of Anatomy 88, 292–310.Google ScholarPubMed
Crossland, W.J. (1981). Plasticity in the chick ventral lateral geniculate nucleus. Journal of Comparative Neurology 203, 671–683.CrossRefGoogle ScholarPubMed
Frost, B.J. (1978). Moving background patterns alter directionally specific responses of pigeon tectal neurons. Brain Research 151, 599–603.CrossRefGoogle ScholarPubMed
Frost, B.J. & DiFranco, D.E. (1976). Motion characteristics of single units in the pigeon optic tectum. Vision Research 16, 1229–1234.CrossRefGoogle ScholarPubMed
Frost, B.J. & Nakayama, K. (1983). Single visual neurons code opposing motion independent of direction. Science 220, 744–745.CrossRefGoogle ScholarPubMed
Guiloff, G.D., Maturana, H.R. & Varela, F.J. (1987). Cytoarchitecture of the avian ventral lateral geniculate nucleus. Journal of Comparative Neurology 264, 509–526.CrossRefGoogle ScholarPubMed
Hamdi, F.A. & Whitteridge, D. (1954). The representation of the retina on the optic tectum of the pigeon. Quarterly Journal of Experimental Physiology 39, 111–119.CrossRefGoogle ScholarPubMed
Hardy, O., Leresche, N. & Jassik-Gerschenfeld, D. (1984). Post-synaplic potentials in neurons of the pigeon's optic tectum in response to afferent stimulation from the retina and other visual structures: An intracellular study. Brain Research 311, 65–74.CrossRefGoogle ScholarPubMed
Hardy, O., Leresche, N. & Jassik-Gerschenfeld, D. (1985). Morphology and laminar distribution of electrophysiologically identified cells in the pigeon's optic tectum: An intracellular study. Journal of Comparative Neurology 233, 390–404.CrossRefGoogle ScholarPubMed
Hayes, B.P. & Webster, K.E. (1975). An electron microscope study of the retino-receptive layers of the pigeon's optic tectum. Journal of Comparative Neurology 162, 447–466.CrossRefGoogle Scholar
Henke, H. & Fonnum, F. (1976). Topographical and subcellular distribution of choline acetyltransferase and glutamate decarboxylase in pigeon optic tectum. Journal of Neurochemistry 27, 387–391.CrossRefGoogle ScholarPubMed
Henke, H., Schenker, T.M. & Cuénod, M. (1976). Effects of retinal ablation on uptake of glutamate, glycine, GABA, proline and choline in pigeon tectum. Journal of Neurochemistry 26, 131–134.CrossRefGoogle ScholarPubMed
Hickmott, P.W. & Constantine-Paton, M. (1993). The contributions of NMDA, non-NMDA. and GABA receptors to postsynaptic responses in neurons of the optic tectum. Journal of Neuroscience 13, 4339–4353.CrossRefGoogle ScholarPubMed
Hodos, W. & Karten, H.J. (1974). Visual intensity and pattern discrimination deficits after lesions of the optic lobe in pigeons. Brain, Behavior, and Evolution 9, 165–194.Google ScholarPubMed
Holden, A.L. (1968). The field potential profile during activation of the avian optic tectum. Journal of Physiology (London) 194, 75–90.CrossRefGoogle ScholarPubMed
Hughes, C.P. & Pearlman, A.L. (1974). Single unit receptive fields and the cellular layers of the pigeon optic tectum. Brain Research 80, 365–377.CrossRefGoogle ScholarPubMed
Hunt, S.P. & Kunzle, H. (1976 a). Observations on the projections and intrinsic organization of the pigeon optic tectum: An autoradiographic study based on anterograde and retrograde, axonal and dendritic flow. Journal of Comparative Neurology 170, 153–172.CrossRefGoogle ScholarPubMed
Hunt, S.P. & Kunzle, H. (1976 b). Selective uptake and transport of label within three identified neuronal systems after injection of 3H-GABA into the pigeon optic tectum: An autoradiographic and Golgi study. Journal of Comparative Neurology 170, 173–190.CrossRefGoogle ScholarPubMed
Jarvis, C.D. (1974). Visual discrimination and spatial localization deficits after lesions of the tectofugal pathway in pigeons. Brain, Behavior, and Evolution 9, 195–228.Google ScholarPubMed
Jassik-Gerschenfeld, D. & Guichard, J. (1972). Visual receptive fields of single cells in the pigeon's optic tectum. Brain Research 40, 303–317.CrossRefGoogle ScholarPubMed
Joseph, K.C., Kim, S.U., Stieber, A. & Gonatas, N.K. (1978). Endocytosis of cholera toxin into neuronal GERL. Proceedings of the National Academy of Sciences of the U.S.A. 76, 2815–2819.CrossRefGoogle Scholar
Langdon, R.B. & Freeman, J.A. (1986). Antagonists of glutaminergic neurotransmission block retinotectal transmission in goldfish. Brain Research 398, 169–174.CrossRefGoogle ScholarPubMed
LaVail, J.H. & Cowan, W.M. (1971). The development of the chick optic tectum. I. Normal morphology and cytoarchitectonic development. Brain Research 28, 391–419.CrossRefGoogle ScholarPubMed
Luppi, P.-H., Fort, P. & Jouvet, M. (1990). lontophoretic application of unconjugated cholera toxin B subunit (Ctb) combined with immunohistochemistry of neurochemical substances: A method for transmitter identification of retrogradely labeled neurons. Brain Research 534, 209–224.CrossRefGoogle Scholar
Matsumoto, N., Kiyama, H. & Bando, T. (1983). An intracellular study of the optic tectum of the carp in vitro. Neuroscience Letters 38, 17–22.CrossRefGoogle ScholarPubMed
Mitzdorf, U. (1985). Current source-density method and application in cat cerebral cortex: Investigation of evoked potentials and EEG phenomena. Physiological Reviews 65, 37–100.CrossRefGoogle ScholarPubMed
Miyamoto, T., Sakurai, T. & Okada, Y. (1990). Masking effect of NMDA receptor antagonists on the formation of long-term potentiation (LTP) in superior colliculus slices from the guinea pig. Brain Research 518, 166–172.CrossRefGoogle ScholarPubMed
Mori, S. (1973). Analysis of field response in optic tectum of the pigeon. Brain Research 54, 193–206.CrossRefGoogle ScholarPubMed
Nistri, A., Sivilotti, L. & Welsh, D.M. (1990). An electrophysiological study of the action of N-methyl-D-aspartate on excitatory synaptic transmission in the optic tectum of the frog in vitro. Neuropharmacology 29, 681–687CrossRefGoogle ScholarPubMed
O'Flaherty, J.J. (1970). A Golgi analysis of the tectum of the mallard duck. Journal fur Hirnforschung 12, 389–404.Google ScholarPubMed
O'Flaherty, J.J. (1971). The optic nerve of the Mallard duck: Fibrediameter frequency distribution and physiological properties. Journal of Comparative Neurology 143, 17–24.CrossRefGoogle Scholar
Okada, E., Maeda, T. & Watanabe, T. (1982). Immunocytochemical study on cholera toxin binding sites by monoclonal anti-cholera toxin antibody in neuronal tissue culture. Brain Research 242, 233–241.CrossRefGoogle Scholar
O'Leary, J.L. & Bishop, G.H. (1943). Analysis of potential sources in the optic lobe of duck and goose. Journal of Cellular and Comparative Physiology 22, 73–87.CrossRefGoogle Scholar
Peters, J.J., Vonderahe, A.R. & Powers, T.H. (1958). Electrical studies of functional development of the eye and optic lobes in the chick embryo. Journal of Experimental Zoology 139, 459–468.CrossRefGoogle Scholar
Ramón y Cajal, S. (1891). Sur la fine structure du lobe optique des oiseaux et sur l'origine reelle des nerfs optiques. Journal International d'Anatomie et de Physiologie 8, 337–366.Google Scholar
Ramón y Cajal, S. (1911). Histologie de Systeme Nerveux de l'Homme et des Vertebres. Paris: Maloine.Google Scholar
Repérant, J. (1973). Nouvelles donnees sur les projections visuelles chez le pigeon (Columba livia). Journal fur Hirnforschung 14, 151–187.Google Scholar
Repérant, J. & Angaut, P. (1977). The retinotectal projections in the pigeon. An experimental optical and electron microscope study. Neuroscience 2, 119–140.CrossRefGoogle ScholarPubMed
Roberts, W.A., Eaton, S.A. & Salt, T.E. (1991). Excitatory amino acid receptors mediate synaptic responses to visual stimuli in superior colliculus neurones of the rat. Neuroscience Letters 129, 161–164.CrossRefGoogle ScholarPubMed
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
Sakurai, T. & Okada, Y. (1992). Selective reduction of glutamate in rat superior colliculus and dorsal lateral geniculate nucleus after contralateral enucleation. Brain Research 573, 197–203.CrossRefGoogle ScholarPubMed
Stone, J. & Freeman, J.A. (1971). Synaptic organization of the pigeon's optic tectum: A Golgi and current source-density analysis. Brain Research 27, 203–221.CrossRefGoogle ScholarPubMed