Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-24T15:26:19.689Z Has data issue: false hasContentIssue false
  • English
  • Français

Contribution of quisqualate/ kainate and NMDA receptors to excitatory synaptic transmission in the rat's visual cortex

Published online by Cambridge University Press:  02 June 2009

A. Nishigori ,
T. Tsumoto  and
F. Kimura
A. Nishigori
Affiliation:
Department of Neurophysiology, Biomedical Research Center, Osaka University Medical School, Kita-ku, Osaka 530, Japan
T. Tsumoto
Affiliation:
Department of Neurophysiology, Biomedical Research Center, Osaka University Medical School, Kita-ku, Osaka 530, Japan
F. Kimura
Affiliation:
Department of Neurophysiology, Biomedical Research Center, Osaka University Medical School, Kita-ku, Osaka 530, Japan
Get access Rights & Permissions [Opens in a new window]

Abstract

Actions of antagonists for excitatory amino-acid (EAA) receptors on extracellularly and intracellularly recorded responses of layer II/III cells to electrical stimulation of the underlying white matter were studied in a slice preparation of rat's visual cortex. Antagonists used were 2-amino-5-phosphonovalerate (APV) and 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX), which are selective antagonists for EAA receptors of N-methyl-D-aspartate (NMDA) and quisqualate/kainate (non-NMDA) type, respectively. In extracellular recordings, it was found that responses of almost all of the cells were suppressed by CNQX. In contrast, sensitivity to APV was different between cells with short- and long-latency responses; 81% of the former responses were not suppressed by APV, while about a half of the latter were suppressed. Excitatory postsynaptic potentials (EPSPs) evoked by white-matter stimulation were recorded intracellularly from 42 neurons. Most of polysynaptically elicited EPSPs were sensitive to APV, whereas the majority of monosynaptic EPSPs were not. CNQX almost completely suppressed EPSPs irrespective of monosynaptically or polysynaptically evoked, but in some cases slow EPSPs with low amplitude were spared. These CNQX-resistant EPSPs were elicited polysynaptically and had an anomalous voltage dependence, a characteristic of NMDA receptors. It is suggested that non-NMDA receptors contribute dominantly to first-order synaptic transmission while NMDA receptors participate substantially in second-order transmission so as to serve as a booster of outputs from visual cortex.

Keywords

Visual cortexExcitatory amino acidsNMDA receptorsQuisqualate/kainate receptorsRat
Type
Research Article
Information
Visual Neuroscience , Volume 5 , Issue 6 , December 1990 , pp. 591 - 604
Copyright
Copyright © Cambridge University Press 1990

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

Andreasen, M., Lambert, J.D.C. & Jensen, M.S. (1989). Effects of new non-N-methyl-D-aspartate antagonists on synaptic transmission in the in vitro rat hippocampus. Journal of Physiology (London) 414, 317–336.CrossRefGoogle ScholarPubMed
Artola, A. & Singer, W. (1987). Long-term potentiation and NMDA receptors in rat visual cortex. Nature 330, 649–652.CrossRefGoogle ScholarPubMed
Artola, A. & Singer, W. (1990). The involvement of N-methyl-D-aspartate receptors in induction and maintenance of long-term potentiation in rat visual cortex. European Journal of Neuroscience 2, 254–269.CrossRefGoogle ScholarPubMed
Aston-Jones, G., Shaver, R. & Dinan, T.G. (1985). Nucleus basalis neurons exhibit axonal branching with decreased impulse conduction velocity in rat cerebrocortex. Brain Research 325, 271–285.CrossRefGoogle ScholarPubMed
Baughman, R.W. & Gilbert, C.D. (1981). Aspartate and glutamate as possible neurotransmitters in the visual cortex. Journal of Neuroscience 1, 429–439.CrossRefGoogle ScholarPubMed
Bishop, P.O., Coombs, J.S. & Henry, G.H. (1973). Receptive fields of simple cells in the cat striate cortex. Journal of Physiology (London) 231, 31–60.CrossRefGoogle ScholarPubMed
Blake, J.F., Brown, M.W. & Collingridge, G.L. (1988). CNQX blocks acidic amino-acid-induced depolarization and synaptic components mediated by non-NMDA receptors in rat hippocampal slices. Neuroscience Letters 89, 182–186.CrossRefGoogle ScholarPubMed
Bullier, J. & Henry, G.H. (1979). Ordinal position of neurons in cat striate cortex. Journal of Neurophysiology 42, 1251–1270.CrossRefGoogle ScholarPubMed
Bullier, J., McCourt, M.S. & Henry, G.H. (1988). Physiological studies on the feedback connection to the striate cortex from cortical areas 18 and 19 of the cat. Experimental Brain Research 70, 90–98.CrossRefGoogle Scholar
Burkhalter, A. (1989). Intrinsic connections of rat primary visual cortex: laminar organization of axonal projections. Journal of Comparative Neurology 279, 171–186.CrossRefGoogle ScholarPubMed
Burne, R.A., Parnavelas, J.G. & Lin, C.-S (1984). Response properties of neurons in the visual cortex of the rat. Experimental Brain Research 53, 374–383.CrossRefGoogle ScholarPubMed
Clark, R.M. & Collins, G.G.S. (1975). The release of endogenous amino acids from the rat visual cortex. Journal of Physiology (London) 263, 383–400.Google Scholar
Cleland, B.G. & Lee, B.B. (1985). A comparison of visual responses of cat lateral gemculate nucleus neurones with those of ganglion cells afferent to them. Journal of Physiology (London) 369, 249–268.CrossRefGoogle Scholar
Creutzfeldt, O.D. & Ito, M (1968). Functional synaptic organization of primary visual cortex neurons in the cat. Experimental Brain Research 6, 324–352.CrossRefGoogle ScholarPubMed
Davies, J. & Francis, A.A., Jones, A.W. & Watkins, J.C. (1981). 2-amino-5-phosphonovalerate (APV), a potent and selective antagonist of amino-acid-induced and synaptic excitation. Neuroscience Letters 21,77–81.CrossRefGoogle Scholar
Drejer, J. & Honoré, T. (1988). New quinoxalinediones show potent antagonism of quisqualate responses in cultured mouse cortical neurons. Neuroscience Letters 87, 104–108.CrossRefGoogle ScholarPubMed
Fletcher, E.J., Martin, D., Aran, J.A. & Honoré, T. (1989). Quinoxalinediones selectively block quisqualate and kainate receptors and synaptic events in rat neocortex and hippocampus and frog spinal cord in vitro. British Journal of Pharmacology 95, 585–597.CrossRefGoogle Scholar
Forsythe, I.D. & Westbrook, G.L. (1988). Slow excitatory postsynaptic currents mediated by N-methyl-D-aspartate receptors on cultured mouse central neurones. Journal of Physiology (London) 396, 515–533.CrossRefGoogle ScholarPubMed
Fox, K., Sato, H. & Daw, N. (1989). The location and function of NMDA receptors in cat and kitten visual cortex. Journal of Neuroscience 9, 2443–2454.CrossRefGoogle Scholar
Gilbert, C.D. (1983). Microcircuitry of the visual cortex. Annual Review of Neuroscience 6, 217–247.CrossRefGoogle ScholarPubMed
Guedes, R., Watanabe, S. & Creutzfeldt, O.D. (1983). Functional role of association fibers for a visual association area: the posterior suprasylvian sulcus of the cat. Experimental Brain Research 49, 13–27.CrossRefGoogle ScholarPubMed
Hablitz, J.J. & Langmoen, I.A. (1986). N-methyl-D-aspartate receptor antagonists reduce synaptic excitation in the hippocampus. Journal of Neuroscience 6, 102–106.CrossRefGoogle ScholarPubMed
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
Henderson, Z. (1981). A projection from acetylcholine esterase containing neurons in the diagonal band to the occipital cortex of the rat. Neuroscience 6, 1081–1088.CrossRefGoogle Scholar
Hicks, T.P. (1987). Excitatory amino-acid pathways in cerebral cortex. In Excitatory Amino Acid Transmission, ed. Hicks, T.P., Lodge, D. & McLennan, H., pp. 373–380. New York: Alan R. Liss.Google Scholar
Honoré, T., Davies, S.N., Drejer, J., Fletcher, E.J., Jacobson, P., Lodge, D. & Nielsen, F.E. (1988). Quinoxalinediones: potent competitive non-NMDA glutamate receptor antagonists. Science 241, 701–703.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1962). Receptive fields, binocular interaction, and functional architecture in the cat's visual cortex. Journal of Physiology (London) 160, 106–154.CrossRefGoogle ScholarPubMed
Jones, K.A. & Baughman, R.W. (1988). NMDA- and non-NMDA receptor components of excitatory synaptic potentials recorded from cells in layer V of rat visual cortex. Journal of Neuroscience 8, 3522–3534.CrossRefGoogle Scholar
Kimura, F., Nishigori, A., Shirokawa, T. & Tsumoto, T. (1989). Longterm potentiation and N-methyl-D-aspartate receptors in the visual cortex of young rats. Journal of Physiology (London) 414, 125–144.CrossRefGoogle ScholarPubMed
Kleinschmidt, A., Bear, M.F. & Singer, W. (1987). Blockade of “NMDA” receptors disrupts experience-dependent plasticity of kitten striate cortex. Science 238, 355–358.CrossRefGoogle ScholarPubMed
Krieg, W.J.S. (1946). Connections of the cerebral cortex, I: The albino rat. A topography of the cortical area. Journal of Comparative Neurology 84, 221–275.CrossRefGoogle Scholar
Macdonald, J.F., Porietis, A.V. & Wojtowicz, J.M. (1982). L-aspartic acid induces a region of negative slope conductance in the current-voltage relationship of cultured spinal cord neurons. Brain Research 237, 248–253.CrossRefGoogle ScholarPubMed
Mayer, M.L. & Westbrook, G.L. (1985). The action of N-methyl-Daspartic acid on mouse spinal neurones in culture. Journal of Physiology (London) 361, 65–90CrossRefGoogle Scholar
Mayer, M.L. & Westbrook, G.L. (1987). The physiology of excitatory amino acids in the vertebrate central nervous system. Progress in Neurobiology 28, 197–276.CrossRefGoogle ScholarPubMed
Miller, K.D., Chapman, B. & Stryker, M.P. (1989). Visual responses in adult cat visual cortex depend on N-methyl-D-aspartate receptors. Proceedings of National Academy of Science of the U.S.A. 86, 5183–5187.CrossRefGoogle ScholarPubMed
Nakamura, S. (1977). Some electrophysiological properties of neurons of rat locus coeruleus. Journal of Physiology (London) 267, 641–658.CrossRefGoogle ScholarPubMed
Neuman, R.S., Ben-Ari, Y., Gho, M. & Cherubini, E. (1988). Blockade of excitatory synaptic transmission by 6-cyano-7-nitroquinox- aline-2,3-dione (CNQX) in the hippocampus in vitro. Neuroscience Letters 92, 64–68.CrossRefGoogle ScholarPubMed
Nishigori, A., Kimura, F. & Tsumoto, T. (1990). Contribution of non NMDA and NMDA receptors to excitatory synaptic transmission in the rat's visual cortex. Neuroscience Research (Suppl. 11), 106.Google Scholar
Nowak, L., Bregestovski, P., Ascher, P., Herbet, A. & Prochiantsz, A. (1984). Magnesium gate glutamate-activated channels in mouse central neurones. Nature 307, 462–465.CrossRefGoogle ScholarPubMed
Parnavelas, J.G., Lieberman, A.R. & Webster, K.E. (1977). Organization of neurons in the visual cortex, area 17, of the rat. Journal of Anatomy 124, 305–322.Google ScholarPubMed
Perkins, M.N. & Stone, T.W. (1982). An iontophoretic investigation of the actions of convulsant kynurenines and their interaction with the endogenous excitant quinolinic acid. Brain Research 247, 184–187.CrossRefGoogle ScholarPubMed
Peters, A. (1985). The visual cortex of the rat. In Cerebral Cortex, Vol. 3: Visual Cortex, ed. Peters, A. & Jones, E.G., pp. 19–80. New York and London: Plenum Press.Google Scholar
Peters, A. & Feldman, M.L. (1976). The projection of the lateral geniculate nucleus to area 17 of the rat cerebral cortex, I: General description. Journal of Neurocytology 5, 63–84.CrossRefGoogle ScholarPubMed
Peters, A., Proskauer, C.G., Feldman, M.L. & Kiemerer, L.(1979). The projection of the lateral geniculate nucleus to area 17 of the rat cerebral cortex, V: Degenerating terminals synapsing with Golgi-impregnated neurons. Journal of Neurocytology 8, 331–357.CrossRefGoogle ScholarPubMed
Pettigrew, J.D., Nikara, T. & Bishop, P.O. (1968). Responses to moving slits by single units in cat striate cortex. Experimental Brain Research 6, 373–390.Google ScholarPubMed
Sherman, S.M., Watkins, D.W. & Wilson, J.R. (1976). Further differences in receptive-field properties of simple and complex cells in catstriate cortex. Vision Research 16, 919–927.CrossRefGoogle Scholar
Shirokawa, T., Nishigori, A., Kimura, F. & Tsumoto, T. (1989). Actions of excitatory amino-acid antagonists on synaptic potentials of layer II/III neurons of the cat's visual cortex. Experimental Brain Research 78, 489–500.CrossRefGoogle ScholarPubMed
Singer, W., Tretter, F. & Cynader, M. (1975). Organization of cat striate cortex: a correlation of receptive-field properties with afferent and efferent connections. Journal of Neurophysiology 37, 1080–1098.CrossRefGoogle Scholar
Swadlow, H.A. & Waxman, S.G. (1976). Variations in conduction velocity and excitability following single and multiple impulses of visual callosal axons in the rabbit. Experimental Neurology 53, 128–150.CrossRefGoogle ScholarPubMed
Szentagothai, J. (1973). Synaptology of the visual cortex. In Central Processing of Visual Information. Handbook of Sensory Physiology, Vol. III/3, Part B, ed. Jung, R. pp. 270–324. New York: Springer-Verlag.Google Scholar
Tamura, H., Hicks, T.P., Hata, Y., Tsumoto, T. & Yamatodani, A. (1990). Release of glutamate and aspartate from visual cortex of the cat following activation of afferent pathways. Experimental Brain Research 80, 447–455.CrossRefGoogle ScholarPubMed
Thomson, A.M. (1986). A magnesium-sensitive postsynaptic potential in rat cerebral cortex resembles neuronal responses to Nmethylaspartate. Journal of Physiology (London) 370, 531–549.CrossRefGoogle ScholarPubMed
Toyama, K., Matsunami, K., Ohno, T. & Tokashiki, S. (1974). An intracellular study of neuronal organization in the visual cortex. Experimental Brain Research 21, 45–66.CrossRefGoogle ScholarPubMed
Tsumoto, T. (1990). Excitatory amino-acid transmitters and their receptors in neural circuits of the cerebral neocortex. Neuroscience Research (in press).CrossRefGoogle Scholar
Tsumoto, T., Hagihara, K., Sato, H. & Hata, Y. (1987). NMDA receptors in the visual cortex of young kittens are more effective than those of adult cats. Nature 327, 513–514.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
Tsumoto, T. & Suda, K. (1982). Laminar difference in development of afferent innervation to striate cortex neurons in kittens. Experimental Brain Research 45, 433–446.CrossRefGoogle ScholarPubMed
Watkins, J.C. & Evans, R.H. (1981). Excitatory amino-acid transmitters. Annual Review of Pharmacology and Toxicology 21, 165–204.CrossRefGoogle ScholarPubMed
Yamada, K.A., Dubinsky, J.M. & Rothman, S.M. (1989). Quantitative physiological characterization of a quinoxalinedione non-NMDA receptor antagonist. Journal of Neuroscience 9, 3230–3236.CrossRefGoogle ScholarPubMed
Yamamoto, C. & McIlwain, H. (1966). Electrical activities in the sections from the mammalian brain maintained in chemically defined media in vitro. Journal of Neurochemistry 13, 1333–1343.CrossRefGoogle ScholarPubMed