Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-28T20:49:03.309Z Has data issue: false hasContentIssue false

Retinogeniculate EPSPs recorded intracellularly in the ferret lateral geniculate nucleus in vitro: Role of NMDA receptors

Published online by Cambridge University Press:  02 June 2009

Manuel Esguerra
Affiliation:
Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge
Young H. Kwon
Affiliation:
Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge
Mriganka Sur
Affiliation:
Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge

Abstract

We used an in vitro preparation of the ferret lateral geniculate nucleus (LGN) to examine the role of the NMDA class of excitatory amino acid (EAA) receptors in retinogeniculate transmission. Intracellular recordings revealed that blockade of NMDA receptors both shortened the time course and reduced the amplitude of fast and slow components of excitatory postsynaptic potentials (EPSPs) evoked by optic tract stimulation. The amplitude and width of the EPSPs mediated by NMDA receptors increased as membrane potential was depolarized towards spike threshold. Individual LGN cells were influenced to varying extents by blockade of NMDA receptors; NMDA and non-NMDA receptor blockade together attenuated severely the entire retinogeniculate EPSP. The dependence of all components of retinogeniculate EPSPs (and action potentials) on NMDA receptor activation supports the hypothesis that the NMDA receptor participates in fast (<10 ms) synaptic events underlying conventional retinogeniculate transmission. The voltage dependence of the NMDA receptor-gated conductance suggests strongly that the transmission of retinal information through the LGN is subject to modulation by extraretinal inputs that affect the membrane potential of LGN neurons.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1992

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

Artola, A. & Singer, W. (1987). Long-term potentiation and NMDA receptors in rat visual cortex. Nature 330, 649652.CrossRefGoogle ScholarPubMed
Bloomfield, S.A., Hamos, J.E. & Sherman, S.M. (1987). Passive cable properties and morphological correlates of neurones in the lateral geniculate nucleus of the cat. Journal of Physiology 383, 653692.CrossRefGoogle ScholarPubMed
Claps, A. & Casagrande, V.A. (1990). The distribution and morphology of corticogeniculate axons in ferrets. Brain Research 530, 126129.CrossRefGoogle ScholarPubMed
Cline, H.T., Debski, E.A. & Constantine-Paton, M. (1987). N-methyl-D-aspartate antagonist desegregates eye-specific stripes. Proceedings of the National Academy of Sciences of the U.S.A. 84, 43424345.CrossRefGoogle ScholarPubMed
Coan, E.J. & Collingridge, G.L. (1987). Characterization of an N-methyl-D-aspartate receptor component of synaptic transmission in rat hippocampal slices. Neuroscience 22, 18.CrossRefGoogle ScholarPubMed
Coleman, P.A. & Miller, R.F. (1988). Do N-methyl-D-aspartate receptors mediate synaptic responses in the mudpuppy retina? Journal of Neuroscience 8, 47284733.CrossRefGoogle ScholarPubMed
Connors, B.W., Gutnick, M.J. & Prince, A.A. (1982). Electrophysiological properties of neocortical neurons in vitro. Journal of Neurophysiology 48, 13021320.CrossRefGoogle ScholarPubMed
Crunelli, V., Kelly, J.S., Leresche, N. & Pirchio, M. (1987). On the excitatory post-synaptic potential evoked by stimulation of the optic tract in the rat lateral geniculate nucleus. Journal of Physiology 384, 603618.CrossRefGoogle ScholarPubMed
Deschenes, M., Paradis, M., Roy, J.P. & Steriade, M. (1984). Electrophysiology of neurones of lateral thalamic nuclei in cat: Resting properties and burst discharges. Journal of Neurophysiology 51, 11961219.CrossRefGoogle ScholarPubMed
Dingledine, R. (1986). NMDA receptors: What do they do? Trends in Neuroscience 9, 4749.CrossRefGoogle Scholar
Esguerra, M., Kwon, Y.H. & Sur, M. (1989). NMDA and non-NMDA receptors mediate retinogeniculate transmission in cat and ferret LGN in vitro. Society for Neuroscience Abstracts 15, 175.Google Scholar
Escubrra, M., Roe, A.W. & Sur, M. (1987). Morphology of identified ferret LGN neurons characterized in vivo and in vitro. Society for Neuroscience Abstracts 13, 1434.Google Scholar
Esguerra, M. & Sur, M. (1990). Corticogeniculate feedback gates retinogeniculate transmission by activating NMDA receptors. Society for Neuroscience Abstracts 16, 159.Google Scholar
Fox, K., Sato, H. & Daw, N. (1990). The effect of varying stimulus intensity on NMDA-receptor activity in cat visual cortex. Journal of Neurophysiology 64, 14131428.CrossRefGoogle ScholarPubMed
Friedlander, M.J., Lin, C.-S., Stanford, L.R. & Sherman, S.M. (1981). Morphology of functionally identified neurons in lateral geniculate nucleus of the cat. Journal of Neurophysiology 46, 80129.CrossRefGoogle ScholarPubMed
Hahm, J., Langdon, R.B. & Sur, M. (1991). Disruption of retinogeniculate afferent segregation by antagonists to NMDA receptors. Nature 351, 568570.CrossRefGoogle ScholarPubMed
Hartveit, E. & Heggelund, P. (1990). Neurotransmitter receptors mediating excitatory input to cells in the cat lateral geniculate nucleus. II. Nonlagged cells. Journal of Neurophysiology 63, 13611372.CrossRefGoogle ScholarPubMed
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, 13471360.CrossRefGoogle ScholarPubMed
Hernandez-Cruz, A. & Pape, H.-C. (1989). Identification of two calcium currents in acutely dissociated neurons from the rat lateral geniculate nucleus. Journal of Neurophysiology 6, 12701283.CrossRefGoogle Scholar
Humphrey, A.L. & Weller, R.E. (1988). Structural correlates of functionally distinct X-cells in the lateral geniculate nucleus of the cat. Journal of Comparative Neurology 268, 448468.CrossRefGoogle ScholarPubMed
Jahnsen, H. & Llinas, R. (1984). Electrophysiological properties of guineapig thalamic neurones: An in vitro study. Journal of Physiology 349, 205226.CrossRefGoogle ScholarPubMed
Kauer, J.A., Malenka, R.C. & Nicoll, R.A. (1988). A persistent post-synaptic modification mediates long-term potentiation in the hippocampus. Neuron 1, 911917.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, 377391.CrossRefGoogle Scholar
Koch, C. (1985). Understanding the intrinsic circuitry of the cat's lateral geniculate nucleus: Electrical properties of the spinetriad arrangement. Proceedings of the Royal Society (London) 225, 365390.Google 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, 414428.CrossRefGoogle ScholarPubMed
Lodge, D., Davies, S.N., Jones, M.G., Millar, J., Manallack, D.T., Ornstein, P.L., Verberne, A.J.M., Young, N. & Beart, P.M. (1988). A comparison between the in vivo and in vitro activity of five potent and competitive NMDA antagonists. British Journal of Pharmacology 95, 957965.CrossRefGoogle ScholarPubMed
Macdermott, A.B. & Dale, N. (1987). Receptors, ion channels, and synaptic potentials underlying the integrative actions of excitatory amino acids. Trends in Neuroscience 10, 280284.CrossRefGoogle Scholar
Mayer, M.L. & Westbrook, G.L. (1987). The physiology of excitatory amino acids in the vertebrate central nervous system. Progress in Neurobiology 28, 197276.CrossRefGoogle ScholarPubMed
McCormick, D.A. & Feeser, H.R. (1990). Functional implications of burst firing and single spike activity in lateral geniculate nucleus neurons. Neuroscience 39, 103113.CrossRefGoogle Scholar
Roe, A.W., Garraghty, P.E. & Sur, M. (1989). Terminal arbors of single ON-center and OFF-center X and Y retinal ganglion cell axons within the ferret's lateral geniculate nucleus. Journal of Comparative Neurology 288, 208242.CrossRefGoogle ScholarPubMed
Scharfman, H.E., Lu, S.-M., Guido, W., Adams, P.R. & Sherman, S.M. (1990). N-methyl-D-aspartate receptors contribute to excitatory postsynaptic potentials of cat lateral geniculate neurons recorded in thalamic slices. Proceedings of the National Academy of Sciences of the U.S.A. 87, 45484552.CrossRefGoogle ScholarPubMed
Sherman, S.M. & Koch, C. (1986). The control of retinogeniculate transmission in the mammalian lateral geniculate nucleus. Experimental Brain Research 63, 120.CrossRefGoogle ScholarPubMed
Sillito, A.M., Murphy, P.C., Salt, T.E. & Moody, C.I. (1990a). Dependence of retinogeniculate transmission in cat on NMDA receptors. Journal of Neurophysiology 63, 347355.CrossRefGoogle ScholarPubMed
Sillito, A.M., Murphy, P.C. & Salt, T.E. (1990b). The contribution of the non-N-methyl-D-aspartate group of excitatory amino acid receptors to retinogeniculate transmission in the cat. Neuroscience 34, 273280.CrossRefGoogle ScholarPubMed
Steriade, M. & Llinas, R. (1988). The functional states of the thalamus and the associated neuronal interplay. Physiological Reviews 68, 649742.CrossRefGoogle ScholarPubMed
Watkins, J.C. & Olverman, H.J. (1987). Agonists and antagonists for excitatory amino acid receptors. Trends in Neuroscience 10, 265272.CrossRefGoogle Scholar