Experimental Brain Research

, Volume 69, Issue 2, pp 407–416 | Cite as

Actions of excitatory amino acid antagonists on geniculo-cortical transmission in the cat's visual cortex

  • K. Hagihara
  • T. Tsumoto
  • H. Sato
  • Y. Hata
Article
Received:
Accepted:

Summary

To test the possibility that glutamate and aspartate are transmitters at geniculo-cortical synapses and to elucidate which type of receptors for the excitatory amino acids (EAA) operate at these synapses, we studied effects of microionophoretic administration of EAA antagonists on the responses of visual cortical neurons to afferent electrical and visual stimulation in the cat. The antagonists used were kynurenate, a non-selective antagonist for all classes of EAA receptors and 2-amino-5-phos-phonovalerate (APV), a selective antagonist for N-methyl-D-aspartate (NMDA)-preferring receptors. The administration of kynurenate suppressed responses elicited by electrical stimulation of the dorsal lateral geniculate nucleus (LGN) and optic chiasm (OX) of 65% of the cells tested. This suppression was more marked for the short-latency responses which were evoked monosynaptically from the LGN, than for the longer-latency responses. In contrast with the effectiveness of kynurenate, APV failed to suppress electrically and visually elicited responses in 66% of the cortical cells. Such differences between kynurenate and APV were particularly prominent in layers IV and VI, which receive direct inputs from the LGN, but were less marked or were not recognizable in layers II + III and V. These results support previous suggestions that EAAs may be excitatory transmitters in the cerebral cortex, at least at geniculo-cortical synapses, and indicate further that EAA receptors of the “non-NMDA type” may be involved in afferent synaptic transmission in the cat's visual cortex.

Key words

Visual cortex Glutamate Excitatory transmitters Geniculo-cortical synapses Kynurenic acid 
This is a preview of subscription content, log in to check access.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Baughman RW, Gilbert CD (1981) Aspartate and glutamate as possible neurotransmitters in the visual cortex. J Neurosci 1: 427–439Google Scholar
  2. Bradford HF, Richards CD (1976) Specific release of endogenous glutamate from pyriform cortex stimulated in vitro. Brain Res 105: 168–172Google Scholar
  3. Brooks PA, Smith DS, Stone TW, Kelly JS (1986) Postsynaptic action of kynurenic acid in the rat dentate gyrus. Neurosci Lett 66: 96–100Google Scholar
  4. Bullier J, Henry GH (1979) Ordinal position of neurons in cat striate cortex. J Neurophysiol 42: 1251–1263Google Scholar
  5. Clark RM, Collins GGS (1975) The release of endogenous amino acids from the rat visual cortex. J Physiol (Lond) 263: 383–400Google Scholar
  6. Collingridge GL, Kehl SJ, McLennan H (1983a) The antagonism of amino acid-induced excitations of rat hippocampal CA1 neurones in vitro. J Physiol (Lond) 334: 19–31Google Scholar
  7. Collingridge GL, Kehl SJ, McLennan H (1983b) Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J Physiol (Lond) 334: 33–46Google Scholar
  8. Creutzfeldt OD, Fuster JM, Herz A, Straschill M (1966) Some problems of the information transmission in the visual system. In: Eccles JC (ed) Brain and conscious experience. Springer, Berlin, pp 138–164Google Scholar
  9. Curtis DR, Duggan AW, Felix D, Johnston GAR, Tebecis AK, Watkins JC (1972) Excitation of mammalian central neurones by acidic amino acids. Brain Res 41: 283–301Google Scholar
  10. Davies J, Francis AA, Jones AW, Watkins JC (1981) 2-amino-5-phosphonovalerate (APV), a potent and selective antagonist of amino acid-induced and synaptic excitation. Neurosci Lett 21: 77–81Google Scholar
  11. Davies J, Watkins JC (1982) Actions of D and L forms of 2-amino-5-phosphonovalerate and 2-amino-4-phosphonobutyrate in the cat spinal cord. Brain Res 235: 378–386Google Scholar
  12. Dingledine R (1983) N-methylaspartate activates voltage-dependent calcium conductance in rat hippocampal pyramidal cells. J Physiol (Lond) 343: 385–405Google Scholar
  13. Elmslie KS, Yoshikami D (1985) Effects of kynurenate on root potentials evoked by synaptic activity and amino acids in the frog spinal cord. Brain Res 330: 265–272Google Scholar
  14. Evans RH, Francis AA, Jones AW, Smith DAB, Watkins JC (1982) The effects of a series of ω-phosphonic α-carboxylic amino acids on electrically evoked and excitant amino acid-induced responses in isolated spinal cord preparations. Br J Pharmacol 75: 65–75Google Scholar
  15. French-Mullen JMH, Hori N, Carpenter DO (1986) Receptors for excitatory amino acids on neurons in rat pyriform cortex. J Neurophysiol 55: 1283–1294Google Scholar
  16. Flatman JA, Schwindt PC, Crill WE, Stafstrom CE (1983) Multiple actions of N-methyl-D-aspartate on cat neocortical neurons in vitro. Brain Res 266: 169–173Google Scholar
  17. Fonnum F (1984) Glutamate: a neurotransmitter in mammalian brain. J Neurochem 42: 1–11Google Scholar
  18. Ganong AH, Cotman CW (1986) Kynurenic acid and quinolinic acid act at N-methyl-D-aspartate receptors in the rat hippocampus. J Pharmacol Exp Ther 236: 293–299Google Scholar
  19. Ganong AH, Lanthorn TH, Cotman CW (1983) Kynurenic acid inhibits synaptic and acidic amino acid-induced responses in the rat hippocampus and spinal cord. Brain Res 273: 170–174Google Scholar
  20. Gilbert CD (1977) Laminar differences in receptive field properties of cells in cat primary visual cortex. J Physiol (Lond) 268: 391–421Google Scholar
  21. Gilbert CD (1983) Microcircuitry of the visual cortex. Ann Rev Neurosci 6: 217–247Google Scholar
  22. Hagihara K, Tsumoto T, Sato H, Hata Y (1987) Actions of an excitatory amino acid antagonist on geniculo-cortical synapses in the cat. In: Hicks TP, Lodge D, McLennan H (eds) Excitatory amino acid transmission. Alan R Liss, New York, pp 409–412Google Scholar
  23. Harris EW, Ganong AH, Cotman CW (1984) Long-term potentiation in the hippocampus involves activation of N-methyl-D-aspartate receptors. Brain Res 323: 132–137Google Scholar
  24. Harvey AR (1980) A physiological analysis of subcortical and commissural projections of area 17 and 18 of the cat. J Physiol (Lond) 302: 507–534Google Scholar
  25. Hayashi T (1954) Effects of sodium glutamate on the nervous system. Keio J Med 302: 183–192Google Scholar
  26. Herrling PL (1985) Pharmacology of the corticocaudate excitatory postsynaptic potential in the cat: evidence for its mediation by quisqualate- or kainate-receptors. Neuroscience 14: 417–426Google Scholar
  27. Hicks TP, Guedes RCA (1983) Neuropharmacological properties of electrophysiologically identified, visually responsive neurones of the posterior lateral suprasylvian area. A microiontophoretic study. Exp Brain Res 49: 157–173Google Scholar
  28. Hicks TP, Guedes RCA, Veale WL, Veenhuizen J (1985) Aspartate and glutamate as synaptic transmitters of parallel visual cortical pathways. Exp Brain Res 58: 421–425Google Scholar
  29. Hicks TP (1987) Excitatory amino acid pathways in cerebral cortex. In: Hicks TP, Lodge D, McLennan H (eds) Excitatory amino acid transmission. Alan R Liss, New York, pp 373–380Google Scholar
  30. Hubel DH, Wiesel TN (1962) Receptive fields, binocular interactions and functional architecture in the cat's visual cortex. J Physiol (Lond) 160: 106–154Google Scholar
  31. Huettner JE, Baughman RW (1986) Primary culture of identified neurons from the visual cortex of postnatal rats. J Neurosci 6: 3044–3060Google Scholar
  32. Jahr CE, Jessell TM (1985) Synaptic transmission between dorsal root ganglion and dorsal horn neurons in culture: antagonism of monosynaptic excitatory postsynaptic potentials and glutamate excitation by kynurenate. J Neurosci 5: 2281–2289Google Scholar
  33. Jasper HH, Koyama I (1969) Rate of release of amino acids from the cerebral cortex as affected by brain stem and thalamic stimulation. Can J Physiol Pharmacol 47: 889–905Google Scholar
  34. Krnjević K, Phillis JW (1963) Iontophoretic studies of neurones in the mammalian cerebral cortex. J Physiol (Lond) 165: 274–304Google Scholar
  35. MacDonald JF, Porietis AV, Wojtowicz JM (1982) L-aspartic acid induces a region of negative slope conductance in the current-voltage relationship of cultured spinal cord neurons. Brain Res 237: 248–253Google Scholar
  36. McLennan H (1982) The isomers of 2-amino-5-phosphonovalerate as excitatory amino acid antagonists — a reappraisal. Eur J Pharmacol 79: 135–137Google Scholar
  37. McLennan H (1983) Receptors for the excitatory amino acids in the mammalian central nervous system. Prog Neurobiol 20: 251–271Google Scholar
  38. Morris RGM, Anderson E, Lynch GS, Baudry M (1986) Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature 319: 774–776Google Scholar
  39. Nowak L, Bregestovski P, Ascher P (1984) Magnesium gates glutamate-activated channels in mouse central neurons. Nature 307: 462–465Google Scholar
  40. Oka J-I, Metherate RS, Hicks TP (1986) Excitatory amino acid antagonists and synaptic transmission in the cat's intact thalamo-cortical somatosensory pathway. In: Hicks TP, Lodge D, McLennan H (eds) Excitatory amino acid transmission. Alan R Liss, New York, pp 401–404Google Scholar
  41. Otsuka R, Hassler R (1962) Über Aufbau und Gliederung der corticalen Sehsphäre bei Katzen. Arch Psychiat Z Ges Neurol 203: 212–234Google Scholar
  42. Perkins MN, Stone TW (1982) An iontophoretic investigation of the actions of convulsant kynurenines and their interaction with the endogenous excitant quinolinic acid. Brain Res 247: 184–187Google Scholar
  43. Perkins MN, Stone TW (1985) Actions of kynurenic acid and quinolinic acid in the rat hippocampus in vivo. Exp Neurol 88: 570–579Google Scholar
  44. Robinson MB, Anderson KD, Koerner JF (1984) Kynurenic acid as an antagonist of hippocampal excitatory transmission. Brain Res 309: 119–126Google Scholar
  45. Singer W, Tretter F, Cynader M (1975) Organization of cat striate cortex: a correlation of receptive-field properties with afferent and efferent connections. J Neurophysiol 38: 1080–1098Google Scholar
  46. Stone TW (1986) The relative potencies of (-)-2-amino-5-phosphono-valerate and (-)-2-amino-7-phosphonohepatanoate as antagonists of N-methyl-aspartate and quinolinic acids and repetitive spikes in rat hippocampal slices. Brain Res 381: 195–198Google Scholar
  47. Tanaka K (1985) Organization of geniculate inputs to visual cortical cells in the cat. J Neurophysiol 42: 357–364Google Scholar
  48. Thomson AM, West DC, Lodge D (1985) An N-methyl-aspartate receptor-mediated synapse in rat cerebral cortex: a site of action for ketamine? Nature 313: 479–481Google Scholar
  49. Thomson AM (1986) Comparison of responses to transmitter candidates at an N-methylaspartate receptor mediated synapse, in slices of rat cerebral cortex. Neuroscience 17: 37–47Google Scholar
  50. Toyama K, Matsunami K, Ohno T, Tokashiki S (1974) An intracellular study of neuronal organization in the visual cortex. Exp Brain Res 21: 45–66Google Scholar
  51. Tsumoto T (1974) Characteristics of the thalamic ventrobasal relay neurons as a function of conduction velocities of medial lemniscal fibers. Exp Brain Res 21: 211–224Google Scholar
  52. Tsumoto T (1978) Inhibitory and excitatory binocular convergence to visual cortical neurons of the cat. Brain Res 159: 85–97Google Scholar
  53. Tsumoto T, Suda K (1980) Three groups of cortico-geniculate neurons and their distribution in binocular and monocular segments of cat striate cortex. J Comp Neurol 193: 223–236Google Scholar
  54. Tsumoto T, Suda K (1982) Postnatal development of the corticofugal projection from striate cortex to lateral geniculate nucleus in kittens. Dev Brain Res 4: 323–332Google Scholar
  55. Tsumoto T, Masui H, Sato H (1986) Excitatory amino acid transmitters in neuronal circuits of the cat visual cortex. J Neurophysiol 55: 469–483Google Scholar
  56. Tsumoto T, Masui H, Sato H (1987a) Actions of glutamate/aspartate antagonists on visually- and amino acid-induced excitations in the cat visual cortex. In: Hicks TP, Lodge D, McLennan H (eds) Excitatory amino acid transmission. Alan R Liss, New York, pp 389–396Google Scholar
  57. Tsumoto T, Hagihara K, Sato H, Hata Y (1987b) NMDA receptors in the visual cortex of young kittens are more effective than those of adult cats. Nature 327: 513–514Google Scholar
  58. Watkins JC, Evans RH (1981) Excitatory amino acid transmitters. Ann Rev Pharmacol Toxicol 21: 165–204Google Scholar
  59. Wigstrom H, Gustafsson B (1984) A possible correlate of the postsynaptic condition for long-lasting potentiation in the guinea pig hippocampus in vitro. Neurosci Lett 44: 327–332Google Scholar

Copyright information

© Springer-Verlag 1988

Authors and Affiliations

  • K. Hagihara
    • 1
  • T. Tsumoto
    • 1
  • H. Sato
    • 1
  • Y. Hata
    • 1
  1. 1.Department of NeurophysiologyInstitute of Higher Nervous Activity, Osaka University Medical SchoolOsakaJapan

Personalised recommendations