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Inhibitory glutamate receptor channels

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Abstract

Inhibitory glutamate receptors (IGluRs) are a family of ion channel proteins closely related to ionotropic glycine and γ-aminobutyric acid (GABA) receptors; They are gated directly by glutamate; the open channel is permeable to chloride and sometimes potassium. Physiologically and pharmacologically, IGluRs most closely resemble GABA receptors; they are picrotoxin-sensitive and sometimes crossdesensitized by GABA. However, the amino acid sequences of cloned IGluRs are most similar to those of glycine receptors. Ibotenic acid, a conformationally restricted glutamate analog closely related to muscimol, activates all IGluRs. Quisqualate is not an IGluR agonist except among pulmonate molluscs and for a unique multiagonist receptor in the crayfishAustropotamobius torrentium. Other excitatory amino acid agonists are generally ineffective. Avermectins have several effects on IGluRs, depending on concentration: potentiation, direct gating, and blockade, both reversible and irreversible. Since IGluRs have only been clearly described in protostomes and pseudocoelomates, these effects may mediate the powerful antihelminthic and insecticidal action of avermectins, while explaining their low toxicity to mammals.

IGluRs mediate synaptic inhibition in neurons and are expressed extrajunctionally in striated muscles. The presence of IGluRs in a neuron or muscle is independent of the presence or absence of excitatory glutamate receptors or GABA receptors in the cell. Generally, extrajunctional IGluRs in muscle have a higher sensitivity to glutamate than do neuronal synaptic receptors. Some extrajunctional receptors are sensitive in the range of circulating plasma glutamate levels, suggesting a role for IGluRs in regulating muscle excitability.

The divergence of the IGlu/GABA/Gly/ACh receptor superfamily in protostomes could become a powerful model system for adaptive molecular evolution. Physiologically and pharmacologically, protostome receptors are considerably more diverse than their vertebrate counterparts. Antagonist profiles are only loosely correlated with agonist profiles (e.g., curare-sensitive GABA receptors, bicuculline-sensitive AChRs), and pharmacologically identical receptors may be either excitatory or inhibitory, and permeable to different ions. The assumption that agonist sensitivity reliably connotes discrete, homologous receptor families is contraindicated. Protostome ionotropic receptors are highly diverse and straightforward to assay; they provide an excellent system in which to study and integrate fundamental questions in molecular evolution and adaptation.

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References

  • Accili E. A. and DiFrancesco D. (1996) Inhibition of the hyperpolarization-activated current (If) of rabbit SA node myocytes by niflumic acid.Pflugers Arch. 431, 757–762.

    PubMed  CAS  Google Scholar 

  • Adams E., Simkiss K., and Taylor M. (1982) Metal ion metabolism in the moulting crayfish (Austropotamobius pallipes).Comp. Biochem. Physiol. 72, 73–76.

    Google Scholar 

  • Adelsberger H., von Beckerath N., Franke C., and Dudel J. (1994) A patch-clamp study on a novel gamma-aminobutyric acid-activated chloride channel of crayfish deep extensor abdominal muscle.Neurosci. Lett. 170, 221–224.

    PubMed  CAS  Google Scholar 

  • Akaike N., Inoue M., and Krishtal O. A. (1986) “Concentration-clamp” study of gamma-aminobutyric-acid-induced chloride current kinetics in frog sensory neurones.J. Physiol. 379, 171–185.

    PubMed  CAS  Google Scholar 

  • Albert J., Lingle C. J., Marder E., and O'Neil M. B., (1986) A GABA-activated chloride-conductance not blocked by picrotoxin on spiny lobster neuromuscular preparations.Br. J. Pharm. 87, 771–779.

    CAS  Google Scholar 

  • Altschul S. F., Gish W., Miller W., Myers E. W., and Lipman D. (1990) Basic local alignment search tool.J. Mol. Biol. 215, 403–410.

    PubMed  CAS  Google Scholar 

  • Arena J. P. (1994) Expression ofCaenorhabditis elegans mRNA inXenopus oocytes: a model system to study the mechanism of action of avermectins.Parasit. Today 10, 35–37.

    CAS  Google Scholar 

  • Arena J. P., Liu K. K., Paress P. S., and Cully D. F. (1991) Avermectin-sensitive chloride currents induced byCaenorhabditis elegans RNA inXenopus oocytes.Mol. Pharm. 40, 368–374.

    CAS  Google Scholar 

  • Arena J. P., Liu K. K., Paress P. S., Schaeffer J. M., and Cully D. F. (1992) Expression of a glutamate-activated chloride current inXenopus oocytes injected withCaenorhabditis elegans RNA: evidence for modulation by avermectin.Mol. Brain Res. 15, 339–348.

    PubMed  CAS  Google Scholar 

  • Arenson M. S. and Nistri A. (1982) A novel inhibitory-excitatory response of frog motoneuronsin vitro to glutamate.J. Physiol. 328, 9P.

    Google Scholar 

  • Arshavsky Y. I., Deliagina T. G., Gamkrelidze G. N., Orlovsky G. N., Panchin Y. V., Popova L. B., and Shupliakov O. V. (1993) Pharmacologically induced elements of the hunting and feeding behavior in the pteropod molluscClione limacina. I. Effects of GABA.J. Neurophysiol. 69, 512–521.

    PubMed  CAS  Google Scholar 

  • Ascher P., Nowak L., and Kehoe J. S. (1986) Glutamate-activated channels in molluscan and vertebrate neurones, inIon Channels in Neural Membranes (Ritchie J. M., Keynes R. D., and Bolis L., eds.), Liss, New York, pp. 283–295.

    Google Scholar 

  • Barnard E. A., Darlison M. G., and Seeburg P. (1987) Molecular biology of the GABA-A receptor: the receptor/channel superfamily.Trends Neurosci. 10, 502–509.

    CAS  Google Scholar 

  • Barnes R. D. (1987)Invertebrate Zoology, 5th ed. Harcourt Brace Jovanovich, New York.

    Google Scholar 

  • Bermudez I., Hawkins C. A., Taylor A. M., and Beadle D. J. (1991) Actions of insecticides on the insect GABA receptor complex.J. Recept. Res. 11, 221–232.

    PubMed  CAS  Google Scholar 

  • Bidaut M. (1980) Pharmacological dissection of pyloric network of the lobster stomatogastric ganglion using picrotoxin.J. Neurophysiol. 44, 1089–1101.

    PubMed  CAS  Google Scholar 

  • Bokisch A. J. and Walker R. J. (1986) The action of avermectin (MK 936) on identified central neurones fromHelix and its interaction with acetylcholine and gamma-aminobutyric acid (GABA) responses.Comp. Biochem. Physiol. C 84, 119–125.

    PubMed  CAS  Google Scholar 

  • Bolker J. A. and Raff R. A. (1996) Developmental genetics and traditional homology.BioEssays 18, 489–494.

    PubMed  CAS  Google Scholar 

  • Bolshakov V. Y., Gapon S. A., and Magazanik L. G. (1991) Different types of glutamate receptors in isolated and identified neurones of the molluscPlanorbarius corneus.J. Physiol. 439, 15–35.

    PubMed  CAS  Google Scholar 

  • Bolshakov V. Y., Gapon S. A., and Magazanik L. G. (1992) Transduction mechanism for glutamate-induced potassium current in neurones of the molluscPlanorbarius corneus.J. Physiol. 455, 33–50.

    PubMed  CAS  Google Scholar 

  • Bolshakov V. Y., Gapon S. A., Katchman A. N., and Magazanik L. G. (1993) Activation of a common potassium channel in molluscan neurones by glutamate, dopamine and muscarinic agonist.J. Physiol. 468, 11–33.

    PubMed  CAS  Google Scholar 

  • Boore J. L. and Brown W. M. (1994) Mitochondrial genomes and the phylogeny of molluscs.Nautilus 108, 61–78.

    Google Scholar 

  • Boore J. L., Collins T. M., Stanton D., Daehler L. L., and Brown W. M. (1995) Deducing the pattern of arthropod phylogeny from mitochondrial DNA rearrangements.Nature 376, 163–165.

    PubMed  CAS  Google Scholar 

  • Bormann J. and Clapham D. E. (1985) Gamma-aminobutyric acid receptor channels in adrenal chromaffin cells: a patch-clamp study.Proc. Natl. Acad. Sci. USA 82, 2168–2172.

    PubMed  CAS  Google Scholar 

  • Bormann J., Hamill O. P., and Sakmann B. (1987) Mechanism of anion permeation through channels gated by glycine and gamma-aminobutyric acid in mouse cultured spinal neurones.J. Physiol. 385, 243–286.

    PubMed  CAS  Google Scholar 

  • Burg R. W., Miller B. M., Baker E. E., Birnbaum J., Currie S. A., Hartman R., Kong Y. L., Monaghan R. L., Olson G., Putter I., Tunac J. B., Wallick H., Stapley E. O., Oiwa R., and Omura S. (1979) Avermectins, new family of potent anthelminthic agents: producing organism and fermentation.Antimicrob. Agents. Chemother. 15, 361–367.

    PubMed  CAS  Google Scholar 

  • Carlyle R. F. (1970a) The action of glutamic acid and some derivatives on isolated supra oral sphincter preparations of the sea anemone.Actinia equina.J. Physiol. 212, 32P-33P.

    CAS  Google Scholar 

  • Carlyle R. F. (1970b) The effects of amino acids and some related substances on isolated preparations of the sea anemoneActinia equina.J. Physiol. 208, 67P-68P.

    PubMed  CAS  Google Scholar 

  • Carlyle R. F. (1971) The occurrence of some amino acids in, and their release from, isolated supra oral sphincter preparations of the sea anemoneActinia equina.J. Physiol. 215, 44P-45P.

    PubMed  CAS  Google Scholar 

  • Carlyle R. F. (1974) The occurrence in and actions of amino acids on isolated supra oral sphincter preparations of the sea anemoneActinia equina.J. Physiol. 236, 635–652.

    PubMed  CAS  Google Scholar 

  • Camien M. N., Sarlet H., Duchateau G., and Florkin M. (1951) Non-protein amino acids in muscle and blood of marine and fresh water crustacea.J. Biol. Chem. 193, 881–885.

    PubMed  CAS  Google Scholar 

  • Campbell W. C. and Benz G. W. (1984) Ivermectin: a review of efficacy and safety.J. Vet. Pharm. Ther. 7, 1–16.

    CAS  Google Scholar 

  • Carpenter D. O., Swann J. W., and Yarowsky P. J. (1977) Effect of curare on responses to different putative neurotransmitters inAplysia neurons.J. Neurobiol. 8, 119–132.

    PubMed  CAS  Google Scholar 

  • Cazalets J.-R. and Harris-Warrick R. M. (1989)Soc. Neurosci. Abstracts 15, 998.

    Google Scholar 

  • Chabala J. C., Mrozik H., Tolman R. L., Eskola P., Lusi A., Peterson L. H., Woods M. F., Fisher M. H., Campbell W. C., Egerton J. R., and Ostlind D. A. (1980) Ivermectin, a new broad-spectrum antiparasitic agent.J. Med. Chem. 23, 1134–1136.

    PubMed  CAS  Google Scholar 

  • Chenoy-Marchais D. (1982) ACl-conductance activated by hyperpolarization inAplysia neurones.Nature 299, 359–361.

    PubMed  CAS  Google Scholar 

  • Chiba C. and Saito T. (1994) APB (2-amino-4-phosphonobutyric acid) activates a chloride conductance in ganglion cells isolated from newt retina.Neuroreport 5, 489–492.

    PubMed  CAS  Google Scholar 

  • Cleland T. A. and Selverston A. I. (1995) Glutamate-gated inhibitory currents of central pattern generator neurons in the lobster stomatogastric ganglion.J. Neurosci. 15, 6631–6639.

    PubMed  CAS  Google Scholar 

  • Cull-Candy S. G. (1976) Two types of extrajunctionall-glutamate receptors in locust muscle fibres.J. Physiol. 255, 449–464.

    PubMed  CAS  Google Scholar 

  • Cull-Candy S. G. (1978) Glutamate sensitivity and distribution of receptors along normal and denervated locust muscle fibres.J. Physiol. 276, 165–181.

    PubMed  CAS  Google Scholar 

  • Cull-Candy S. G. and Miledi R. (1981) Junctional and extrajunctional membrane channels activated by GABA in locust muscle fibres.Proc. Roy. Soc. Lond. B 211, 527–535.

    CAS  Google Scholar 

  • Cull-Candy S. G., Donnellan J. F., James R. W., and Lunt G. G. (1976) 2-Amino-4-phosphonobutyric acid as a glutamate antagonist on locust muscle.Nature 262, 408–409.

    PubMed  CAS  Google Scholar 

  • Cully D. F. and Paress P. S. (1991) Solubilization and characterization of a high affinity ivermectin binding site fromCaenorhabditis elegans.Mol. Pharm. 40, 326–332.

    CAS  Google Scholar 

  • Cully D. F., Vassilatis D. K., Liu K. K., Paress P. S., van der Ploeg L. H. T., Schaeffer J. M., and Arena J. P. (1994) Cloning of an avermectin-sensitive glutamate-gated chloride channel fromCaenorhabditis elegans.Nature 371, 707–711.

    PubMed  CAS  Google Scholar 

  • Cully D. F., Paress P. S., Liu K. K., Schaeffer J. M., and Arena J. P. (1996) Identification of aDrosophila melanogaster glutamate-gated chloride channel sensitive to the antiparasitic agent avermectin.J. Biol. Chem. 271, 20,187–20,191.

    CAS  Google Scholar 

  • Darlison M. G. (1992) Invertebrate GABA and glutamate receptors: molecular biology reveals predictable structures but some unusual pharmacologies.Trends Neurosci. 15, 469–474.

    PubMed  CAS  Google Scholar 

  • Darlison M. G., Hutton M. L., and Harvey R. J. (1993) Molluscan ligand-gated ion-channel receptors.Exs 63, 48–64.

    PubMed  CAS  Google Scholar 

  • Delgado R., Barla R., Latorre R., and Labarca P. (1989)l-glutamate activates excitatory and inhibitory channels inDrosophila larval muscle.FEBS Lett. 243, 337–342.

    PubMed  CAS  Google Scholar 

  • Dickinson P. S. (1995) The contributions of motor neuronal and muscle modulation to behavioral flexibility in the stomatogastric system.Am. Zool. 35, 548–555.

    Google Scholar 

  • Dubas F. (1991) Actions of putative amino acid neurotransmitters on the neuropile arborizations of locust flight motoneurones.J. Exp. Biol. 155, 337–356.

    CAS  Google Scholar 

  • Duce I. R. and Scott R. H. (1985) Actions of dihydro-avermectin B1a on insect muscle.Br. J. Pharm. 85, 395–401.

    CAS  Google Scholar 

  • Dudel J. (1977) Aspartate and other inhibitors of excitatory synaptic transmission in crayfish muscle.Pflugers Arch. 369, 7–16.

    PubMed  CAS  Google Scholar 

  • Dudel J., Franke C., Hatt H., and Usherwood P. N. (1989) Chloride channels gated by extrajunctional glutamate receptors (H-receptors) on locust leg muscle.Brain Res. 481, 215–220.

    PubMed  CAS  Google Scholar 

  • Eernisse D. J., Albert J. S., and Anderson F. E. (1992) Annelida and Arthropoda are not sister taxa: a phylogenetic analysis of spiralian metazoan morphology.Syst. Biol. 41, 305–330.

    Google Scholar 

  • Eisen J. S. and Marder E. (1982) Mechanisms underlying pattern generation in lobster stomatogastric ganglion as determined by selective inactivation of identified neurons. III. Synaptic connections of electrically coupled pyloric neurons.J. Neurophysiol. 48, 1392–1415.

    PubMed  CAS  Google Scholar 

  • Eliasof S. and Werblin F. (1993) Characterization of the glutamate transporter in retinal cones of the tiger salamander.J. Neurosci. 13, 402–411.

    PubMed  CAS  Google Scholar 

  • Elson R. C. and Selverston A. I. (1995) Slow and fast synaptic inhibition evoked by pattern-generating neurons of the gastric mill network in spiny lobsters.J. Neurophysiol. 74, 1996–2011.

    PubMed  CAS  Google Scholar 

  • Etter A., Cully D. F., Schaeffer J. M., Liu K. K., and Arena J. P. (1996) An amino acid substitution in the pore region of a glutamate-gated chloride channel enables the coupling of ligand binding to channel gating.J. Biol. Chem. 271, 16,035–16,039.

    CAS  Google Scholar 

  • Fairman W. A., Vandenberg R. J., Arriza J. L., Kavanaugh M. P., and Amara S. G. (1995) An excitatory amino-acid transporter with properties of a ligand-gated chloride channel.Nature 375, 599–603.

    PubMed  CAS  Google Scholar 

  • Field K. G., Olsen G. J., Lane D. J., Giovannoni S. J., Ghiselin M. T., Raff E. C., Pace N. R., and Raff R. A. (1988) Molecular phylogeny of the animal kingdom.Science 239, 748–753.

    PubMed  CAS  Google Scholar 

  • Fitch W. M. (1970) Distinguishing homologous from analogous proteins.Syst. Zool. 19, 99–113.

    PubMed  CAS  Google Scholar 

  • Florey E. and Murdock L. L. (1974) The ionic mechanism of action of GABA andl-glutamate on a crustacean striated muscle (vas deferens of the crayfish).Comp. Gen. Pharm. 5, 91–99.

    CAS  Google Scholar 

  • Franciolini F. and Nonner W. (1987) Anion and cation permeability of a chloride channel in rat hippocampal neurons.J. Gen. Physiol. 90, 453–478.

    PubMed  CAS  Google Scholar 

  • Franciolini F. and Nonner W. (1994a) Anion-cation interactions in the pore of neuronal background chloride channels.J. Gen. Physiol. 104, 711–723.

    PubMed  CAS  Google Scholar 

  • Franciolini F. and Nonner W. (1994b) A multi-ion permeation mechanism in neuronal background chloride channels.J. Gen. Physiol. 104, 725–746.

    PubMed  CAS  Google Scholar 

  • Frank E. (1974) The sensitivity to glutamate of denervated muscles of the crayfish.J. Physiol. 242, 371–382.

    PubMed  CAS  Google Scholar 

  • Franke C., Hatt H., and Dudel J. (1986) The inhibitory chloride channel activated by glutamate as well as GABA.J. Comp. Physiol. A 159, 591–609.

    CAS  Google Scholar 

  • Franke C., Hatt H., and Dudel J. (1987) Liquid filament switch for ultra-fast exchanges of solutions at excised patches of synaptic membrane of crayfish muscle.Neurosci. Lett. 77, 199–204.

    PubMed  CAS  Google Scholar 

  • Fraser S. P., Djamgoz M. B., Usherwood P. N., O'Brien J., Darlison M. G., and Barnard E. A. (1990) Amino acid receptors from insect muscle: electrophysiological characterization inXenopus oocytes following expression by injection of mRNA.Mol. Brain Res. 8, 331–341.

    PubMed  CAS  Google Scholar 

  • Friedrich M. and Tautz D. (1995) Ribosomal DNA phylogeny of the major extant arthropod classes and the evolution of myriapods.Nature 376, 165–167.

    PubMed  CAS  Google Scholar 

  • Fritz L. C., Wang C. C., and Gorio A. (1979) Avermectin B1a irreversibly blocks postsynaptic potentials at the lobster neuromuscular junction by reducing muscle membrane resistance.Proc. Natl. Acad. Sci. USA 76, 2062–2066.

    PubMed  CAS  Google Scholar 

  • Gerschenfeld H. M. and Lasansky A. (1964) Action of glutamic acid and other naturally occurring amino acids on snail central neurones.Int. J. Neuropharm. 3, 301–314.

    CAS  Google Scholar 

  • Giles D. and Usherwood P. N. (1985a) The effects of putative amino acid neurotransmitters on somata isolated from neurons of the locust central nervous system.Comp. Biochem. Physiol. C 80, 231–236.

    PubMed  CAS  Google Scholar 

  • Giles D. P. and Usherwood P. N. (1985b) Locust nymphal neurones in culture: a new technique for studying the physiology and pharmacology of insect central neurones.Comp. Biochem. Physiol. C 80, 53–59.

    PubMed  CAS  Google Scholar 

  • Glantz R. M. and Pfeiffer-Linn C. (1992) NMDA receptors in invertebrates.Comp. Biochem. Physiol. C 103, 243–248.

    Google Scholar 

  • Gorman A. L. F. and Marmor M. F. (1971) A biphasic potential produced byl-glutamic acid in a giant molluscan neuron.Fed. Proc. 30, 323.

    Google Scholar 

  • Graham D., Pfeiffer F., and Betz H. (1982) Avermectin B1a inhibits the binding of strychnine to the glycine receptor of rat spinal cord.Neurosci. Lett. 29, 173–176.

    PubMed  CAS  Google Scholar 

  • Grant G. B. and Dowling J. E. (1995) A glutamate-activated chloride current in cone-driven ON bipolar cells of the white perch retina.J. Neurosci. 15, 3852–3862.

    PubMed  CAS  Google Scholar 

  • Gration K. A., Clark R. B., and Usherwood P. N. (1979) Three types ofl-glutamate receptor on junctional membrane of locust muscle fibres.Brain Res. 171, 360–364.

    PubMed  CAS  Google Scholar 

  • Graubard K., Raper J. A., and Hartline D. K. (1983) Graded synaptic transmission between identified spiking neurons.J. Neurophysiol. 50, 508–521.

    PubMed  CAS  Google Scholar 

  • Gray G. S. and Fitch W. M. (1983) Evolution of antibiotic resistance genes: the DNA sequence of a kanamycin resistance gene fromStaphylococcus aureus.Mol. Biol. Evol. 1, 57–66.

    PubMed  CAS  Google Scholar 

  • Grenningloh G., Rienitz A., Schmitt B., Methfessel C., Zensen M., Beyreuther K., Gundelfinger E. D., and Betz H. (1987) The strychnine-binding subunit of the glycine receptor shows homology with nicotinic acetylcholine receptors.Nature 328, 215–220.

    PubMed  CAS  Google Scholar 

  • Hall B. K. (1994)Homology: the Hierarchical Basis of Comparative Biology. Academic, New York.

    Google Scholar 

  • Hamill O. P., Bormann J., and Sakmann B. (1983) Activation of multiple-conductance state chloride channels in spinal neurones by glycine and GABA.Nature 305, 805–808.

    PubMed  CAS  Google Scholar 

  • Harris-Warrick R. M., Marder E., Selverston A. I., and Moulins M. (1992)Dynamic Biological Networks: the Stomatogastric Nervous System. MIT Press, Cambridge, MA.

    Google Scholar 

  • Henry C. D., Leslie J., and Kulovich S. (1991) Circulating free amino acids inAplysia californica.Comp. Biochem. Physiol. A 100, 629–632.

    PubMed  CAS  Google Scholar 

  • Hill A. V. (1909) The mode of action of nicotine and curari, determined by the form of the contraction curve and the method of temperature coefficients.J. Physiol. 39, 361–373.

    PubMed  CAS  Google Scholar 

  • Hille B. (1992)Ionic Channels of Excitable Membranes, 2nd ed. Sinauer Associates, Sunderland, MA.

    Google Scholar 

  • Hillis D. M. (1994) Hornology in molecular biology, inHomology: the Hierarchical Basis of Comparative Biology (Hall B. K., ed.), Academic, New York, pp. 339–368.

    Google Scholar 

  • Hillis D. M. and Moritz C., eds. (1990)Molecular Systematics. Sinauer Associates, Sunderland, MA.

    Google Scholar 

  • Holden-Dye L. and Walker R. J. (1990) Avermectin and avermectin derviatives are antagonists at the 4-aminobutyric acid (GABA) receptor on the somatic muscle cells ofAscaris; is this the site of antihelminthic action?Parasitology 2, 265–271.

    Google Scholar 

  • Holden-Dye L., Hewitt G. M., Wann K. T., Krogsgaard-Larsen P., and Walker R. J. (1988) Studies involving avermectin and the 4-aminobutyric acid (GABA) receptor ofAscaris suum muscle.Pestic. Sci. 24, 231–245.

    CAS  Google Scholar 

  • Hollmann M. and Heinemann S. (1994) Cloned glutamate receptors.Ann. Rev. Neurosci. 17, 31–108.

    PubMed  CAS  Google Scholar 

  • Houamed K. M., Kuijper J. L., Gilbert T. L., Haldeman B. A., O'Hara P. J., Mulvihill E. R., Almers W., and Hagen F. S. (1991) Cloning, expression, and gene structure of a G protein-coupled glutamate receptor from rat brain.Science 252, 1318–1321.

    PubMed  CAS  Google Scholar 

  • Hue B., Pelhate M., and Chanelet J. (1979) Pre- and postsynaptic effects of taurine and GABA in the cockroach central nervous system.Can. J. Neurol. Sci. 6, 243–250.

    PubMed  CAS  Google Scholar 

  • Ikemoto Y. and Akaike N. (1988) The glutamate-induced chloride current inAplysia neurones lacks pharmacological properties seen for excitatory responses to glutamate.Eur. J. Pharm. 150, 313–318.

    CAS  Google Scholar 

  • Ikemoto Y., Akaike N., and Ono K. (1988) Kinetic analysis of glutamate-induced chloride current inAplysia neurones: a “concentration clamp” study.Eur. J. Pharm. 150, 303–311.

    CAS  Google Scholar 

  • Jackel C., Krenz W.-D., and Nagy F. (1994a) Bicuculline/baclofen-insensitive GABA response in crustacean neurones in culture.J. Exp. Biol. 191, 167–193.

    PubMed  CAS  Google Scholar 

  • Jackel C., Krenz W.-D., and Nagy F. (1994b) A receptor with GABA-C-like pharmacology in invertebrate neurones in culture.Neuroreport 5, 1097–1101.

    PubMed  CAS  Google Scholar 

  • Johnson B. R., Peck J. H., and Harris-Warrick R. M. (1995) Distributed amine modulation of graded chemical transmission in the pyloric network of the lobster stomatogastric ganglion.J. Neurophysiol. 74, 437–452.

    PubMed  CAS  Google Scholar 

  • Johnson G. A., Curtis D. R., Davies J., and McCulloch R. M. (1974) Spinal interneurone excitation by conformationally restricted analogues ofl-glutamic acid.Nature 248, 804,805.

    Google Scholar 

  • Johnson G. A. R., Curtis D. R., de Groat W. C., and Duggan A. W. (1968) Central actions of ibotenic acid and muscimol.Biochem. Pharm. 17, 2488,2489.

    Google Scholar 

  • Kaneko A. and Tachibana M. (1986) Blocking effects of cobalt and related ions on the gamma-aminobutyric acid-induced current in turtle retinal cones.J. Physiol. 373, 463–479.

    PubMed  CAS  Google Scholar 

  • Kato M., Oomura Y., Maruhashi J., and Shimizu N. (1983) Chemical characteristics of thel-glutamate receptor on theOnchidium neuron.J. Neurosci. 3, 549–556.

    PubMed  CAS  Google Scholar 

  • Katz P. S. and Levitan I. B. (1993) Quisqualate and ACPD are agonists for a glutamate-activated current in identifiedAplysia neurons.J. Neurophysiol. 69, 143–150.

    PubMed  CAS  Google Scholar 

  • Kehoe J. (1972) Three acetylcholine receptors inAplysia neurones.J. Physiol. 225, 115–146.

    PubMed  CAS  Google Scholar 

  • Kehoe J. (1978) Transformation by concanavalin A of the response of molluscan neurones tol-glutamate.Nature 274, 866–869.

    PubMed  CAS  Google Scholar 

  • Kehoe J. (1994) Glutamate activates a K+ conductance increase inAplysia neurons that appears to be independent of G proteins.Neuron 13, 691–702.

    PubMed  CAS  Google Scholar 

  • Kerkut G. A. and Cottrell G. A. (1962) Amino-acids in the blood and nervous system ofHelix aspersa.Comp. Biochem. Physiol. 5, 227–230.

    PubMed  CAS  Google Scholar 

  • Kerkut G. A., Horn N., and Walker R. J. (1969) Long-lasting synaptic inhibition and its transmitter in the snailHelix aspersa.Comp. Biochem. Physiol. 30, 1061–1074.

    PubMed  CAS  Google Scholar 

  • King W. M. and Carpenter D. O. (1987) Distinct GABA and glutamate receptors may share a common channel inAplysia neurons.Neurosci. Lett. 82, 343–348.

    PubMed  CAS  Google Scholar 

  • King W. M. and Carpenter D. O. (1989) Voltageclamp characterization of Cl-conductance gated by GABA andl-glutamate in single neurons ofAplysia. J. Neurophysiol. 61, 892–899.

    CAS  Google Scholar 

  • Kyte J. and Doolittle R. F. (1982) A simple method for displaying the hydropathic character of a protein.J. Mol. Biol. 157, 105–132.

    PubMed  CAS  Google Scholar 

  • Larsson H. P., Picaud S. A., Werblin F. S., and Lecar H. (1996) Noise analysis of the glutamate-activated current in photoreceptors.Biophys. J. 70, 733–742.

    PubMed  CAS  Google Scholar 

  • Laughton D. L., Wheeler S. V., Lunt G. G., and Wolstenholme A. J. (1995) The beta-subunit ofCaenorhabditis elegans avermectin receptor responds to glycine and is encoded by chromosome 1.J. Neurochem. 64, 2354–2357.

    PubMed  CAS  Google Scholar 

  • Lea T. J. and Usherwood P. N. (1973a) Effect of ibotenic acid on chloride permeability of insect muscle-fibres.Comp. Gen. Pharm. 4, 351–363.

    CAS  Google Scholar 

  • Lea T. J. and Usherwood P. N. (1973b) The site of action of ibotenic acid and the identification of two populations of glutamate receptors on insect muscle fibres.Comp. Gen. Pharm. 4, 333–350.

    CAS  Google Scholar 

  • Lee K., Rowe I. C., and Ashford M. L. (1995) NS 1619 activates BKCa channel activity in rat cortical neurones.Eur. J. Pharm. 280, 215–219.

    CAS  Google Scholar 

  • Lerma J. and del Rio R. M. (1992) Chloride transport blockers preventN-methyl-d-aspartate receptor-channel complex activation.Mol. Pharm. 41, 217–222.

    CAS  Google Scholar 

  • Lingle C. (1980) The sensitivity of decapod foregut muscles to acetylcholine and glutamate.J. Comp. Physiol. 138, 187–199.

    CAS  Google Scholar 

  • Lingle C. and Marder E. (1981) A glutamate-activated chloride conductance on a crustacean muscle.Brain Res 212, 481–488.

    PubMed  CAS  Google Scholar 

  • Macdonald J. F. and Nistri A. (1978) A comparison of the action of glutamate, ibotenate and other related amino acids on feline spinal interneurones.J. Physiol. 275, 449–465.

    PubMed  CAS  Google Scholar 

  • Macdonald R. L. and Olsen R. W. (1994) GABA-A receptor channels.Ann. Rev. Neurosci. 17, 569–602.

    PubMed  CAS  Google Scholar 

  • Magazanik L. G., Bolshakov V. Y., and Gapon S. A. (1990) Glutamate receptors in mollusc neurons.J. Evol. Biochem. Physiol. 26, 501–510.

    Google Scholar 

  • Marder E. and Eisen J. S. (1984) Transmitter identification of pyloric neurons: electrically coupled neurons use different transmitters.J. Neurophysiol. 51, 1345–1361.

    PubMed  CAS  Google Scholar 

  • Marder E. and Paupardin-Tritsch D. (1978) The pharmacological properties of some crustacean neuronal acetylcholine, gamma-aminobutyric acid, andl-glutamate responses.J. Physiol. 280, 213–236.

    PubMed  CAS  Google Scholar 

  • Maricq A. V., Peterson A. S., Brake A. J., Myers R. M., and Julius D. (1991) Primary structure and functional expression of the 5HT3 receptor, a serotonin-gated ion channel.Science 254, 432–437.

    PubMed  CAS  Google Scholar 

  • Martin R. J. and Pennington A. J. (1989) A patchclamp study of effects of dihydroavermectin onAscaris muscle.Br. J. Pharm. 98, 747–756.

    CAS  Google Scholar 

  • Masu M., Tanabe Y., Tsuchida K., Shigemoto R., and Nakanishi S. (1991) Sequence and expression of a metabotropic glutamate receptor.Nature 349, 760–765.

    PubMed  CAS  Google Scholar 

  • Mathers D. A. (1985) Spontaneous and GABA-induced single channel currents in cultured murine spinal cord neurons.Can. J. Physiol. Pharmacol. 63, 1228–1233.

    PubMed  CAS  Google Scholar 

  • Mat Jais A. M., Kerkut G. A., and Walker R. J. (1983) The ionic mechanism associated with the biphasic glutamate response on leech Retzius cells.Comp. Biochem. Physiol. C 74, 425–432.

    Google Scholar 

  • Mat Jais A. M., Kerkut G. A., and Walker R. J. (1984) The ionic mechanisms associated with the excitatory response of kainate,l-glutamate, quisqualate, ibotenate, AMPA and methyl-tetrahydrofolate on leech Retzius cells.Comp. Biochem. Physiol. C 77, 115–126.

    PubMed  CAS  Google Scholar 

  • McCreery M. J. and Carpenter D. O. (1984) Modulation of neuronal responses tol-glutamate inAplysia. Cell. Mol. Neurobiol. 47, 91–95.

    Google Scholar 

  • Mellin T. N., Busch R. D., and Wang C. C. (1983) Postsynaptic inhibition of invertebrate neuromuscular transmission by avermectin B1a.Neuropharmacology 22, 89–96.

    PubMed  CAS  Google Scholar 

  • Miwa A., Ui M., and Kawai N. (1990) G protein is coupled to presynaptic glutamate and GABA receptors in lobster neuromuscular synapse.J. Neurophysiol. 63, 173–180.

    PubMed  CAS  Google Scholar 

  • Murdock L. L. (1971) Crayfish vas deferens: contractions in response tol-glutamate and gamma-aminobutyrate.Comp. Gen. Pharm. 2, 93–98.

    CAS  Google Scholar 

  • Murdock L. L. and Chapman G. Y. (1974)l-glutamate in arthropod blood plasma: physiological implications.J. Exp. Biol. 60, 783–794.

    PubMed  CAS  Google Scholar 

  • Newberry N. R. and Nicoll R. A. (1984) A bicuculline-resistant inhibitory post-synaptic potential in rat hippocmapal pyramidal cells in vitro.J. Physiol. 348, 239–254.

    PubMed  CAS  Google Scholar 

  • Nicoll R. A. and Alger B. E. (1981) Synaptic excitation may activate a calcium-dependent potassium conductance in hippocampal pyramidal cells.Science 212, 957–959.

    PubMed  CAS  Google Scholar 

  • Nistri A. (1981) Excitatory and inhibitory action of ibotenic acid on frog spinal motoneuronesin vitro.Brain Res. 208, 397–408.

    PubMed  CAS  Google Scholar 

  • Nistri A. and Arenson M. S. (1983) Multiple postsynaptic responses evoked by glutamate onin vitro spinal motoneurones.Adv. Biochem. Psychopharm. 37, 229–236.

    CAS  Google Scholar 

  • Olsen R. W. and Tobin A. J. (1990) Molecular biology of GABA-A receptors.FASEB J. 4, 1469–1480.

    PubMed  CAS  Google Scholar 

  • Onozuka M., Watanabe K., Nagata K., and Imai S. (1994) Involvement of a Ca2+/calmodulin-dependent protein kinase II-associated mechanism in the induction of an outward potassium current by quisqualate.Brain Res. 650, 336–340.

    PubMed  CAS  Google Scholar 

  • Oomura Y., Ooyama H., and Sawada M. (1974) Analysis of hyperpolarizations induced by glutamate and acetylcholine onOnchidium neurones.J. Physiol. 243, 321–341.

    PubMed  CAS  Google Scholar 

  • Ortells M. O. and Lunt G. G. (1995) Evolutionary history of the ligand-gated ion-channel superfamily of receptors.Trends Neurosci. 18, 121–127.

    PubMed  CAS  Google Scholar 

  • Ottolia M. and Toro L. (1994) Potentiation of large conductance KCa channels by niflumic, flufenamic, and mefenamic acids.Biophys. J. 67, 2272–2279.

    PubMed  CAS  Google Scholar 

  • Oyama Y., Ikemoto Y., Kits K. S., and Akaike N. (1990) GABA affects the glutamate receptor-chloride channel complex in mechanically isolated and internally perfusedAplysia neurons.Eur. J. Pharm. 185, 43–52.

    CAS  Google Scholar 

  • Palmer E., Monaghan D. T., and Cotman C. W. (1989) Trans-ACPD, a selective agonist of the phosphoinositide-coupled excitatory amino acid receptor.Eur. J. Pharm. 166, 585–587.

    CAS  Google Scholar 

  • Parmentier J. and Case J. (1972) Structure-activity relationships of amino acid receptor sites on an identifiable cell body in the brain of the land snailHelix aspersa.Comp. Biochem. Physiol. A 43, 511–518.

    CAS  Google Scholar 

  • Partridge L. D., Sandquist M., and Shaw T. (1994)Soc. Neurosci. Abstact 20, 1522.

    Google Scholar 

  • Patterson C. (1982) Morphological characters and homology, inProblems of Phylogenetic Reconstruction (Joysey K. A. and Friday A. E., eds.), Academic, New York, pp. 21–74.

    Google Scholar 

  • Patterson C. (1990) Metazoan phylogeny: reassessing relationships.Nature 344, 199, 200.

    PubMed  CAS  Google Scholar 

  • Pearlstein E., Marchand A. R., and Clarac F. (1994) Inhibitory effects ofl-glutamate on central processes of crustacean leg motoneurons.Eur. J. Neurosci. 6, 1445–1452.

    PubMed  CAS  Google Scholar 

  • Picaud S. A., Larsson H. P., Grant G. B., Lecar H., and Werblin F. S. (1995) Glutamate-gated chloride channel with glutamate-transporter-like properties in cone photoreceptors of the tiger salamander.J. Neurophysiol. 74, 1760–1771.

    PubMed  CAS  Google Scholar 

  • Piggott S. M., Kerkut G. A., and Walker R. J. (1975) Structure-activity studies on glutamate receptor sites of three identifiable neurones in the suboesophageal ganglia ofHelix aspersa.Comp. Biochem. Physiol. C 51, 91–100.

    PubMed  CAS  Google Scholar 

  • Poronnik, P., Ward M. C., and Cook D. I. (1992) Intracellular Ca2+ release by flufenamic acid and other blockers of the non-selective cation channel.FEBS Lett. 296, 245–248.

    PubMed  CAS  Google Scholar 

  • Premkumar L. and Chung S. H. (1995) Activation of K+ channels by stimulation of metabotropic glutamate receptors.Neuroreport 6, 765–768.

    PubMed  CAS  Google Scholar 

  • Quinlan E. M. and Murphy A. D. (1991) Glutamate as a putative neurotransmitter in the buccal central pattern generator ofHelisoma trivolvis.J. Neurophysiol. 66, 1264–1271.

    PubMed  CAS  Google Scholar 

  • Quinlan E. M., Gregory K., and Murphy A. D. (1995) An identified glutamatergic interneuron patterns feeding motor activity via both excitation and inhibition.J. Neurophysiol. 73, 945–956.

    PubMed  CAS  Google Scholar 

  • Raff R. A. and Kaufman T. C. (1983)Embryos, Genes, and Evolution: the Developmental-Genetic Basis of Evolutionary Change. Indiana University Press, Bloomington, IN.

    Google Scholar 

  • Rainnie D. G., Holmes K. H., and Shinnick G. P. (1994) Activation of postsynaptic metabotropic glutamate receptors by trans-ACPD hyperpolarizes neurons of the basolateral amygdala.J. Neurosci. 14, 7208–7220.

    PubMed  CAS  Google Scholar 

  • Randle J. C. and Renaud L. P. (1987) Actions of gamma-aminobutyric acid on rat supraoptic nucleus neurosecretory neurones in vitro.J. Physiol. 387, 629–647.

    PubMed  CAS  Google Scholar 

  • Riek R. P., Handschumacher M. D., Sung S. S., Tan M., Glynias M. J., Schluchter M. D., Novotny J., and Graham R. M. (1995) Evolutionary conservation of both the hydrophilic and hydrophobic nature of transmembrane residues.J. Theor. Biol. 172, 245–258.

    PubMed  CAS  Google Scholar 

  • Roberts C. J. and Walker R. J. (1982) The actions of glutamate and putative glutamate agonists on the central neurons ofLimulus polyphemus.Comp. Biochem. Physiol. C 73, 167–175.

    Google Scholar 

  • Sakmann B., Hamill O. P., and Bormann J. (1983) Patch-clamp measurements of elementary chloride currents activated by the putative inhibitory transmitter GABA and glycine in mammalian spinal neurons.J. Neur. Trans. 18(Suppl.) 83–95.

    CAS  Google Scholar 

  • Sansom M. S. and Usherwood P. N. (1990) Singlechannel studies of glutamate receptors.Int. Rev. Neurobiol. 32, 51–106.

    PubMed  CAS  Google Scholar 

  • Sattelle D. B. (1992) Receptors forl-glutamate and GABA in the nervous system of an insect (Periplaneta americana).Comp. Biochem. Physiol. C 103, 429–438.

    PubMed  CAS  Google Scholar 

  • Sawada M., Hara N., Ito I., and Maeno T. (1984a) Ionic mechanism of a hyperpolarizing glutamate effect on two identified neurons in the buccal ganglion ofAplysia.J. Neurosci. Res. 11, 91–103.

    PubMed  CAS  Google Scholar 

  • Sawada M., McAdoo D. J., Ichinose M., and Price C. H. (1984c) Influence of glycine and neuron R-14 on contraction of the anterior aorta ofAplysia.Jpn. J. Physiol. 34, 747–767.

    PubMed  CAS  Google Scholar 

  • Sawada M., Gibson D., and McAdoo D. J. (1984b)l-glutamic acid, a possible neurotransmitter to anterior aorta ofAplysia.J. Neurophysiol. 51, 375–386.

    PubMed  CAS  Google Scholar 

  • Schaeffer J. M. and Haines H. W. (1989) Avermectin binding inCaenorhabditis elegans. A two-state model for the avermectin binding site.Biochem. Pharm. 38, 2329–2338.

    PubMed  CAS  Google Scholar 

  • Schmidt J. and Calabrese R. L. (1992) Evidence that acetylcholine is an inhibitory transmitter of heart interneurons in the leech.J. Exp. Biol. 171, 329–347.

    PubMed  CAS  Google Scholar 

  • Schmieden V., Kuhse J., and Betz H. (1993) Mutation of glycine receptor subunit creates beta-alanine receptor responsive to GABA.Science 262, 256–258.

    PubMed  CAS  Google Scholar 

  • Schoepp D., Bockaert J., and Sladeczek F. (1990) Pharmacological and functional characteristics of metabotropic excitatory amino acid receptors.Trends Pharm. Sci. 11, 508–515.

    PubMed  CAS  Google Scholar 

  • Schofield P. R., Darlison M. G., Fujita N., Burt D. R., Stephenson F. A., Rodriguez H., Rhee L. M., Ramachandran J., Reale V., Glencorse T. A., Seeburg P. H., and Barnard E. A. (1987) Sequence and functional expression of the GABA-A receptor shows a ligand-gated receptor superfamily.Nature 328, 221–227.

    PubMed  CAS  Google Scholar 

  • Scholtz G. and Richter S. (1995) Phylogenetic systematics of the reptantian Decapoda (Crustacea, Malacostraca)Zool. J. Linn. Soc. 113, 289–328.

    Google Scholar 

  • Scott R. H. and Duce I. R. (1987) Pharmacology of GABA receptors on skeletal muscle fibres of the locust (Schistocerca gregaria).Comp. Biochem. Physiol. C 86, 305–311.

    PubMed  CAS  Google Scholar 

  • Scott R. H. and Duce I. R. (1985) Effects of 22,23-dihydroavermectin B1a on locust (Schistocerca gregaria) muscles may involve several sites of action.Pestic. Sci. 16, 599–604.

    CAS  Google Scholar 

  • Shank R. P. and Freeman A. R. (1975) Cooperative interaction of glutamate and aspartate with receptors in the neuromuscular excitatory membrane in walking limbs of the lobster.J. Neurobiol. 6, 289–303.

    PubMed  CAS  Google Scholar 

  • Sharp A. A. (1994) Single neuron and small network dynamics explored with the dynamic clamp, PhD. dissertation, Brandeis University.

  • Shinozaki H. and Ishida M. (1980) Inhibitory action of ibotenic acid on the crayfish neuromuscular junction.Brain Res. 198, 157–165.

    PubMed  CAS  Google Scholar 

  • Shinozaki H. and Ishida M. (1981) Electrophysiological studies of kainate, quisqualate, and ibotenate action on the crayfish neuromuscular junction.Adv. Biochem. Psychopharm. 27, 327–336.

    CAS  Google Scholar 

  • Sigel E. and Baur R. (1987) Effect of avermectin Bla on chick neuronal gamma-aminobutyrate receptor channels expressed inXenopus oocytes.Mol. Pharm. 32, 749–752.

    CAS  Google Scholar 

  • Smart T. G. and Constanti A. (1986) Studies on the mechanism of action of picrotoxin and other convulsants at the crustacean muscle GABA receptor.Proc. Roy. Soc. Lond B 227, 191–216.

    CAS  Google Scholar 

  • Smart T. G., Houamed K. M., Van Renterghem C., and Constanti A. (1987) mRNA-directed synthesis and insertion of functional amino acid receptors inXenopus laevis oocytes.Biochem. Soc. Trans. 15, 117–122.

    PubMed  CAS  Google Scholar 

  • Stelzer A. and Wong R. K. (1989) GABA-A responses in hippocampal neurons are potentiated by glutamate.Nature 337, 170–173.

    PubMed  CAS  Google Scholar 

  • Striedter G. F. and Northcutt R. G. (1991) Biological hierarchies and the concept of homology.Brain Behav. Evol. 38, 177–189.

    PubMed  CAS  Google Scholar 

  • Swofford D. L. and Olsen G. J. (1990) Phylogeny reconstruction, inMolecular Systematics (Hillis D. M. and Moritz C., eds.), Sinauer, Sunderland, MA, pp. 411–501.

    Google Scholar 

  • Szczepaniak A. C. and Cottrell G. A. (1973) Biphasic action of glutamic acid and synaptic inhibition in an identified serotonin-containing neurone.Nature New Biol. 241, 62–64.

    PubMed  CAS  Google Scholar 

  • Takeuchi A. and Takeuchi N. (1964) The effect on crayfish muscle of iontophoretically applied glutamate.J. Physiol. 170, 296–317.

    PubMed  CAS  Google Scholar 

  • Takeuchi A. and Takeuchi N. (1965) Localized action of gamma-aminobutyric acid on the crayfish muscle.J. Physiol. 177, 225–238.

    PubMed  CAS  Google Scholar 

  • Takeuchi A. and Takeuchi N. (1967) Anion permeability of the inhibitory post-synaptic membrane of the crayfish neuromuscular junction.J. Physiol. 191, 575–590.

    PubMed  CAS  Google Scholar 

  • Tazaki K. and Chiba C. (1994) Glutamate, acetylcholine, and gamma-aminobutyric acid as transmitters in the pyloric system of the stomatogastric ganglion of a stomatopod,Squilla oratoria.J. Comp. Physiol. A 175, 487–504.

    CAS  Google Scholar 

  • Turbeville J. M., Pfeifer D. M., Field K. G., and Raff R. A. (1991) The phylogenetic status of arthropods, as inferred from 18S rRNA sequences.Mol. Biol. Evol. 8, 669–686.

    PubMed  CAS  Google Scholar 

  • Usherwood P. N. R. (1969) Glutamate sensitivity of denervated insect muscle fibres.Nature 223, 411–413.

    PubMed  CAS  Google Scholar 

  • Usherwood P. N. R. and Grundfest H. (1965) Peripheral inhibition in skeletal muscle of insects.J. Neurophysiol. 28, 497–518.

    PubMed  CAS  Google Scholar 

  • van Gelder N. M. (1971) Molecular arrangement for physiological action of glutamic acid and gamma-aminobutyric acid.Can. J. Physiol. Pharmacol. 49, 513–519.

    PubMed  Google Scholar 

  • van Vreeswijk C., Abbott L. F. and Ermentrout G. B. (1994) When inhibition not excitation synchronizes neural firing.J. Comput. Neurosci 1, 313–321.

    PubMed  Google Scholar 

  • Wafford K. A. and Sattelle D. B. (1986) Effects of amino acid neurotransmitter candidates on an identified insect motoneurone.Neurosci. Lett. 63, 135–140.

    PubMed  CAS  Google Scholar 

  • Wafford K. A. and Sattelle D. B. (1989)l-glutamate receptors on the cell body membrane of an identified insect motor neurone.J. Exp. Biol. 144, 449–462.

    Google Scholar 

  • Walker R. J. (1976) The action of kainic acid and quisqualic acid on the glutamate receptors of three identifiable neurones from the brain of the snail,Helix aspersa.Comp. Biochem. Physiol. C 55, 61–67.

    PubMed  CAS  Google Scholar 

  • Walker R. J. and Roberts C. J. (1982) The pharmacology ofLimulus central neurons.Comp. Biochem. Physiol. C 72, 391–401.

    PubMed  CAS  Google Scholar 

  • Walker R. J., Woodruff G. N., and Kerkut G. A. (1971) The effect of ibotenic acid and muscimol on single neurons of the snail,Helix aspersa.Comp. Gen. Pharm. 2, 168–174.

    CAS  Google Scholar 

  • Walker R. J., James V. A., Roberts C. J., and Kerkut G. A. (1981) Studies on amino acid receptors ofHirudo, Helix, Limulus, andPeriplaneta.Adv. Physiol. Sci. 22, 161–190.

    CAS  Google Scholar 

  • Watanabe K. and Onozuka M. (1994) Glutamate elicits an outward K+ current which is normally suppressed by a Ca2+/calmodulin-dependent protein kinase II.Brain Res. 654, 352–356.

    PubMed  CAS  Google Scholar 

  • Wiley E. O. (1981)Phylogenetics: the Theory and Practice of Phylogenetic Systematics. Wiley, New York.

    Google Scholar 

  • Wo Z. G. and Oswald R. E. (1995) Unraveling the modular design of glutamate-gated ion channels.Trends Neurosci. 18, 161–168.

    PubMed  CAS  Google Scholar 

  • Wright D. J. (1986) Biological activity and mode of action of avermectins, inNeuropharmacology and Pesticide Action (Ford M. G., Lunt G. G., Reay R. C., and Usherwood P. N. R., eds.), Ellis Horwood Ltd., Chichester, UK, pp. 174–202.

    Google Scholar 

  • Yamamoto C., Yamashita H., and Chujo T. (1976) Inhibitory action of glutamic acid on cerebellar interneurones.Nature 262, 786,787.

    PubMed  CAS  Google Scholar 

  • Yarowsky P. J. and Carpenter D. O. (1976) Aspartate: distinct receptors onAplysia neuron.Science 192, 807–809.

    PubMed  CAS  Google Scholar 

  • Yarowsky P. J. and Carpenter D. O. (1978a) Receptors for gamma-aminobutyric acid (GABA) onAplysia neurons.Brain Res. 144, 75–94.

    PubMed  CAS  Google Scholar 

  • Yarowsky P. J. and Carpenter D. O. (1978b) A comparison of similar ionic responses to gamma-aminobutyric acid and acetylcholine.J. Neurophysiol. 41, 531–541.

    PubMed  CAS  Google Scholar 

  • Zufall F., Franke C., and Hatt H. (1988) Acetylcholine activates a chloride channel as well as glutamate and GABA: single channel recordings from crayfish stomach and opener muscles.J. Comp. Physiol. A 163, 609–620.

    Google Scholar 

  • Zufall F., Franke C., and Hatt H. (1989) The insecticide avermectin B1a activates a chloride channel in crayfish muscle membrane.J. Exp. Biol. 142, 191–205.

    CAS  Google Scholar 

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Cleland, T.A. Inhibitory glutamate receptor channels. Mol Neurobiol 13, 97–136 (1996). https://doi.org/10.1007/BF02740637

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