Summary
-
1.
Potentiation of the excitatory response to L-glutamate (Glu) by L-aspartate (Asp), similar to that which has been described at the crustacean neuromuscular junction, is observed inAplysia neurons which are glutamate sensitive.
-
2.
Potentiation of the inhibitory responses to ionophoretically applied Glu in neurons preconditioned with Asp permits experiments which serve to differentiate among four hypotheses previously proposed to explain the underlying mechanism of the phenomenon.
-
3.
The potentiation is inhibited by cooling (Q 10 = 1.3 ± 0.2) and is blocked in Na+-free seawater, where the response to Glu applied alone is increased in both amplitude and duration.
-
4.
These results are most consistent with the view that Glu is normally removed from the extracellular medium through an active reuptake process which is Na+ dependent, is slightly temperature sensitive, and may be blocked by Asp.
References
Baetge, E. E., Bullock, K., and Stallcup, W. B. (1979). A comparison of glutamate transport in cloned cell lines from the central nervous system.Brain Res. 167210–214.
Baker, P. F., and Potashner, S. J. (1971). The dependence of glutamate uptake by crab nerve on external Na+ and K+.Biochim. Biophys. Acta 249616–622.
Bennett, J. P., Logan, W. J., and Snyder, S. M. (1973). Amino acids as central nervous transmitters: The influence of ions, amino acid analogues, and ontogeny on transport systems for L-glutamic and L-aspartic acids and glycine into central nervous synaptosomes of the rat.J. Neurochem. 211533–1550.
Carpenter, D. O., McCreery, M. J., Woodbury, C. M., and Yarowsky, P. J. (1978). Modulation of endogenous discharge in neuron R15 through specific receptors for several neurotransmitters. InAbnormal Neuronal Discharges (Chalazonitis, N., and Boisson, M., Ed.), Raven Press, New York.
Constanti, A., and Nistri, A. (1978). A study of the interaction between glutamate and aspartate at the lobster neuromuscular junction.Br. J. Pharmacol. 62495–505.
Crawford, A. C., and McBurney, R. N. (1977). The synergistic action of L-glutamate and L-aspartate at crustacean excitatory neuromuscular junctions.J. Physiol. 268697–709.
Dekin, M. S. (1983). Permeability changes induced by L-glutamate at the crayfish neuromuscular junction.J. Physiol. 341105–125.
Dudel, J. (1977). Aspartate and other inhibitors of excitatory synaptic transmission in crayfish muscle.Pflugers Arch. 3697–16.
Gerschenfeld, H. M. (1973). Chemical transmission in invertebrate central nervous systems and neuromuscular junctions.Physiol. Rev. 11–119.
Kehoe, J. (1972). Three acetylcholine receptors inAplysia neurones.J. Physiol. 225115–146.
Kehoe, J., and Marder, E. (1976). Identification and effects of neural transmitters in invertebrates.Ann. Rev. Pharmacol. Toxicol. 16245.
Kravitz, E. A., Slater, C. R., Takahashi, K., Bownds, M. D., and Crossfeld, R. M. (1970). Excitatory transmission in invertebrates—glutamate as a potential neuromuscular transmitter compound. InExcitatory Synaptic Mechanisms (Anderson, P., and Jansen, J. K. S., Eds.), Universitetsforlaget, Oslo, pp. 85–93.
Nistri, A., and Constanti, A. (1979). Pharmacological characterization of different types of GABA and glutamate receptors in vertebrate and invertebrate.Prog. Neurobiol. 13117–235.
Onodera, K., and Takeuchi, A. (1975). Ionic mechanisms of the excitatory synaptic membranes of the crayfish neuromuscular junction.J. Physiol. (Lond.) 252295–318.
Onodera, K., and Takeuchi, A. (1976). Permeability changes produced by L-glutamate at the excitatory post-synaptic membrane of the crayfish muscle.J. Physiol. (Lond.) 255669–685.
Osborne, N. N., Schroder, H. U., and Neuhoff, V. (1978). The accumulation of DL-glutamate by the central nervous system of the snailHelix pomatia.Brain Res. 152543–553.
Price, C. H., Coggeshall, R. E., and McAdoo, D. J. (1978). Specific glycine uptake by identified neurons ofAplysia californica. I. Autoradiography.Brain Res. 15425–40.
Shank, R. P., and Freeman, A. R. (1975). Cooperative interaction of glutamate and aspartate with receptors in the excitation in the walking limbs of the lobster.J. Neurobiol. 6289–303.
Swann, J. W., and Carpenter, D. O. (1975). Organization of receptors for neurotransmitters onAplysia neurones.Nature 258751–754.
Takeuchi, A., and Onodera, K. (1973). Reversal potentials of the excitatory transmitter and L-glutamate at the crayfish neuromuscular junction.Nature New Biol. 242124–126.
Wheeler, D. D., and Boyarsky, L. L. (1971). Influx of glutamic acid in peripheral nerve. Energy, ionic, and pH dependence.J. Neurobiol. 2181–190.
Zeman, G. H., Myers, P. R., and Dalton, T. K. (1975). Gamma-aminobutyric acid uptake and metabolism inAplysia dactylomela.Comp. Biochem. Physiol. 51(C):291–299.
Author information
Authors and Affiliations
Additional information
This work was supported by the Armed Forces Radiobiology Research Institute, Defense Nuclear Agency, under Research Work Unit C30203. The views presented in this paper are those of the authors. No endorsement by the Defense Nuclear Agency has been given or should be inferred.
Rights and permissions
About this article
Cite this article
McCreery, M.J., Carpenter, D.O. Modulation of neuronal responses tol-glutamate inAplysia . Cell Mol Neurobiol 4, 91–95 (1984). https://doi.org/10.1007/BF00710945
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00710945