Summary
1. Intracellular and voltage-clamp recordings were obtained from a selected population of neuroscretory (ns) cells in the X organ of the crayfish isolated eyestalk. Pulses of γ-aminobutyric acid (GABA) elicited depolarizing responses and bursts of action potentials in a dose-dependent manner. These effects were blocked by picrotoxin (50 µM) but not by bicuculline. Picrotoxin also suppressed spontaneous synaptic activity.
2. The responses to GABA were abolished by severing the neurite of X organ cells, at about 150 µm from the cell body. Responses were larger when the application was made at the neuropil level.
3. Topical application of Cd2+ (2 mM), while suppressing synaptic activity, was incapable of affecting the responses to GABA.
4. Under whole-cell voltage-clamp, GABA elicited an inward current with a reversal potential dependent on the chloride equilibrium potential. The GABA effect was accompanied by an input resistance reduction up to 33% at a −50 mV holding potential. No effect of GABA was detected on potassium, calcium, and sodium currents present in X organ cells.
5. The effect of GABA on steady-state currents was dependent on the intracellular calcium concentration. At 10−6 M [Ca2+]i, GABA (50 µM) increased the membrane conductance more than threefold and shifted the zero-current potential from−25 to−10 mV. At 10−9 M [Ca2+]i, GABA induced only a 1.3-fold increase in membrane conductance, without shifting the zero-current potential.
6. These results support the notion that in the population of X organ cells sampled in this study, GABA acts as an excitatory neurotransmitter, opening chloride channels.
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References
Adams, P. R., and Brown, D. A. (1975). Actions of γ-aminobutyric acid on sympathetic ganglion cells.J. Physiol. 250:85–120.
Alvarez-Leefmans, F. J., Gamiño, S. M., Giraldez, F., and Noguerón, I. (1988). Intracellular chloride regulation in amphibian dorsal root ganglion neurones studied with ion-selective microelectrodes.J. Physiol. (London)406:225–246.
Andrew, R. D., Orchard, I., and Saleuddin, A. S. M. (1978). Structural reevaluation of the neurosecretory system in the crayfish eyestalk.Cell Tissue Res. 190:235–246.
Aréchiga, H., Cortés, J. J., García, U., and Rodríguez-Sosa, L. (1985a). Neuroendocrine correlates of circadian rhythmicity in crustaceans.Am. Zool. 25:265–274.
Aréchiga, H., García, U., and Martínez-Millán, L. (1990). Synaptic regulation of neurosecretory cell activity in the crayfish eyestalk. InFrontiers in Crustacean Neurobiology (K. Wieseet al., Eds.), Birkhauser Verlag, Basel, pp. 373–380.
Atwood, H. L. (1976). Organization and synaptic physiology of crustacean neuromuscular systems.Prog. Neurobiol. 7:291–391.
Bormann, J., Hamill, O. P., and Sakmann, B. (1987). Mechanism of anion permeation through channels gated by glycine and γ-aminobutyric acid in mouse cultured spinal neurons.J. Physiol. 385:234–286.
Cooke, I. M. (1985). Electrophysiological characterization of peptidergic neurosecretory terminals.J. Exp. Biol. 118:1–35.
Cooke, I. M., and Stuenkel, E. (1985). Electrophysiology of invertebrate neurosecretory cells. InThe Electrophysiology of the Secretory Cell (A. M. Poisner and J. Trifaro, Eds.), Elsevier, Amsterdam, pp. 115–164.
Cherubini, E., Gaiarsa, J. L., and Yehezkel, B.-A. (1991). GABA—an excitatory transmitter in early postnatal life.TINS 14:515–519.
Enna, S. J. (1983). GABA receptors. InThe GABA Receptors (S. J. Enna, Ed.), Humana Press, Clifton, NJ, pp. 1–18.
Fingerman, M. (1985). The physiology and pharmacology of crustacean chromatophores.Am. Zool. 25:233–252.
Gallagher, J. P., and Shinnick-Gallagher, P. (1983). Electrophysiological characteristics of GABA receptor complex. InThe GABA Receptor (S. J. Enna, Ed.), Humana Press, Clifton, NJ, pp. 25–61.
García, U., Onetti, C., Valdiosera, R. and Aréchiga, H. (1991a). GABA is an excitatory transmitter in crayfish central synapses.Third IBRO World Congress of Neuroscience, Montreal, Canada, p. 215.
García, U., García-Colunga, J., and Aréchiga, H. (1991b). Differential effects of gamma-aminobutyric acid, glycine, and taurine on central synapses of crustaceans.Proc. West. Pharmacol. Soc. 34:215–218.
Glantz, R. M., Kirk, M. D., and Aréchiga, H. (1983). Light input to crustacean neurosecretory cells.Brain Res. 265:308–311.
Hamill, O. P., Marty, A., Neher, E., Sackmann, B., and Sigworth, F. J. (1981). Improved patch-clamp and cell-free membrane patches.Pfluegers Arch. 391:81–100.
Iwasaki, S., and Satow, Y. (1970). Spike initiation of neurosecretory neuron soma in Na deficient or TTX medium.J. Physiol. Soc. Jpn. 32:37.
Iwasaki, S., and Satow, Y. (1971). Sodium and calcium-dependent spike potentials in the secretory neurons soma of the X-organ of the crayfish.J. Gen. Physiol. 57:216–238.
Iwasaki, S., and Satow, Y. (1972). Electrical characteristics of the membrane in neurosecretory neurons. InNeuroendocrine Control (K. Yagi and S. Yoshida, Eds.), Wiley, New York, pp. 85–109.
Jaros, P. (1990). Enkephalins, biologically active neuropeptides in invertebrates, with special reference to crustaceans. InFrontiers in Crustacean Neurobiology (K. Wieseet al., Eds.), Birkhauser Verlag, Basel, pp. 471–482.
Johnston, G. A. R. (1986). Multiplicity of GABA receptors. InBenzodiazepine/GABA Receptors and Chloride Channels; Structural and Functional Properties (R. Olsen and J. C. Venter, Eds.), Alan R. Liss, New York, pp. 57–71.
Kirk, M. D., and Glantz, R. M. (1982). A visually induced GABA mediated IPSP in a crustacean neurosecretory cell.Neurosci. Abstr. 8:532.
Kirk, M. D., Prugh, J. I., and Glantz, R. M. (1983). Retinal illumination produces synaptic inhibition of a neurosecretory organ in the crayfish, Pacifastacus leniusculus (Dana).J. Neurobiol. 14:473–480.
Llano, I., Lereshe, N., and Marty, A. (1991). Calcium entry increases the sensitivity of cerebelar Purkinje Cells to applied GABA and decreases inhibitory synaptic currents.Neuron 6:567–574.
Lunt, G. G. (1991). GABA and GABA receptors in invertebrates.Semin. Neurosci. 3:251–258.
Martínez, J. J., Onetti, C. G., García, E., and Hernández, S. (1991). Potassium current kinetics in bursting secretory neurons: Effects of intracellular calcium.J. Neurophys. 66:1455–1461.
Mazda, G. Y., Nistri, A., and Sivilotti, L. (1990). The effect of GABA on the frog optic tectum is sensitive to ammonium and to penicillin.Eur. J. Pharmacol. 179:111–118.
Mouginot, D., Feltz, P., and Schlichter, R. (1991). Modulation of GABA-gated chloride currents by intracellular Ca2+ in cultured porcine melanotrophs.J. Physiol. 437:109–132.
Nagano, M., and Cooke, I. M. (1981). Electrical activity in the crab X organ-sinus gland system. Site of initiation, ionic bases and pharmacology. inNeurosecretory Molecules, Cells, Systems (D. S. Farner and K. Lederis, Eds.), Plenum Press, New York, pp. 504–404.
Nagano, M., and Cooke, I. M. (1987). Comparison of electrical responses of terminals, axons, and somata of a peptidergic neurosecretory system.J. Neurosci. 7:634–648.
Nistri, A., and Constanti, A. (1979). Pharmacological characterization of different types of GABA and glutamage receptors in vertebrates and invertebrates.Prog. Neurobiol. 13:117–235.
Nistri, A., and Sivilotti, L. (1985). An unusual effect of γ-aminobutyric acid on synaptic transmission on frog tectal neuronesin vitro.Br. J. Pharmacol. 85:917–922.
Onetti, C. G., García, U., Valdiosera, R. F., and Aréchiga, H. (1990). Ionic currents in crustacean neurosecretory cells.J. Neurophysiol. 64:1514–1526.
Pfeiffer-Linn, C., and Glantz, R. M. (1989). Acetylcholine and GABA mediate opposing actions on neuronal chloride channels in crayfish.Science 245:1249–1251.
Pfeiffer-Linn, C., and Glantz, R. M. (1991). GABA-mediated inhibition of visual interneurons in the crayfish medulla.J. Comp. Physiol. A 168:373–381.
Russell, J. M., and Brown, A. M. (1972). Active transport of chloride by the giant neuron of the Aplysia abdominal ganglion.J. Gen. Physiol. 60:499–518.
Sansom, N. S. P., and Usherwood, P. N. R. (1990). Single-channel studies of glutamate receptors.Int. Rev. Neurobiol. 32:51–106.
Sivilotti, L., and Nistri, A. (1989). Pharmacology of a novel effect ofγ-aminobutyric acid on the frog optic tectumin vitro.Eur. J. Pharmacol. 164:205–215.
Stuenkel, E. L. (1985). Simultaneous monitoring of electrical secretory activity in peptidergic neurosecretory terminals of the crab.J. Physiol. Lond. 359:163–187.
Takeuchi, A. (1976). Studies of inhibitory effects of GABA in invertebrate nervous system. InGABA in Nervous System Function (E. Roberts, T. N. Chase, and D. B. Tower, Eds.), Raven Press, New York, pp. 255–267.
Yarowsky, P. J., and Carpenter, D. P. (1978). Receptors for gamma-aminobutyric acid (GABA) on Aplysia neurons.Brain Res. 144:75–94.
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García, U., Onetti, C., Valdiosera, R. et al. Excitatory action of γ-aminobutyric acid (GABA) on crustacean neurosecretory cells. Cell Mol Neurobiol 14, 71–88 (1994). https://doi.org/10.1007/BF02088590
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DOI: https://doi.org/10.1007/BF02088590