Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-26T05:08:56.615Z Has data issue: false hasContentIssue false
  • English
  • Français

Comparison of the responses to light and to GABA of cells postsynaptic to barnacle photoreceptors (I-cells)

Published online by Cambridge University Press:  02 June 2009

Joseph C. Callaway  and
Ann E. Stuart
Joseph C. Callaway
Affiliation:
Department of Zoology, University of Washington, Seattle
Ann E. Stuart
Affiliation:
Departments of Physiology and Ophthalmology, University of North Carolina at Chapel Hill, Chapel Hill
Get access Rights & Permissions [Opens in a new window]

Abstract

We tested the hypothesis that gamma-aminobutyric acid (GABA) is the transmitter released by barnacle photoreceptors onto postsynaptic cells (I-cells). GABA was applied to I-cells either by superfusion or by ejecting it with pressure from a pipette positioned close to the I-cell's soma. The I-cell's response to GABA was compared with its response to light (i.e. to the photoreceptors' transmitter) by recording intracellularly from its soma. Bath-applied (100 µm to 10 mM) and pressure-applied GABA (10 mM in pipette) hyperpolarizes I-cells by increasing their conductance, as does the photoreceptors' transmitter. The response to pressure-applied GABA consists of two components; both persist when Co2+ or Cd2+ are added to the saline to block synaptic transmission in the preparation, indicating that GABA affects the I-cell directly rather than affecting a presynaptic cell. GABA hyperpolarizes the I-cell when applied to the cell over the soma and ipsilateral arbor or over the contralateral arbor. The I-cells' responses to GABA and to light both depend on extracellular K+ and are affected by changes in intracellular and extracellular Cl−. However, picrotoxin and β-guanidinopropionic acid block the response to pressure-applied GABA but do not block the response to light even at an order of magnitude higher concentration. Thus, GABA is not likely to be the transmitter that causes the hyperpolarizing response of the I-cell. It may be a neuromodulator or the transmitter of an unknown input to the I-cell.

Keywords

GABAPhotoreceptorSynapsePicrotoxinBarnacle
Type
Research Articles
Information
Visual Neuroscience , Volume 3 , Issue 4 , October 1989 , pp. 301 - 310
Copyright
Copyright © Cambridge University Press 1989

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

Ariel, M., Lasater, E.M., Mangel, S.C. & Dowling, J.E. (1984). On the sensitivity of H1 horizontal cells of the carp retina to glutamate, aspartate, and their agonists. Brain Research 295, 179–183.Google Scholar
Blume, A.J. (1978). Interaction of ligands with the opiate receptors of brain membranes: regulation by ions and nucleotides. Proceedings of the National Academy of Sciences of the U.S.A. 75, 1713–1717.Google Scholar
Bowery, N.G., Hill, D.R. & Hudson, A.L. (1983). Characteristics of GABA receptor binding sites on rat whole brain synaptic membranes. British Journal of Pharmacology 78, 191–206.Google Scholar
Callaway, J.C. & Edwards, J.S. (1987). GABA-like immunoreactivity in the photoreceptors and supraesophageal ganglion of the barnacle (Balanus nubilus). Society for Neuroscience Abstracts 13, 233.Google Scholar
Callaway, J.C. & Stuart, A.E. (1986). Cells postsynaptic to barnacle photoreceptors are sensitive to GABA. Biological Bulletin 171, 491–492.Google Scholar
Callaway, J.C. & Stuart, A.E. (1987). The effect of strontium, barium, and strychnine on the synapse made by barnacle photoreceptors. Biological Bulletin 173, 441.Google Scholar
Callaway, J.C. & Stuart, A.E. (1989). Biochemical and physiological evidence that histamine is the transmitter of barnacle photoreceptors. Visual Neuroscience 3, 311–325.Google Scholar
Callaway, J.C., Stuart, A.E. & Edwards, J.S. (1988). Immunocytochemical localization of histamine in the photoreceptors and segmental ganglia of the barnacle (Balanus nubilus). Society for Neuroscience Abstracts 14, 381.Google Scholar
Callaway, J.C., Stuart, A.E. & Edwards, J.S. (1989). Immunocytochemical evidence for the presence of histamine and GABA in the photoreceptors of the barnacle (Balanus nubilus). Visual Neuroscience 3, 289–299.CrossRefGoogle ScholarPubMed
Feltz, A. (1972). Competitive interaction of β-guanidinopropionic acid and γ-aminobutyric acid on the muscle fibre of the crayfish. Journal of Physiology (London) 216, 391–401.CrossRefGoogle Scholar
Gerschenfeld, H.M. & Paupardin, D. (1973). Actions of 5-hydroxy-tryptamine on molluscan neuronal membranes. In Drug Receptors, ed. Rang, H.P., pp. 45–61. London, England: MacMillan Press.Google Scholar
Hattori, Y. & Kanno, M. (1985). Effect on Ni2+ on the multiphasic positive onotropic responses to histamine mediated by H1-receptors in left atria of guinea pigs. Naunyn-Schmiedeberg's Archives of Pharmacology 329, 188–194.Google Scholar
Hudspeth, A.J. & Stuart, A.E. (1977). Morphology and responses to light of the soma, axon, and terminal regions of individual photoreceptors of the giant barnacle. Journal of Physiology 272, 1–23.Google Scholar
Ireland, S.J. (1987). Origin of 5-hydroxytryptamine-induced hyperpolarization of the rat superior cervical ganglion and vagus nerve. British Journal of Pharmacology 92, 407–416.CrossRefGoogle ScholarPubMed
Koike, H. & Tsuda, K. (1980). Cellular synthesis and axonal transport of gamma-aminobutyric acid in a photoreceptor cell of the barnacle. Journal of Physiology 305, 125–138.Google Scholar
Korn, J.S., Giacchino, J.L., Chamberlain, N.L. & Dingledine, R. (1987). Epileptiform burst activity induced by potassium in the hippocampus and its regulation by GABA-mediated inhibition. Journal of Neurophysiology 57, 325–340.Google Scholar
Oertel, D. & Stuart, A.E. (1981). Transformation of signals by interneurones in the barnacle's visual pathway. Journal of Physiology 311, 127–146.Google Scholar
Oland, L.A. & Stuart, A.E. (1986). Pattern of convergence of the receptors of the barnacle's three ocelli onto second-order cells. Journal of Neurophysiology 55, 882–895.CrossRefGoogle Scholar
Oland, L.A., French, K.A., Hayashi, J.H. & Stuart, A.E. (1983). Lateral visual pathway of giant barnacle. Journal of Neurophysiology 49, 516–527.CrossRefGoogle ScholarPubMed
Oland, L.A., Stuart, A.E., Hayashi, J.H. & Callaway, J.C. (1987). Voltage spread in an identified interneuron of the barnacle's visual system. Journal of Neurophysiology 58, 1420–1430.Google Scholar
Peters, J.A., Hales, T.G. & Lambert, J.J. (1988). Divalent cations modulate 5-HT3 receptor-induced currents in N1E-115 neuroblastoma cells. European Journal of Pharmacology 151, 491–495.Google Scholar
Ross, W.N. & Stuart, A.E. (1978). Voltage-sensitive calcium channels in the presynaptic terminals of a decrementally conducting photo-receptor. Journal of Physiology 274, 173–191.Google Scholar
Rouot, B.M., U'Prichard, D.C. & Snyder, S.H. (1980). Multiple α2-noradrenergic receptor sites in rat brain: selective regulation of high-affinity [3H]Clonidine binding by guanine nucleotides and divalent cations. Journal of Neurochemistry 34, 374–384.Google Scholar
Schnapp, B.J. & Stuart, A.E. (1983). Synaptic contacts between physiologically identified neurons in the visual system of the barnacle. Journal of Neuroscience 3, 1100–1115.Google Scholar
Stansfeld, C.E. & Wallis, D.I. (1984). Generation of an unusual depolarizing response in rabbit primary afferent neurones in the absence of divalent cations. Journal of Physiology (London) 352, 49–72.Google Scholar
Stuart, A.E. & Callaway, J.C. (1987). Physiological and immunocytochemical evidence that barnacle photoreceptors use GABA as a neurotransmitter. Investigative Ophthalmology and Visual Science (Suppl.) 28, 238.Google Scholar
Stuart, A.E. & Oertel, D. (1978). Neuronal properties underlying processing of visual information in the barnacle nervous system. Nature (London) 275, 287–290.Google Scholar
Stuart, A.E., Hayashi, J.H., Moore, J.W. & Davis, R.E. (1986). Currents in the synaptic terminals of barnacle photoreceptors. In Calcium, Neuronal Function, and Transmitter Release, ed. Rahamimoff, R. & Katz, B., pp. 443–455. Boston: Martinus Nijhoff Publishing.Google Scholar
Stuart, A.E., Hayashi, J.H. & Oland, L.A. (1983). Voltage spread in an interneuron of the barnacles visual system. Society for Neuroscience Abstracts 9, 679.Google Scholar
Timpe, L.C. & Stuart, A.E. (1984). Is γ-aminobutyric acid the neurotransmitter of barnacle photoreceptors? Brain Research 307, 225–231.Google Scholar