Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-28T05:21:25.008Z Has data issue: false hasContentIssue false
  • English
  • Français

Biochemical and physiological evidence that histamine is the transmitter of barnacle photoreceptors

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:
Department of Physiology, University of North Carolina at Chapel Hill, Chapel Hill
Get access Rights & Permissions [Opens in a new window]

Abstract

We tested the hypothesis that histamine is the transmitter released by barnacle photoreceptors. Median and lateral ocelli were incubated with 3H-histidine and found to synthesize 3H-histamine, identified by high-voltage electrophoresis. Synthesis could be blocked by the histidine decarboxylase inhibitor (S)-α-fluoromethylhistidine. Histamine was applied to 1-cells either by superfusion or by pressure ejection from a pipette (100 µM or 1 mM histamine) positioned close to the I-cell's soma. When bath-applied at concentrations ranging from 5–100 µM, histamine hyperpolarized the I-cell in a dose-dependent fashion and increased its conductance. At 100 µM, histamine abolished the I-cell's response to light. The response to a pulse of pressure-applied histamine was a hyperpolarization whose amplitude was graded with dose (determined by the duration of the pulse). This response persisted in concentrations of Co2+ and Cd2+ that blocked synaptic transmission from the photoreceptors. Cimetidine, an antagonist of mammalian H2 receptors, markedly decreased the cell's responses both to HA and to light at 100 µM and blocked both responses at 1 mM. Pyrilamine and triprolidine, H1 antagonists, had a complex effect on the I-cell's responses to histamine and to light. Neither H1 nor H2 antagonists, nor histamine itself, affected the voltage or light responses recorded in the presynaptic terminal region, or any phase of calcium-dependent action potentials induced in the terminal in the presence of tetraethylammonium ion. Thus, biochemical, immunocytochemical, and physiological evidence suggests that HA is the transmitter from these photoreceptors to the I-cells. Although gammaaminobutyric acid (GABA) is also present in the photoreceptors, it did not affect the I-cell's responses to light or to histamine when bath-applied at 100 µM. Thus, GABA does not appear to modulate transmission from the photoreceptor to the I-cell.

Keywords

HistaminePhotoreceptorSynapseCimetidineBarnacle
Type
Research Articles
Information
Visual Neuroscience , Volume 3 , Issue 4 , October 1989 , pp. 311 - 325
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

Ashmore, J.F. & Copenhagen, D.R. (1983). An analysis of transmission from cones to hyperpolarizing bipolar cells in the retina of the turtle. Journal of Physiology (London) 340, 569–597.CrossRefGoogle ScholarPubMed
Battelle, B.-A., Calman, B.G., Grieco, F.D., Mleziva, M.B., Callaway, J.C. & Stuart, A.E. (1989). Histamine: a putative afferent neurotransmitter in Limulus eyes. Investigative Ophthalmology and Visual Science (Suppl.) 30, 290.Google Scholar
Beaven, M.A. & Roderick, M.A. (1980). Impromidine, a potent inhibitor of histamine methyltransferase (HMT) and diamine oxidase (DAO). Biochemical Pharmacology 29, 2897–2900.CrossRefGoogle ScholarPubMed
Brown, H.M., Hagiwara, S., Koike, H. & Meech, R.M. (1970). Membrane properties of a barnacle photoreceptor examined by the voltage clamp technique. Journal of Physiology (London) 208, 385–413.Google Scholar
Callaway, J.C. (1989). Biochemical, immunocytochemical, and physiological studies of histamine, CABA, and serotonin in arthropod nervous systems. Ph.D. Thesis, University of Washington, Seattle, Washington.Google Scholar
Callaway, J.C, Masinovsky, B. & Edwards, J.S. (1985). Immunocytochemical study of arthropod neurons with antibodies specific to molluscan small cardioactive peptide and serotonin: a comparative study. Society for Neuroscience Abstracts 11, 326.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). Comparison of the responses to light and to GABA of cells postsynaptic to barnacle photoreceptors (I-cells). Visual Neuroscience, 3, 301–310.CrossRefGoogle ScholarPubMed
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
Claiborne, B.J. & Selverston, A.I. (1984). Histamine as a neurotransmitter in the stomatogastric nervous system of the spiny lobster. Journal of Neuroscience 4, 708–721.CrossRefGoogle ScholarPubMed
Darwin, C. (1854). A Monograph on the Subclass Cirripedia. The Balanidae; the Verrucidae, etc. London: Ray Society.Google Scholar
Edgington, D.R. & Stuart, A.E. (1979). Calcium channels in the high resistivity axonal membrane of photoreceptors of the giant barnacle. Journal of Physiology (London) 294, 433–445.CrossRefGoogle ScholarPubMed
Ellas, M.S. & Evans, P.D. (1983). Histamine in the insect nervous system: distribution, synthesis, and metabolism. Journal of Neurochemistry 41, 562–568.CrossRefGoogle Scholar
Fatt, P. & Katz, B. (1951). An analysis of the end-plate potential recorded with an intracellular electrode. Journal of Physiology (London) 115, 320–370.CrossRefGoogle ScholarPubMed
Garbarg, M., Barbin, G., Rodergas, E. & Schwartz, J.C. (1980). Inhibition of histamine synthesis in brain by α-fluoromethylhistidine, a new irreversible inhibitor: in vitro and in vivo studies. Journal of Neurochemistry 35, 1045–1052.Google Scholar
Gola, M. & Ducreux, C. (1984). A re-excitation mechanism for strychnine-induced doublets in molluscan neurons. Comparative Biochemistry and Physiology 77C, 257–266.Google Scholar
Gruol, D.L. & Weinreich, D. (1979). Cooperative interactions of histamine and competitive antagonism by cimetidine at neuronal histamine receptors in the marine mollusc (Aplysia californica). Neuropharmacology 18, 415–421.CrossRefGoogle ScholarPubMed
Gwilliam, G.F. (1965). The mechanism of the shadow reflex in Cirripedia, II: Photoreceptor cell response, second-order response, and motor cell output. Biological Bulletin 125, 470–485.CrossRefGoogle Scholar
Hardie, R.C. (1987). Is histamine a neurotransmitter in insect photoreceptors? Journal of Comparative Physiology 161, 201–213.Google Scholar
Hardie, R.C. (1988). Effects of antagonists on putative histamine receptors in the first visual neuropile of the housefly (Musca domestica). Journal of Experimental Biology 138, 221–241.CrossRefGoogle Scholar
Hardie, R.C. (1989). A histamine-activated chloride channel underlying synaptic transmission at a photoreceptor synapse. Nature (London) 339, 704–706.Google Scholar
Hayashi, J.H. (1986). Synaptic transmission between the barnacle's photoreceptor and its second-order cell. Ph.D. Thesis, University of North Carolina, Chapel Hill, North Carolina.Google Scholar
Hayashi, J.H., Moore, J.W. & Stuart, A.E. (1985). Adaptation in the input-output relation of the synapse made by the barnacle photoreceptor. Journal of Physiology (London) 368, 179–195.CrossRefGoogle Scholar
Koike, H. (1983). Transmitter substance of barnacle photoreceptor. In The Physiology of Excitable Cells, ed. New York: Alan R. Liss, Inc., pp. 523–534.Google Scholar
Koike, H. & Tsuda, K. (1980). Cellular synthesis and axonal transport of gamma-aminobutyric acid in a photoreceptor cell of the barnacle. Journal of Physiology (London) 305, 125–138.Google Scholar
Kollonitsch, J., Patchett, A.A., Marburg, S., Maycock, A.L., Perkins, L.M., Doldouras, G.A., Duggan, D.E. & Aster, S.D. (1978). Selective inhibitors of biosynthesis of aminergic neurotransmitters. Nature (London) 274, 906–908.CrossRefGoogle ScholarPubMed
Kretz, R., Shapiro, E., Baily, C.H., Chen, M. & Kandel, E.R. (1986). Presynaptic inhibition produced by an identified presynaptic inhibitory neuron, II: Presynaptic conductance changes caused by histamine. Journal of Neurophysiology 55, 131–146.Google Scholar
Laughlin, S.B. & Hardie, R.C. (1978). Common strategies for light adaptation in the peripheral visual systems of fly and dragonfly. Journal of Comparative Physiology 128, 319–340.Google Scholar
Laughlin, S.B., Howard, J. & Blakeslee, B. (1987). Synaptic limitations to contrast coding in the retina of the blowfly (Calliphora). Proceedings of the Royal Society B (London) 231, 437–467.Google ScholarPubMed
Maxwell, G.D., Tait, J.F. & Hildebrand, J.G. (1978). Regional synthesis of neurotransmitter candidates in the CNS of the moth (Manduca sexta). Comparative Biochemistry and Physiology 61C, 109–119.Google Scholar
McCaman, R.E. & Weinreich, D. (1982). On the nature of histamine-mediated slow hyperpolarizing synaptic potentials in identified molluscan neurones. Journal of Physiology (London) 328, 485–506.Google Scholar
McClintock, T.S. (1988). A histamine-gated anion channel suppresses lobster olfactory receptor cell activity. Biological Bulletin 175, 307.Google Scholar
McGeer, P.L., Eccles, J.C. & McGeer, E.G. (1987). Molecular Neurobiology of the Mammalian Brain (2nd edition). New York: Plenum Press.CrossRefGoogle Scholar
Nässel, D.R., Holmqvist, M.H., Hardie, R.C., Hákanson, R. & Sundler, F. (1988). Histamine-like immunoreactivity in photoreceptors of the compound eyes and ocelli of the flies Calliphora erythrocephala and Musca domestica. Cell and Tissue Research 253, 639–646.CrossRefGoogle ScholarPubMed
Oertel, D. & Stuart, A.E. (1981). Transformation of signals by in-terneurones in the barnacle's visual pathway. Journal of Physiology (London) 311, 127–146.CrossRefGoogle Scholar
Pirvola, U., Tuomisto, L., Yamatodani, A. & Panula, P. (1988). Distribution of histamine in the cockroach brain and visual system: an immunocytochemical and biochemical study. Journal of Comparative Neurology 276, 514–526.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 (London) 274, 173–191.Google Scholar
Sarthy, P.V. (1989). Histamine: a neurotransmitter candidate for photoreceptors in Drosophila melanogaster. Investigative Ophthalmology and Visual Science (Suppl.) 30, 290.Google Scholar
Schlemermeyer, E., Schütte, M. & Ammermüller, J. (1989). Immunohistochemical and electrophysiological evidence that histamine is a photoreceptor transmitter in locust ocellar retina. Investigative Ophthalmology and Visual Science (Suppl.) 30, 290.Google Scholar
Schwartz, J.C., Arrang, J.M., Garbarg, M. & Korner, M. (1986). Properties and roles of the three subclasses of histamine receptors in brain. Journal of Experimental Biology 124, 203–224.Google Scholar
Schwartz, J.H., Elste, A., Shapiro, E. & Gotoh, H. (1986). Biochemical and morphological correlates of transmitter type in C2, an identified histaminergic neuron in Aplysia. Journal of Comparative Neurology 245, 401–421.CrossRefGoogle ScholarPubMed
Shapiro, B.I., Wang, C.M. & Narahashi, T. (1974). Effects of strychnine on ionic conductances of squid axon membrane. Journal of Pharmacology and Experimental Therapeutics 188, 66–76.Google ScholarPubMed
Simmons, P.J. & Hardie, R.C. (1988). Evidence that histamine is a neurotransmitter of photoreceptors in the locust ocellus. Journal of Experimental Biology 138, 205–209.CrossRefGoogle Scholar
Stockbridge, N. & Ross, W.N. (1984). Localized Ca2+ and calcium-activated potassium conductances in terminals of a barnacle photoreceptor. Nature (London) 309, 266–268.CrossRefGoogle ScholarPubMed
Stuart, A.E. & Callaway, J.C. (1988). Histamine is synthesized by barnacle ocelli and affects second-order visual cells. Investigative Ophthalmology and Visual Science (Suppl.) 29, 223.Google Scholar
Stuart, A.E., Hayashi, J.H., Moore, J.W. & Davis, R.E. (1986). Currents in the synaptic terminals of barnacle photoreceptor. In Calcium, Neuronal Function, and Transmitter Release, ed. Rahaminoff, R. & Katz, B., pp. 443–455. Boston: Martinus Nijhoff Publishing.CrossRefGoogle Scholar
Stuart, A.E. & Oertel, D. (1978). Neuronal properties underlying processing of visual information in the barnacle nervous system. Nature (London) 275, 287–290.CrossRefGoogle Scholar
Timpe, L.C. (1982). The roles of acetylcholine and gamma-aminobutyric acid in the visual system of the barnacle. Ph.D. Thesis, Harvard University, Cambridge, Massachusetts.Google Scholar
Timpe, L.C. & Stuart, A.E. (1984). Is γ-aminobutyric acid the neurotransmitter of barnacle photoreceptors? Brain Research 307, 225–231.CrossRefGoogle ScholarPubMed
Weinreich, D. & Rubin, L. (1981). Irreversible inhibitors of histidine decarboxylase in Aplysia ganglia: a tool for the identification of histaminergic synapses. Comparative Biochemistry and Physiology 69C, 383–385.Google Scholar
Weinreich, D. & Yu, Y.T. (1977). The characterization of histidine decarboxylase and its distribution in nerves, ganglia, and in single neuronal cell bodies from the CNS of Aplysia californica. Journal of Neurochemistry 28, 361–369.CrossRefGoogle ScholarPubMed