Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-23T05:08:21.889Z Has data issue: false hasContentIssue false
  • English
  • Français

A role for 5HT3 receptors in visual processing in the mammalian retina

Published online by Cambridge University Press:  02 June 2009

William J. Brunken  and
Xiao-Tao Jin
William J. Brunken
Affiliation:
Department of Biology, Boston College, Chestnut Hill
Xiao-Tao Jin
Affiliation:
Department of Biology, Boston College, Chestnut Hill
Get access Rights & Permissions [Opens in a new window]

Abstract

We investigated the role of 5HT3 receptors in the mammalian retina using electrophysiological techniques to monitor ganglion cell activity. Activation of 5HT3 receptors with the selective agonist 1-phenylbiguanide (PBG) increased the ON responses of ON-center ganglion cells, while decreasing the OFF responses of OFF-center cells. The application of a selective 5HT3 antagonist had a reciprocal effect, namely it reduced the center response in ON-center cells and concomitantly increased the center responses in OFF-center cells. Since putative serotoninergic amacrine cells in the retina are connected specifically to the rod bipolar cell, these agents most likely affect the rod bipolar terminal. These data, together with previous studies, suggest that both 5HT2 and 5HT3 receptors mediate an excitatory influence which serves to facilitate the output from rod bipolar cells, the former via a phosphatidyl inositol second-messenger system, and the latter via a direction channel.

Keywords

RetinaSerotoninRabbitGanglion cells5HT3 receptorsRod pathways
Type
Articles
Information
Visual Neuroscience , Volume 10 , Issue 3 , May 1993 , pp. 511 - 522
Copyright
Copyright © Cambridge University Press 1993

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

Ames, A. & Pollen, D.A. (1969). Neurotransmission in central nervous tissue: A study of Isolated rabbit retina. Journal of Neuro-physiology 32, 424–442.CrossRefGoogle ScholarPubMed
Andrade, R. & Chaput, Y. (1991). The electrophysiology of serotonin receptor subtypes. In Serotonin Receptor Subtypes Basic and Clinical Aspects, ed. Peroutka, S.J., pp. 103–124. New York: Wiley-Liss.Google Scholar
Andrade, R. & Nicoll, R.A. (1987). Novel anxiolytics discriminate between postsynaptic serotonin receptors mediating different physiological responses on single neurons of the rat hippocampus. Naunyn-Schmiedebergs Archives of Pharmacology 336, 5–10.CrossRefGoogle ScholarPubMed
Andrade, R. & Nicoll, R.A. (1988). Pharmacologically distinct actions of serotonin on single pyramidal neurones of the rat hippocampus recorded in vitro. Journal of Physiology (London) 394, 99–124.CrossRefGoogle Scholar
Ariel, M. & Daw, N.W. (1982 a). Effects of cholinergic drugs on receptive properties of rabbit retinal ganglion cells. Journal of Physiology (London) 324, 135–160.CrossRefGoogle ScholarPubMed
Ariel, M. & Daw, N.W. (1982 b). Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells. Journal of Physiology (London) 324, 161–185.CrossRefGoogle ScholarPubMed
Barlow, H.B., Fitzhugh, R. & Kuffler, S.W. (1957 a). Dark adaptation, absolute threshold, and Purkinje shift in single units of the cat’s retina. Journal of Physiology (London) 137, 327–337.CrossRefGoogle ScholarPubMed
Barlow, H.B., Fitzhugh, R. & Kuffler, S.W. (1957 b). Change of organization in the receptive filed of the cat’s retina during dark adaptation. Journal of Physiology (London) 137, 338–354.CrossRefGoogle Scholar
Barlow, J.M., Barnes, N.M., Brunken, W.J. & Robertson, D.W. (1991). Identification of 5HT3 receptor recognition sites in rabbit retina. International Conference on 5-Hydroxytryptamine-CNS Receptors and Brain Function 1, 53.Google Scholar
Blazynski, C., Ferrendelli, J.A. & Cohen, A.I. (1985). Indoleamine-sensitive adenylate-cyclase in rabbit retina—Characterization and distribution. Journal of Neurochemistry 45, 440–447.CrossRefGoogle ScholarPubMed
Bobker, D.H. & Williams, J.T. (1990). Ion conductances affected by 5-HT receptor subtypes in mammalian neurons. Trends in Neuro-science 13, 169–173.CrossRefGoogle ScholarPubMed
Brunken, W.J., Jin, X.T. & Pis-Lopez, A.M. (1992). The properties of the serotoninergic system in the retina. In Progress in Retinal Research, Vol. 12, ed. Osborne, N.N. & Chader, G.J., pp. 75–99. Oxford, England: Pergamon Press.Google Scholar
Brunken, W. J. & Daw, N.W. (1986). 5-HTL2 antagonists reduce on responses in the rabbit retina. Brain Research 384, 161–165.CrossRefGoogle ScholarPubMed
Brunken, W. J. & Daw, N.W. (1987). The actions of serotoninergic agonists and antagonists on the activity of brisk ganglion cells in the rabbit retina. Journal of Neuroscience 7, 4054–4065.CrossRefGoogle Scholar
Brunken, W.J. & Daw, N.W. (1988 a). The effects of serotonin agonists and antagonists on the response properties of complex ganglion cells in the rabbit’s retina. Visual Neuroscience 1, 181–188.CrossRefGoogle ScholarPubMed
Brunken, W.J. & Daw, N.W. (1988 b). Neuropharmacological analysis of the role of the indoleamine-accumulating amacrine cells in the rabbit retina. Visual Neuroscience 1, 275–285.CrossRefGoogle ScholarPubMed
Brunken, W.J. & Daw, N.W. (1988 c). 5HT3 receptors in the rabbit retina? Society for Neuroscience Abstracts 14, 846.Google Scholar
Caldwell, J.H. & Daw, N.W. (1978). New properties of rabbit retinal ganglion cells. Journal of Physiology (London) 276, 257–276.CrossRefGoogle ScholarPubMed
Conn, P. J. & Sanders-Bush, E. (1984). Selective 5HT2 antagonists inhibit serotonin-stimulated phosphatidylinositol metabolism in cerebral cortex. Neuropharmacology 23, 993–996.CrossRefGoogle ScholarPubMed
Conn, P.J. & Sanders-Bush, E. (1986). Regulation of serotonin-stimulated phosphoinositide hydrolysis—Relation to the serotonin 5-HT2 binding site. Journal of Neuroscience 6, 3669–3675.CrossRefGoogle Scholar
Cornfield, L.J. & Nelson, D.L. (1991). Biochemistry of 5-hydroxy-tryptamine receptor subtypes—Coupling to second-messenger systems. In Serotonin Receptor Subtypes: Basic and Clinical Aspects, ed. Sanders-Bush, E., pp. 81–102. New York: Wiley-Liss.Google Scholar
Cutcliffe, N. & Osborne, N.N. (1987). Serotonergic and cholinergic stimulation of inositol phosphate formation in the rabbit retina. Evidence for the presence of serotonin and muscarinic receptors. Brain Research 421, 95–104.CrossRefGoogle ScholarPubMed
DeVivo, M. & Maayani, S. (1986). Characterization of the 5-hydroxy-tryptamine receptor-mediated inhibition of forskolin-stimulated adenylate cyclase activity in guinea pig and rat hippocampal membranes. Journal of Pharmacology and Experimental Therapeutics 238, 248–253.Google Scholar
Dolan, R.P. & Schiller, P.H. (1989). Evidence for only depolarizing rod bipolar cells in the primate retina. Visual Neuroscience 2, 421–424.CrossRefGoogle ScholarPubMed
Ehinger, B. & Floren, I. (1978). Quantitation of the uptake of indole-amines and dopamine in the rabbit retina. Experimental Eye Research 26, 1–11.CrossRefGoogle Scholar
Ehinger, B. & Holmgren, I. (1979). Electron microscopy of the indoleamine-accumulating neurons of the indoleamine-accumulating neurons in the retina of the rabbit. Cell and Tissue Research 197, 175–194.CrossRefGoogle ScholarPubMed
Grünert, U. & Martin, P.R. (1991). Rod bipolar cells in the macaque monkey retina: Immunoreactivity and connectivity. Journal of Neuroscience 11, 2742–2758.CrossRefGoogle ScholarPubMed
Holmgren-Taylor, I. (1982). Electron microscopic observation on the indoleamine accumulating neurons and their synaptic connections in the retina of the cat. Journal of Comparative Neurology 208, 144–156.CrossRefGoogle ScholarPubMed
Holohean, A.M., Hackman, J.C. & Davidoff, R.A. (1990). Changes in membrane potential of frog motoneurons induced by activation of serotonin receptor subtypes. Neuroscience 34, 555–564.CrossRefGoogle ScholarPubMed
Kilpatrick, G.J., Jones, B.J. & Tyers, M.B. (1987). Identification and distribution of 5-HT3 receptors in rat brain using radioligand binding. Nature 330, 746–748.CrossRefGoogle ScholarPubMed
Levick, W.R. (1967). Receptive fields and trigger features of ganglion cells in the visual streak of the rabbit’s retina. Journal of Physiology (London) 188, 285–307.CrossRefGoogle Scholar
Levick, W.R. (1972). Another tungsten microelectrode. Medical and Biological Engineering 10, 510–515.CrossRefGoogle ScholarPubMed
Mitchell, C.K. & Redburn, D.A. (1985). Analysis of pre- and post-synaptic factors of the serotonin system in rabbit retina. Journal of Cell Biology 100, 64–73.CrossRefGoogle Scholar
Müller, B. & Peichl, L. (1991). Rod bipolar cells in the cone-dominated retina of the tree shrew Tupaia belangeri. Visual Neuroscience 6, 629–639.CrossRefGoogle ScholarPubMed
Müller, F., Wässle, H. & Voigt, T. (1988). Pharmacological modulation of the rod pathway in the cat retina. Journal of Neurophysiology 59, 1657–1672.CrossRefGoogle ScholarPubMed
Nowak, J.Z., Szyc, H. & Nawrocki, J. (1985). Does 5HT play a neu-rotransmitter role in mammalian retina? Studies on uptake and potassium-stimulated release of 14C-5HT and 14C-GABA from bovine and rabbit retinal slices. Polish Journal of Pharmacology and Pharmacy 37, 57–68.Google Scholar
Osborne, N.N. (1981). Binding of [3H]-serotonin to membranes of the bovine retina. Experimental Eye Research 33, 371–380.CrossRefGoogle ScholarPubMed
Osborne, N.N. & Barnett, N.L. (1989). Serotonin levels in the rabbit retina are elevated following intraocular injection of forskolin. Journal of Neurochemistry 53, 1955–1958.CrossRefGoogle ScholarPubMed
Osborne, N.N. & Barnett, N.L. (1990). What constitutes a serotonergic neurone in the retina? Neurochemistry International 17, 177–187.CrossRefGoogle ScholarPubMed
Osborne, N.N. & Beaton, D.W. (1986). Direct histochemical localization of 5,7-dihydroxytryptamine and the uptake of serotonin by a subpopulation of GABA neurones in the rabbit retina. Brain Research 82, 158–162.CrossRefGoogle Scholar
Osborne, N.N. & Ghazi, H. (1991). 5-HT1A receptors positively coupled to C-AMP formation in the rabbit retina. Neurochemistry International 19, 407–411.CrossRefGoogle Scholar
Sandell, J.H. & Masland, R.H. (1986). A system of indoleamine-accumulating neurons in the rabbit retina. Journal of Neuroscience 6, 3331–3347.CrossRefGoogle ScholarPubMed
Sandell, J.H. & Masland, R.H. (1989). Shape and distribution of an unusual retinal neuron. Journal of Comparative Neurology 280, 489–497.CrossRefGoogle ScholarPubMed
Sandell, J.H., Masland, R.H., Raviola, E. & Dacheux, R.F. (1989). Connections of indoleamine-accumulating cells in the rabbit retina. Journal of Comparative Neurology 283, 303–313.CrossRefGoogle ScholarPubMed
Skrandies, W. & Wässle, H. (1988). Dopamine and serotonin in cat retina—Electroretinography and histology. Experimental Brain Research 71, 231–240.CrossRefGoogle Scholar
Sprouse, J.S. & Aghajanian, G.K. (1988). Responses of hippocampal pyramidal cells to putative serotonin 5-HT1A and 5-HT1B agonists: A comparative study with dorsal raphe neurons. Neuropharmacology 27, 707–715.CrossRefGoogle ScholarPubMed
Strettoi, E., Dacheux, R.F. & Raviola, E. (1990). Synaptic connections of rod bipolar cells in the inner plexiform layer of the rabbit retina. Journal of Comparative Neurology 295, 449–466.CrossRefGoogle ScholarPubMed
Sugita, S., Shen, K.-Z. & North, R.A. (1992). 5-hydroxytryptamine is a fast excitatory transmitter at 5-HT3 receptors in rat amygdala. Neuron 8, 199–203.CrossRefGoogle ScholarPubMed
Thier, P. & Wässle, H. (1984). Indoleamine-mediated reciprocal modulation of ON-centre and OFF-centre ganglion cell activity in the retina of the cat. Journal of Physiology (London) 351, 613–630.CrossRefGoogle ScholarPubMed
Todorovic, S.M. & Anderson, E.G. (1990 a). Pharmacological characterization of 5-hydroxytryptamine2 and 5-hydroxytryptamine3 receptors in rat dorsal root ganglion cells. Journal of Pharmacology and Experimental Therapeutics 254, 109–115.Google ScholarPubMed
Todorovic, S. & Anderson, E.G. (1990 b). 5-HT2 and 5-HT3 receptors mediate two distinct depolarizing responses in rat dorsal root ganglion neurons. Brain Research 511, 71–79.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1986). Morphological identification of serotonin-accumulating neurons in the living retina. Science 233, 444–446.CrossRefGoogle ScholarPubMed
Vaney, D.I., Young, H.M. & Gynther, I.C. (1991). The rod circuit in the rabbit retina. Visual Neuroscience 7, 141–154.CrossRefGoogle ScholarPubMed
Wässle, H. & Chun, M.H. (1988). Dopaminergic and indoleamine-accumulating amacrine cells express GABA-like immunoreactivity in the cat retina. Journal of Neuroscience 8, 3383–3394.CrossRefGoogle ScholarPubMed
Yakel, J.L. & Jackson, M.B. (1988). 5-HT3 receptors mediate rapid responses in cultured hippocampus and a clonal cell line. Neuron 1, 615–621.CrossRefGoogle Scholar
Yakel, J.L., Shao, X.M. & Jackson, M.B. (1990). The selectivity of the channel coupled to the 5-HT3 receptor. Brain Research 533, 46–52.CrossRefGoogle Scholar
Yakel, J.L., Trussell, L.O. & Jackson, M.B. (1988). Three serotonin responses in cultured mouse hippocampal and striatal neurons. Journal of Neuroscience 8, 1273–1285.CrossRefGoogle ScholarPubMed