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MLA-sensitive cholinergic receptors involved in the detection of complex moving stimuli in retina

Published online by Cambridge University Press:  25 February 2005

B.T. REED ,
K.T. KEYSER  and
F.R. AMTHOR
B.T. REED
Affiliation:
Vision Science Research Center, University of Alabama at Birmingham, Birmingham
K.T. KEYSER
Affiliation:
Vision Science Research Center, University of Alabama at Birmingham, Birmingham
F.R. AMTHOR
Affiliation:
Department of Psychology, University of Alabama at Birmingham, Birmingham
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Abstract

Acetylcholine, acting through nicotinic acetylcholine receptors, mediates the response properties of many ganglion cells in the rabbit retina, including those that are directionally selective (DS; Ariel & Daw, 1982a,b). For example, Grzywacz et al. (1998) showed that cholinergic input is necessary for DS responses to drifting gratings, a form of textured stimulus. However, the identities and locations of the neuronal acetylcholine receptor (nAChR) subtypes that mediate this input are not clear (Keyser et al., 2000). We investigated the role of methyllycaconitine-sensitive, α7-like nAChRs in mediating DS responses to textured stimuli and apparent motion. We recorded extracellularly from On–Off DS ganglion cells in rabbit retina using everted eyecup preparations. Our data provide evidence that MLA-sensitive nAChRs are involved in mediating directionally selective responses to apparent motion and to a variety of complex, textured stimuli such as drifting square-wave gratings, transparent motion, and second-order motion.

Keywords

AcetylcholineRetinal ganglion cellsα-bungarotoxinNicotinic acetylcholine receptorsMLATransparent motionSecond-order motionα7
Type
Research Article
Information
Visual Neuroscience , Volume 21 , Issue 6 , November 2004 , pp. 861 - 872
Copyright
© 2004 Cambridge University Press

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References

REFERENCES

Albuquerque, E.X., Pereira, E.F., Braga, M.F., & Alkondon, M. (1998). Contribution of nicotinic receptors to the function of synapses in the central nervous system: The action of choline as a selective agonist of alpha 7 receptors. Journal of Physiology 92, 309–316.Google Scholar
Alkondon, M., Pereira, E.F.R., Wonnacott, S., & Albuquerque, E.X. (1992). Blockade of nicotinic currents in hippocampal neurons defines methyllycaconitine as a potent and specific receptor antagonist. Molecular Pharmacology 41, 802–808.Google Scholar
Alkondon, M., Pereira, E.F.R., & Albuquerque, E.X. (1998). α-Bungarotoxin- and methyllycaconitine-sensitive nicotinic receptors mediate fast synaptic transmission in interneurons of rat hippocampal slices. Brain Research 810, 257–263.Google Scholar
Ames, A. & Pollen, D.A. (1969). Neurotransmission in central nervous tissue, a study of isolated rabbit retina. Journal of Neurophysiology 32, 424–442.Google Scholar
Ames, A. & Nesbett, F.B. (1981). In vitro retina as an experimental model of the central nervous system. Journal of Neurochemistry 37, 867–877.Google Scholar
Amthor, F.R., Oyster, C.W., & Takahashi, E.S. (1984). Morphology of ON–OFF direction-selective ganglion cells in the rabbit retina. Brain Research 298, 187–190.Google Scholar
Amthor, F.R., Takahashi, E.S., & Oyster, C.W. (1989). Morphologies of rabbit retinal ganglion cells with complex receptive fields. Journal of Comparative Neurology 280, 97–121.Google Scholar
Amthor, F.R. & Grzywacz, N.M. (1993). Inhibition in ON–OFF directionally selective ganglion cells in the rabbit retina. Journal of Neurophysiology 69, 2174–2187.Google Scholar
Amthor, F.R., Grzywacz, N.M., & Merwine, D.K. (1996). Extra-receptive-field motion facilitation in On–Off directionally selective ganglion cells of the rabbit retina. Visual Neuroscience 13, 303–309.Google Scholar
Ariel, M. & Daw, N.W. (1982a). Effects of cholinergic drugs on receptive field properties of rabbit retinal ganglion cells. Journal of Physiology 324, 135–160.Google Scholar
Ariel, M. & Daw, N.W. (1982b). Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells. Journal of Physiology 324, 161–185.Google Scholar
Armstrong-James, M. & Millar, J., (1979). Carbon fibre microelectrodes. Journal of Neuroscience Methods 1, 279–287.Google Scholar
Baldridge, W.H. (1996). Optical recordings of the effects of cholinergic ligands on neurons in the ganglion cell layer of mammalian retina. Journal of Neuroscience 16, 5060–5072.Google Scholar
Barlow, H.B. & Hill, R.M. (1963). Selective sensitivity to direction of movement in ganglion cells of the rabbit retina. Science 139, 412–414.Google Scholar
Barlow, H.B., Hill, R.M., & Levick, W.R. (1964). Retinal ganglion cells responding selectively to direction and speed of image motion in the rabbit. Journal of Physiology 173, 377–407.Google Scholar
Barlow, H.B. & Levick, W.R. (1965). The mechanism of directionally selective units in rabbit's retina. Journal of Physiology 178, 477–504.Google Scholar
Brioni, J.D., Decker, M.W, Sullivan, J.P., & Arneric, S.P. (1997). The pharmacology of (-)-nicotine and novel cholinergic channel modulators. Advances in Pharmacology 37, 153–214.Google Scholar
Britten, K.H., Shadlen, M.N., Newsome, W.T., & Movshon, J.A. (1993). Responses of neurons in macaque MT to stochastic motion signals. Visual Neuroscience 10, 1157–1169.Google Scholar
Caldwell, J.H., Daw, N.W., & Wyatt H.J. (1978). Effects of picrotoxin and strychnine on rabbit retinal ganglion cells: Lateral interactions for cells with more complex receptive fields. Journal of Physiology 276, 277–298.Google Scholar
Chang, K.T. & Berg, D.K. (1999). Nicotinic acetylcholine receptors containing α7 subunits are required for reliable synaptic transmission in situ. Journal of Neuroscience 19, 3701–3710.Google Scholar
Chavez-Noriega, L.E., Crona, J.H., Washburn, M.S., Urrutia, A., Elliott, K.J., & Johnson, E.C. (1997). Pharmacological characterization of recombinant human neuronal nicotinic acetylcholine receptors hα2β2, hα2β4, hα3β2, hα3β4, hα4β2, hα4β4 and hα7 expressed in xenopus oocytes. Journal of Pharmacology and Experimental Therapeutics 280, 346–356.Google Scholar
Chiao, C. & Masland, R.H. (2002). Starburst cells nondirectionally facilitate the responses of direction-selective retinal ganglion cells. Journal of Neuroscience 22, 10509–10513.Google Scholar
Cohen, E.D. & Miller, R.F. (1995). Quinoxalines block the mechanism of directional selectivity in ganglion cells of the rabbit retina. Proceedings of the National Academy of Sciences of the U.S.A. 92, 1127–1131.Google Scholar
Demb, J.B., Zaghloul, K., & Sterling, P. (2001). Cellular basis for the response to second-order motion cues in Y retinal ganglion cells. Neuron 22, 711–721.Google Scholar
Famiglietti, E.V., Jr. (1983). “Starburst” amacrine cells and cholinergic neurons: Mirror-symmetric On and Off amacrine cells of rabbit retina. Brain Research 261, 138–144.Google Scholar
Fried, S.I., Münch, T.A., & Werblin, F.S. (2002). Mechanisms and circuitry underlying directional selectivity in the retina. Nature 420, 411–414.Google Scholar
Grzywacz, N.M. & Amthor, F.R. (1989). A computationally robust anatomical model for retinal directional selectivity. In Advances in Neural Information Processing Systems I, ed. Touretzky, D.S., pp. 477–484. San Mateo, California: Morgan Kaufman.
Grzywacz, N.M. & Amthor, F.R. (1993). Facilitation in On–Off directionally selective ganglion cells in the rabbit retina. Journal of Neurophysiology 69, 2188–2199.Google Scholar
Grzywacz, N.M., Tootle, J.S., & Amthor, F.R. (1997). Is the input to a GABAergic or cholinergic synapse the sole asymmetry in rabbit's retinal directional selectivity? Visual Neuroscience 14, 39–54.Google Scholar
Grzywacz, N.M., Amthor, F.R., & Merwine, D.K. (1998). Necessity of acetylcholine for retinal directionally selective responses to drifting gratings in rabbit. Journal of Physiology 512, 575–581.Google Scholar
He, S. & Masland, R.H. (1997). Retinal direction selectivity after targeted laser ablation of starburst amacrine cells. Nature 389, 378–382.Google Scholar
Keyser, K.T., MacNeil, M.A., Dmitrieva, N., Wang, F., Masland, R.H., & Lindstrom, J.M. (2000). Amacrine, ganglion, and displaced amacrine cells in the rabbit retina express nicotinic acetylcholine receptors. Visual Neuroscience 17, 743–752.Google Scholar
Kittila, C.A. & Massey, S.C. (1997). Pharmacology of directionally selective ganglion cells in the rabbit retina. Journal of Neurophysiology 77, 675–689.Google Scholar
Klink, R., de Kerchove d'Exaerde, A., Zoli, M., & Changeux, J.P. (2001). Molecular and physiological diversity of nicotinic acetylcholine receptors in the midbrain dopaminergic nuclei. Journal of Neuroscience 21, 1452–1463.Google Scholar
Le Novere, N., Corringer, P.J., & Changeux, J.P. (2002). The diversity of subunit composition in nAChRs: Evolutionary origins, physiologic and pharmacologic consequences. Journal of Neurobiology 53, 447–456.Google Scholar
Lindstrom, J.M. (2000). The structures of neuronal nicotinic receptors. In Handbook of Experimental Pharmacology, ed. Clementi, F., Fornasari, D. & Gotti, C., pp. 101–162. Berlin-Heidelburg: Springer-Verlag.
MacAllan, D.R.E., Lunt, G.G., Wonnacott, S., Swanson, K.L., Rapoport, H., & Albuquerque, E.X. (1988). Methyllycaconitine and (+)-anatoxin-a differentiate between nicotinic receptors in vertebrate and invertebrate nervous systems. FEBS Letters 226, 357–363.Google Scholar
Marc, R.E., Murry, R.F., & Basinger, S.F. (1995). Pattern recognition of amino acid signatures in retinal neurons. Journal of Neuroscience 15, 5106–5129.Google Scholar
Mariani, A.P. & Hersh, L.B. (1988). Synaptic organization of cholinergic amacrine cells in the rhesus monkey retina. Journal of Comparative Neurology 267, 269–280.Google Scholar
Masland, R.H. & Ames, A. (1976). Responses to acetylcholine of ganglion cells in an isolated mammalian retina. Journal of Neurophysiology 32, 424–442.Google Scholar
Masland, R.H., Mills, J.W., & Cassidy, C. (1984). The functions of acetylcholine in the rabbit retina. Proceedings of the Royal Society B (London) 223, 121–139.Google Scholar
Massey, S.C. & Neal, M.J. (1979). The light evoked release of acetylcholine from rabbit retina in vivo and its inhibition by gamma-aminobutyric acid. Journal of Neurochemistry 32, 1327–1329.Google Scholar
Massey, S.C. & Redburn, D.A. (1982). A tonic gamma-aminobutyric acid mediated inhibition of cholinergic amacrine cells in the rabbit retina. Journal of Neuroscience 2, 1633–1643.Google Scholar
Massey, S.C. & Miller, R.F. (1988). Glutamate receptors of ganglion cells in the rabbit retina: Evidence for glutamate as a bipolar cell transmitter. Journal of Physiology 405, 635–655.Google Scholar
Massey, S.C. & Miller, R.F. (1990). N-methyl-D-aspartate receptors of ganglion cells in rabbit retina. Journal of Neurophysiology 63, 16–30.Google Scholar
McGehee, D.S., Heath, M.J., Gelber, S., Devay, P., & Role, L.W. (1995). Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors. Science 269, 1692–1696.Google Scholar
McReynolds, J.S. & Miyachi, E. (1986). The effect of cholinergic agonists and antagonists on ganglion cells in the mudpuppy retina. Neuroscience Research (Suppl.) 4, S153–S161.Google Scholar
Nakayama, H., Shioda, S., Nakajo, S., Ueno, S., Nakashima, T., & Nakai, Y. (1997). Immunocytochemical localization of nicotinic acetylcholine receptor in the rat cerebellar cortex. Neuroscience Research 29, 233–239.Google Scholar
Nambi Aiyar, V., Benn, M.H., Hanna, T., Jacyno, J., Roth, S.H., & Wilkens, J.L. (1979). The principal toxin of Delphinium brownii Rydb., and its mode of action. Experentia 35, 1367–1368.Google Scholar
Newsome, W.T., Mikami, A., & Wurtz, R.H. (1986). Motion selectivity in macaque visual cortex. III. Psychophysics and physiology of apparent motion. Journal of Neurophysiology 55, 1340–1351.Google Scholar
Nishida, S., Sasaki, Y., Murakami, I., Watnabe, T., & Tootell, R.B.H. (2003). Neuroimaging of direction-selective mechanisms for second-order motion. Journal of Neurophysiology 90, 3242–3254.Google Scholar
Noell, W.K. & Lasansky, A. (1959). Effects of electrophoretically applied drugs and electric currents on ganglion cells of the retina. Federation Proceedings 18, 115.Google Scholar
Ölveczky, B.P., Baccus, S.A., & Meister, M. (2003). Segregation of object and background motion in the retina. Nature 423, 401–408.Google Scholar
Papke, R.L., Bencheif, M., & Lippiello, P. (1996). An evaluation of nicotinic acetylcholine receptor activation by quaternary nitrogen compounds indicates that choline is selective for the α7 subtype. Neuroscience Letters 213, 201–204.Google Scholar
Papke, R.L., Meyer, E., & Uteshev, V.V. (2000). α7 receptor-selective agonists and modes of α7 receptor activation. European Journal of Pharmacology 393, 179–195.Google Scholar
Pourcho, R.G. (1979). Localization of cholinergic synapses in mammalian retina with peroxidase-conjugated α-bungarotoxin. Vision Research, 19, 287–292.Google Scholar
Quick, M.W. & Lester, R.A.J. (2002). Desensitization of neuronal nicotinic receptors. Journal of Neurobiology 53, 457–478.Google Scholar
Reed, B.T., Amthor, F.R., & Keyser, K.T. (2000). Pharmacological analysis of nicotinic receptors in rabbit retinal ganglion cells (Abstract). Investigative Ophthalmology and Visual Science (Suppl.) 41, S251.Google Scholar
Reed, B.T., Amthor, F.R., & Keyser, K.T. (2001). Pharmacological analysis shows multiple nAChR subtypes in rabbit retina and a possible role for the α7 subtype in directional selectivity (Abstract). Investigative Ophthalmology and Visual Science (Suppl.) 42, 5677.Google Scholar
Reed, B.T., Amthor, F.R., & Keyser, K.T. (2002a). Rabbit retinal ganglion cell responses mediated by α-bungarotoxin-sensitive nicotinic acetylcholine receptors. Visual Neuroscience 19(4), 427–438.Google Scholar
Reed, B.T., Strang, C.E., Brockway, F.R., Amthor, F.R., & Keyser, K.T. (2002b). MLA sensitivity in the rabbit retina is mediated by functional α7 nAChRs (Abstract). Investigative Ophthalmology and Visual Science (Suppl.) 43, 4770.Google Scholar
Schwartz, I.R. & Bok, D. (1979). Electron microscopic localization of [125I]α-bungarotoxin binding sites in the outer plexiform layer of the goldfish retina. Journal of Neurocytology 8, 53–66.Google Scholar
Seguela, P., Wadiche, J., Dineley-Miller, K., Dani, J.A., & Patrick, J.W. (1993). Molecular cloning, functional properties, and distribution of rat brain α7, a nicotinic cation channel highly permeable to calcium. Journal of Neuroscience 13, 596–604.Google Scholar
Snowden, R.J., Treue, S., Erickson, R.G., & Andersen, R.A. (1991). The response of area MT and V1 neurons to transparent motion. Journal of Neuroscience 11, 2768–2785.Google Scholar
Strang, C.E., Reed, B.T., Renna, J.M., Amthor, F.R., & Keyser, K.T. (2002). Nicotinic receptor subtypes in rabbit retina (Abstract). In Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience 37. 1.
Strang, C.E., Amthor, F.R., & Keyser, K.T. (2003). Rabbit brisk ganglion cells express functional β2-containing nicotinic acetylcholine receptors. Visual Neuroscience 20, 651–662.Google Scholar
Straschill, M. (1968). Action of drugs on single neurons in the cat's retina. Vision Research 8, 35–47.Google Scholar
Straschill, M. & Perwein, J. (1973). The effect of iontophoretically applied acetylcholine upon the cat's retinal ganglion cells. Pflügers Archives 339, 289–298.Google Scholar
Tauchi, M. & Masland, R.H. (1984). The shape and arrangement of the cholinergic neurons in the rabbit retina. Proceedings of the Royal Society B (London) 223, 101–109.Google Scholar
Vijayaraghavan, S., Pugh, P.C., Zhong-wei, Z., Rathouz, M.M., & Berg, D.K. (1992). Nicotinic receptors that bind α-bungarotoxin on neurons raise intracellular free Ca2+. Neuron 8, 353–362.Google Scholar
Vogel, Z. & Nirenberg, M. (1976). Localization of acetylcholine receptors during synaptogenesis in retina. Proceedings of the National Academy of Sciences USA 73, 1806–1810.Google Scholar
Vogel, Z., Maloney, G.J., Ling, A., & Daniels, M.P. (1977). Identification of acetylcholine receptor sites in retina with peroxidase-labeled α bungarotoxin. Proceedings of the National Academy of Sciences of the U.S.A. 74, 3268–3272.Google Scholar
Ward, J.M., Cockcroft, V.B., Lunt, G.G., Smillie, F.S., & Wonnacott, S. (1990). Methyllycaconitine, a selective probe for neuronal α-bungarotoxin binding sites. FEBS Letters 270, 45–48.Google Scholar
Wyatt, H.J. & Daw, N.W. (1975). Directionally sensitive ganglion cells in the rabbit retina: Specificity for stimulus direction, size and speed. Journal of Neurophysiology 38, 613–626.Google Scholar
Yamada, E.S., Dmitrieva, N., Keyser, K.T., Lindstrom, J.M., Hersh, L.B., & Marshak, D.W. (2003). Synaptic connections of starburst amacrine cells and localization of acetylcholine receptors in primate retinas. Journal of Comparative Neurology 46, 76–90.Google Scholar
Yang, G. & Masland, R.H. (1994). Receptive fields and dendritic structure of directionally selective retinal ganglion cells. Journal of Neuroscience 14, 5267–5280.Google Scholar
Yazulla, S. & Schmidt, J. (1976). Radioautographic localization of 125I-α-bungarotoxin binding sites in the retina of goldfish and turtle. Vision Research 16, 878–880.Google Scholar
Yazulla, S. & Schmidt, J. (1977). Two types of receptors for α-bungarotoxin in the synaptic layers of the pigeon retina. Brain Research 138, 45–47.Google Scholar
Yum, L., Wolf, K.M., & Chiappinelli, V.A. (1996). Nicotinic acetylcholine receptors in separate brain regions exhibit different affinities for methyllycaconitine. Neuroscience 72, 545–555.Google Scholar
Zhang, Z.W., Coggan, J.S., & Berg, D.K. (1996). Synaptic currents generated by neuronal acetylcholine receptors sensitive to alpha-bungarotoxin. Neuron 17, 1231–1240.Google Scholar
Zucker, C. & Yazulla, S. (1982). Localization of synaptic and nonsynaptic nicotinic acetylcholine receptors in the goldfish retina. Journal of Comparative Neurology 204, 188–195.Google Scholar