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Nicotinic acetylcholine receptor expression by directionally selective ganglion cells

Published online by Cambridge University Press:  09 August 2007

CHRISTIANNE E. STRANG ,
JORDAN M. RENNA ,
FRANKLIN R. AMTHOR  and
KENT T. KEYSER
CHRISTIANNE E. STRANG
Affiliation:
Department of Vision Sciences, University of Alabama at Birmingham, Birmingham, Alabama
JORDAN M. RENNA
Affiliation:
Department of Vision Sciences, University of Alabama at Birmingham, Birmingham, Alabama
FRANKLIN R. AMTHOR
Affiliation:
Department of Psychology, University of Alabama at Birmingham, Birmingham, Alabama
KENT T. KEYSER
Affiliation:
Department of Vision Sciences, University of Alabama at Birmingham, Birmingham, Alabama
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Abstract

Acetylcholine (ACh) enhances the preferred direction responses of directionally selective ganglion cells (DS GCs; Ariel & Daw, 1982; Ariel & Adolph, 1985) through the activation of nicotinic acetylcholine receptors (nAChRs; Ariel & Daw, 1982; Massey et al., 1997; Kittila & Massey, 1997). DS GCs appear to express at least two types of nAChRs, those that are sensitive to the partially subtype-specific antagonist methyllycaconitine (MLA), and those that are MLA-insensitive (Reed et al., 2002). Our purpose was to confirm the expression of α7 nAChRs by DS GCs and to assess the contributions of other nAChR subtypes to DS GC responses. Using choline as a nAChR partially subtype-specific agonist, we found that the majority of DS GCs demonstrated responses to choline while under synaptic blockade. The blockade or reduction of choline-induced responses by bath application of nanomolar (nM) concentrations of MLA provided direct evidence that the choline responses were mediated by α7 nAChRs. Because choline is a partial agonist for α3β4 nAChRs (Alkondon et al., 1997), the residual choline responses are consistent with mediation by α3β4 nAChRs. Additionally, a subset of DS GCs responded to nicotine but not to choline, indicating the expression of a third nAChR subtype. The pharmacological results were supported by single cell reverse transcription polymerase chain reaction (RT-PCR) and immunohistochemistry experiments. The expression of α7 and specific non-α7 nAChR subtypes was correlated with the preferred direction. This indicates the possibility of differential responses to ACh depending on the direction of movement. This is the first description of differential expression of multiple nAChR subtypes by DS GCs.

Keywords

Directional selectivityAch receptorRetina
Type
Research Article
Information
Visual Neuroscience , Volume 24 , Issue 4 , July 2007 , pp. 523 - 533
Copyright
© 2007 Cambridge University Press

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References

REFERENCES

Ackert, J.M., Wu, S.H., Lee, J.C., Abrams, J., Hu, E.H., Perlman, I. & Bloomfield, S.A. (2006). Light-induced changes in spike synchronization between coupled ON direction selective ganglion cells in the mammalian retina. Journal of Neuroscience 26, 4206–4215.Google Scholar
Alkondon, M. & Albuquerque, E.X. (1993). Diversity of nicotinic acetylcholine receptors in rat hippocampal neurons. I. Pharmacological and functional evidence for distinct structural subtypes. Journal of Pharmacology & Experimental Therapeutics 265, 1455–1473.Google Scholar
Alkondon, M., Pereira, E.F., Cortes, W.S., Maelicke, A. & Albuquerque, E.X. (1997). Choline is a selective agonist of alpha7 nicotinic acetylcholine receptors in the rat brain neurons. European Journal of Neuroscience 9, 2734–2742.Google Scholar
Alkondon, M., Pereira, E.F., Eisenberg, H.M. & Albuquerque, E.X. (1999). Choline and selective antagonists identify two subtypes of nicotinic acetylcholine receptors that modulate GABA release from CA1 interneurons in rat hippocampal slices. Journal of Neuroscience 19, 2693–2705.Google Scholar
Alkondon, M., Pereira, E.F., 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., Reinhardt, S., Lobron, C., Hermsen, B., Maelicke, A. & Albuquerque, E.X. (1994). Diversity of nicotinic acetylcholine receptors in rat hippocampal neurons. II. The rundown and inward rectification of agonist-elicited whole-cell currents and identification of receptor subunits by in situ hybridization. Journal of Pharmacology & Experimental Therapeutics 271, 494–506.Google Scholar
Amthor, F.R., Grzywacz, N.M., Keyser, K.T. & Dacheux, R.F. (1997). Contribution of cholinergic amacrine cells to directional selectivity in rabbit retinal ganglion cells. Investigative Ophthalmology. Visual Science 39, S949.Google Scholar
Amthor, F.R., Keyser, K.T. & Dmitrieva, N.A. (2002). Effects of the destruction of starburst-cholinergic amacrine cells by the toxin AF64A on rabbit retinal directional selectivity. Visual Neuroscience 19, 495–509.Google Scholar
Amthor, F.R., Takahashi, E.S. & Oyster, C.W. (1989). Morphologies of rabbit retinal ganglion cells with concentric receptive fields. Journal of Comparative Neurology 280, 72–96.Google Scholar
Araki, C.M. & Hamassaki-Britto, D.E. (2000). Calretinin co-localizes with the NMDA receptor subunit NR1 in cholinergic amacrine cells of the rat retina. Brain Research 869, 220–224.Google Scholar
Ariel, M. & Adolph, A.R. (1985). Neurotransmitter inputs to directionally sensitive turtle retinal ganglion cells. Journal of Neurophysiology 54, 1123–1143.Google Scholar
Ariel, M. & Daw, N.W. (1982). Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells. Journal of Physiology 324, 161–185.Google Scholar
Brecha, N., Johnson, D., Peichl, L. & Wassle, H. (1988). Cholinergic amacrine cells of the rabbit retina contain glutamate decarboxylase and gamma-aminobutyrate immunoreactivity. Proceedings of the National Academy of Sciences of the United States of America 85, 6187–6191.Google Scholar
Clementi, F., Fornasari, D. & Gotti, C. (2000). Neuronal nicotinic receptors, important new players in brain function. European Journal of Pharmacology 393, 3–10.Google Scholar
Costa, L.G. & Murphy, S.D. (1984). Interaction of choline with nicotinic and muscarinic cholinergic receptors in the rat brain in vitro. Clinical & Experimental Pharmacology & Physiology 11, 649–654.Google Scholar
Dmitrieva, N.A., Pow, D.V., Lindstrom, J.M. & Keyser, K.T. (2003). Identification of cholinoceptive glycinergic neurons in the mammalian retina. Journal of Comparative Neurology 456, 167–175.Google Scholar
Famiglietti, E.V. & Tumosa, N. (1987). Immunocytochemical staining of cholinergic amacrine cells in rabbit retina. Brain Research 413, 398–403.Google Scholar
Fried, S.I., Munch, T.A. & Werblin, F.S. (2005). Directional selectivity is formed at multiple levels by laterally offset inhibition in the rabbit retina. Neuron 46, 117–127.Google Scholar
Genzen, J.R., Van Cleve, W. & McGehee, D.S. (2001). Dorsal root ganglion neurons express multiple nicotinic acetylcholine receptor subtypes. Journal of Neurophysiology 86, 1773–1782.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
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
Hayden, S.A., Mills, J.W. & Masland, R.M. (1980). Acetylcholine synthesis by displaced amacrine cells. Science 210, 435–437.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
Howell, D.C. (2002). Statistical Methods for Psychology. Pacific Grove, CA: Duxbury Press.
Hutchins, J.B. & Hollyfield, J.G. (1987). Cholinergic neurons in the human retina. Experimental Eye Research 44, 363–375.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., d'Exaerde, A.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
Lena, C., de Kerchove, D.E., Cordero-Erausquin, M., Le Novere, N., del Mar, A. & Changeux, J.P. (1999). Diversity and distribution of nicotinic acetylcholine receptors in the locus ceruleus neurons. Proceedings of the National Academy of Sciences of the United States of America 96, 12126–12131.Google Scholar
Lindstrom, J.M. (1996). Neuronal nicotinic acetylcholine receptors. In Ion Channels, Vol. 4, ed. Narahashi, T., pp. 377–449. New York: Plenum Press.
Lindstrom, J.M. (2000). The structures of neuronal nicotinic receptors. In Handbook of Experimental Pharmacology Vol. 144, eds. Clementi, F., Fornasari, D. & Gotti, C., pp. 101–162. Berlin: Springer-Verlag.
Lockman, P.R. & Allen, D.D. (2002). The transport of choline. Drug Development & Industrial Pharmacy 28, 749–771.Google Scholar
Masland, R.H. & Ames, A. (1976). Responses to acetylcholine of ganglion cells in an isolated mammalian retina. Journal of Neurophysiology 39, 1220–1235.Google Scholar
Masland, R.H. & Cassidy, C. (1987). The resting release of acetylcholine by a retinal neuron. Proceedings of the Royal Society of London—Series B: Biological Sciences 232, 227–238.Google Scholar
Masland, R.H. & Livingstone, C.J. (1976). Effect of stimulation with light on synthesis and release of acetylcholine by an isolated mammalian retina. Journal of Neurophysiology 39, 1210–1219.Google Scholar
Masland, R.H., Mills, J.W. & Hayden, S.A. (1984). Acetylcholine-synthesizing amacrine cells: identification and selective staining by using radioautography and fluorescent markers. Proceedings of the Royal Society of London—Series B: Biological Sciences 223, 79–100.Google Scholar
Massey, S.C., Linn, D.M., Kittila, C.A. & Mirza, W. (1997). Contributions of GABAA receptors and GABAC receptors to acetylcholine release and directional selectivity in the rabbit retina. Visual Neuroscience 14, 939–948.Google Scholar
McReynolds, J.S. & Miyachi, E. (1986). The effect of cholinergic agonists and antagonists on ganglion cells in the mudpuppy retina. Neuroscience Research—Supplement 4, S153–S161.Google Scholar
Oesch, N., Euler, T. & Taylor, W.R. (2005). Direction-selective dendritic action potentials in rabbit retina. Neuron 47, 739–750.Google Scholar
O'Malley, D.M. & Masland, R.H. (1989). Co-release of acetylcholine and gamma-aminobutyric acid by a retinal neuron. Proceedings of the National Academy of Sciences of the United States of America 86, 3414–3418.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
Papke, R.L. & Porter, P.J. (2002). Comparative pharmacology of rat and human alpha7 nAChR conducted with net charge analysis. British Journal of Pharmacology 137, 49–61.Google Scholar
Parker, J.C., Sarkar, D., Quick, M.W. & Lester, R.A. (2003). Interactions of atropine with heterologously expressed and native alpha 3 subunit-containing nicotinic acetylcholine receptors. British Journal of Pharmacology 138, 801–810.Google Scholar
Reed, B.T., Amthor, F.R. & Keyser, K.T. (2002). Rabbit retinal ganglion cell responses mediated by alpha-bungarotoxin-sensitive nicotinic acetylcholine receptors. Visual Neuroscience 19, 427–438.Google Scholar
Reed, B.T., Keyser, K.T. & Amthor, F.R. (2004). MLA-sensitive cholinergic receptors involved in the detection of complex moving stimuli in retina. Visual Neuroscience 21, 861–872.Google Scholar
Simpson, J.I., Leonard, C.S. & Soodak, R.E. (1988). The accessory optic system of rabbit. II. Spatial organization of direction selectivity. Journal of Neurophysiology 60, 2055–2072.Google Scholar
Smith, R.D., Grzywacz, N.M. & Borg-Graham, L.J. (1996). Is the input to a GABAergic synapse the sole asymmetry in turtle's retinal directional selectivity? Visual Neuroscience 13, 423–439.Google Scholar
Strang, C.E., Amthor, F.R. & Keyser, K.T. (2003). Rabbit retinal ganglion cell responses to nicotine can be mediated by β2-containing nicotinic acetylcholine receptors. Visual Neuroscience 20, 651–662.Google Scholar
Strang, C.E., Andison, M.E., Amthor, F.R. & Keyser, K.T. (2005). Rabbit retinal ganglion cells express functional {alpha}7 nAChRs. American Journal of Physiology-Cell Physiology 289, C644–C655.Google Scholar
Straschill, M. & Perwein, J. (1973). The effect of iontophoretically applied acetylcholine upon the cat's retinal ganglion cells. Pflugers Archiv—European Journal of Physiology 339, 289–298.Google Scholar
Sun, W., Deng, Q., Levick, W.R. & He, S. (2006). ON direction-selective ganglion cells in the mouse retina. Journal of Physiology 576, 197–202.Google Scholar
Uteshev, V.V., Meyer, E.M. & Papke, R.L. (2002). Activation and inhibition of native neuronal alpha-bungarotoxin-sensitive nicotinic ACh receptors. Brain Research 948, 33–46.Google Scholar
Vaney, D.I. (1994). Territorial organization of direction-selective ganglion cells in rabbit retina. Journal of Neuroscience 14, 6301–6316.Google Scholar
Wang, F., Gerzanich, V., Wells, G., Anand, R., Peng, X., Keyser, K.T. & Lindstrom, J. (1996). Assembly of human neuronal nicotinic receptor α5 subunits with α3, β2 and β4 subunits. Journal of Biological Chemistry 271, 17656–17665.Google Scholar
Yoshida, K., Watanabe, D., Ishikane, H., Tachibana, M., Pastan, I. & Nakanishi, S. (2001). A key role of starburst amacrine cells in originating retinal directional selectivity and optokinetic eye movement. Neuron 30, 771–780.Google Scholar
Zhang, J., Li, W., Hoshi, H., Mills, S.L. & Massey, S.C. (2005). Stratification of alpha ganglion cells and ON/OFF directionally selective ganglion cells in the rabbit retina. Visual Neuroscience 22, 535–549.Google Scholar