Hostname: page-component-7dd5485656-wlg5v Total loading time: 0 Render date: 2025-10-31T09:57:02.607Z Has data issue: false hasContentIssue false
  • English
  • Français

Rabbit retinal ganglion cell responses to nicotine can be mediated by β2-containing nicotinic acetylcholine receptors

Published online by Cambridge University Press:  30 March 2004

CHRISTIANNE E. STRANG ,
FRANKLIN R. AMTHOR  and
KENT T. KEYSER
CHRISTIANNE E. STRANG
Affiliation:
Department of Psychology, University of Alabama at Birmingham, Birmingham
FRANKLIN R. AMTHOR
Affiliation:
Department of Psychology, University of Alabama at Birmingham, Birmingham
KENT T. KEYSER
Affiliation:
Department of Physiological Optics, University of Alabama at Birmingham, Birmingham
Get access Rights & Permissions [Opens in a new window]

Abstract

Acetylcholine (ACh) affects the response properties of many retinal ganglion cells (GCs) through the activation of nicotinic acetylcholine receptors (nAChRs). To date there have been few studies directly correlating the expression of specific nAChR subtypes with the physiological and morphological characteristics of specific retinal GCs. This study was designed to correlate responses to nicotine application with immunohistochemical evidence of nAChR expression in physiologically and morphologically identified ganglion cells. Extracellular recordings were used to physiologically identify rabbit retinal GCs, based on responses to light stimulation. Cells were then tested for responses to nicotine application and/or for expression of nAChRs, as judged by immunoreactivity to mAb210, an nAChR antibody. The morphologies of many physiologically identified cells were also determined by dye injection. More than three-fourths of ganglion cells tested responded to nicotine application under cobalt-induced synaptic blockade. The nicotine sensitivity was consistent with nAChR immunoreactivity and was also correlated with specific morphological subgroups of GCs. Overall, approximately two-thirds of all physiologically identified GCs that were processed for immunohistochemistry displayed immunoreactivity. In total, 18 of 22 physiologically identified cells demonstrated both sensitivity to nicotine application under synaptic blockade and mAb210 immunoreactivity (mAb210-IR). Thus, mAb210-IR is likely to represent functional nAChRs that can modulate retinal information processing and visual functioning via direct excitation of a number of GC classes.

Keywords

Nicotinic acetylcholine receptorRetinaGanglion cellMorphology

Information

Type
Research Article
Information
Visual Neuroscience , Volume 20 , Issue 6 , November 2003 , pp. 651 - 662
Copyright
© 2003 Cambridge University Press

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.)

Article purchase

Temporarily unavailable

References

REFERENCES

Amthor, F.R. & Jackson, C.A. (1986). Staining of retinal neurons in the isolated eyecup by extracellular horseradish peroxidase injection. Vision Research 26, 269–274.Google Scholar
Amthor, F.R., Takahashi, E.S., & Oyster, C.W. (1989a). Morphologies of rabbit retinal ganglion cells with concentric receptive fields. Journal of Comparative Neurology 280, 72–96.Google Scholar
Amthor, F.R., Takahashi, E.S., & Oyster, C.W. (1989b). Morphologies of rabbit retinal ganglion cells with complex receptive fields. Journal of Comparative Neurology 280, 97–121.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
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
Brandon, C. (1987a). Cholinergic neurons in the rabbit retina: Dendritic branching and ultrastructural connectivity. Brain Research 426, 119–130.Google Scholar
Brandon, C. (1987b). Cholinergic neurons in the rabbit retina: Immunocytochemical localization, and relationship to GABAergic and cholinesterase-containing neurons. Brain Research 401, 385–391.Google Scholar
Britto, L.R., Rogers, S.W., Hamassaki-Britto, D.E., & Duvoisin, R.M. (1994). Nicotinic acetylcholine receptors in the ground squirrel retina: Localization of the β4 subunit by immunohistochemistry and in situ hybridization. Visual Neuroscience 11, 569–577.Google Scholar
Chavez-Noriega, L.E., Crona, J.H., Washburn, M.S., Urrutia, A., Elliot, K.J., & Johnson, E.C. (1997). Pharmacological characterization og recombinant human neuronal nicotinic receptors hα2β2, hα2β4, hα3β2, hα3β4, hα4β2, hα4β4 and hα7 expressed in Xenopus oocytes. Journal of Pharmacology and Experimental Therapies 280, 346–356.Google Scholar
Chavez-Noriega, L.E., Gillespie, A., Stauderman, K.A., Crona, J.H., Claeps, B.O., Elliott, K.J., Reid, R.T., Rao, T.S., Velicelebi, G., Harpold, M.M., Johnson, E.C., & Corey-Naeve, J. (2000). Characterization of the recombinant human neuronal nicotinic acetylcholine receptors alpha3beta2 and alpha4beta2 stably expressed in HEK293 cells. Neuropharmacology 39, 2543–2560.Google Scholar
Clementi, F., Fornasari, D., & Gotti, C. (2000a). Neuronal nicotinic acetylcholine receptors: From structure to therapeutics. Trends in Pharmacological Sciences 21, 35–37.Google Scholar
Clementi, F., Fornasari, D., & Gotti, C. (2000b). Neuronal nicotinic receptors, important new players in brain function. European Journal of Pharmacology 393, 3–10.Google Scholar
Criswell, M.H. & Brandon, C. (1993). Acetylcholinesterase and choline acetyltransferase localization patterns do correspond in cat and rat retinas. Vision Research 33, 1747–1753.Google Scholar
Dmitrieva, N.A., Lindstrom, J.M., & Keyser, K.T. (2001). The relationship between GABA-containing cells and the cholinergic circuitry in the rabbit retina. Visual Neuroscience 18, 93–100.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. (1983). On and off pathways through amacrine cells in mammalian retina: The synaptic connections of “starburst” amacrine cells. Vision Research 23, 1265–1279.Google Scholar
Famiglietti, E.V. & Tumosa, N. (1987). Immunocytochemical staining of cholinergic amacrine cells in rabbit retina. Brain Research 413, 398–403.Google Scholar
Grunert, U. (2000). Distribution of GABA and glycine receptors on bipolar and ganglion cells in the mammalian retina. Microscopy Research and Technique 50, 130–140.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
Hutchins, J.B. & Hollyfield, J.G. (1986). Human retinas synthesize and release acetylcholine. Journal of Neurochemistry 47, 81–87.Google Scholar
Hutchins, J.B. & Hollyfield, J.G. (1987). Acetylcholinesterase in the human retina. Brain Research 400, 300–311.Google Scholar
Ikeda, H. & Sheardown, M.J. (1982). Acetylcholine may be an excitatory transmitter mediating visual excitation of ‘transient’ cells with the periphery effect in the cat retina: Iontophoretic studies in vivo. Neuroscience 7, 1299–1308.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
Kuryatov, A., Olale, F.A., Choi, C., & Lindstrom, J.M. (2000). Acetylcholine receptor extracellular domain determines sensitivity to nicotine-induced inactivation. European Journal of Pharmacology 393, 11–21.Google Scholar
Lindstrom, J.M. (1996). Neuronal nicotinic acetylcholine receptors. In Ion Channels, Volume 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, ed. Clementi, F., Fornasari, D. & Gotti, C., pp. 101–162. Berlin Heidelburg: Springer-Verlag.
Lipton, S.A. (1988). Spontaneous release of acetylcholine affects the physiological nicotinic responses of rat retinal ganglion cells in culture. Journal of Neuroscience 8, 3857–3868.Google Scholar
Marc, R.E. & Jones, B.W. (2002). Molecular phenotyping of retinal ganglion cells. Journal of Neuroscience 22, 413–427.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. & 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. (1979). Autoradiographic identification of acetylcholine in the rabbit retina. Journal of Cell Biology 83, 159–178.Google Scholar
Masland, R.H. & Cassidy, C. (1987). The resting release of acetylcholine by a retinal neuron. Proceedings of the Royal Society B (London) 232, 227–238.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
McGillem, G.S., Rotolo, T.C., & Dacheux, R.F. (2000). GABA responses of rod bipolar cells in rabbit retinal slices. Visual Neuroscience 17, 381–389.Google Scholar
Mitchell, C.K. & Redburn, D.A. (1991). Melatonin inhibits ACh release from rabbit retina. Visual Neuroscience 7, 479–486.Google Scholar
Muller, J.F. & Dacheux, R.F. (1997). Alpha ganglion cells of the rabbit retina lose antagonistic surround responses under dark adaptation. Visual Neuroscience 14, 395–401.Google Scholar
Peichl, L., Buhl, E.H., & Boycott, B.B. (1987). Alpha ganglion cells in the rabbit retina. Journal of Comparative Neurology 263, 25–41.Google Scholar
Pourcho, R.G. (1979). Localization of cholinergic synapses in mammalian retina with peroxidase-conjugated alpha-bungarotoxin. Vision Research 19, 287–292.Google Scholar
Reed, B.T., Amthor, F.R., & Keyser, K.T. (2002). Rabbit retinal ganglion cell responses mediated by α-bungarotoxin-sensitive acetylcholine receptors. Visual Neuroscience 19, 427–438.Google Scholar
Rockhill, R.L., Daly, F.J., MacNeil, M.A., Brown, S.P., & Masland, R.H. (2002). The diversity of ganglion cells in a mammalian retina. Journal of Neuroscience 22, 3831–3843.Google Scholar
Rodieck, R.W. & Marshak, D.W. (1992). Spatial density and distribution of choline acetyltransferase immunoreactive cells in human, macaque, and baboon retinas. Journal of Comparative Neurology 321, 46–64.Google Scholar
Sandmann, D., Engelmann, R., & Peichl, L. (1997). Starburst cholinergic amacrine cells in the tree shrew retina. Journal of Comparative Neurology 389, 161–176.Google Scholar
Sargent, P.B. (1993). The diversity of neuronal nicotinic acetylcholine receptors. Annual Review of Neuroscience 16, 403–443.Google Scholar
Schmidt, M., Humphrey, M.F., & Wassle, H. (1987). Action and localization of acetylcholine in the cat retina. Journal of Neurophysiology 58, 997–1015.Google Scholar
Strang, C.E., Amthor, F.R., & Keyser, K.T. (2002a). Expression and function of nicotinic acetylcholine receptors in the rabbit retina. Annual Meeting Abstract and Program Planner accessed at www. arvo.org. Association for Research in Vision and Ophthalmology (Abstract 4766).Google Scholar
Strang, C.E., Renna, J.M., Reed., B.T., Amthor, F.R., & Keyser, K.T. (2002b). Nicotinic receptor subtypes in rabbit retina. Society for Neuroscience 28 (Abstract 37.1).Google Scholar
Vardi, N., Masarachia, P.J., & Sterling, P. (1989). Structure of the starburst amacrine network in the cat retina and its association with alpha ganglion cells. Journal of Comparative Neurology 288, 601–611.Google Scholar
Voigt, T. (1986). Cholinergic amacrine cells in the rat retina. Journal of Comparative Neurology 248, 19–35.Google Scholar
Whiting, P., Schoepfer, R., Conroy, W.G., & Gore, M.J.K.K.T. (1991). Expression of nicotinic acetylcholine receptor subtypes in brain and retina. Molecular Brain Research 10, 61–70.Google Scholar
Wilkinson, C.S., Amthor, F.R., Andison, M.E., & Keyser, K.T. (2001). α3β2 nAChRs are expressed by several physiologically distinct classes of ganglion cells in the rabbit retina. Society for Neuroscience Abstracts 27, (Abstract 397, 14).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 461, 76–90.Google Scholar