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Is the input to a GABAergic or cholinergic synapse the sole asymmetry in rabbit's retinal directional selectivity?

Published online by Cambridge University Press:  02 June 2009

Norberto M. Grzywacz ,
John S. Tootle  and
Franklin R. Amthor
Norberto M. Grzywacz
Affiliation:
Smith-Kettlewell Eye Research Institute, 2232 Webster Street, San Francisco
John S. Tootle
Affiliation:
Department of Physiological Optics and Vision Science Research Center, University of Alabama at Birmingham, Birmingham
Franklin R. Amthor
Affiliation:
Department of Psychology and Neurobiology Research Center, University of Alabama at Birmingham, Birmingham
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Abstract

We examined contrast, direction of motion, and concentration dependencies of the effects of GABAergic and cholinergic antagonists, and anticholinesterases on responses to movement of On—Off directionally selective (DS) ganglion cells of the rabbit's retina. The drugs tested were curare and hexamethonium bromide (cholinergic antagonists), physostigmine (anticholinesterase), and picrotoxin (GABAergic antagonist). They all reduced the cells' directional selectivity, while maintaining their preferred-null axis. However, cholinergic antagonists did not block directional selectivity completely even at saturating concentrations. The failure to eliminate directional selectivity was probably not due to an incomplete blockade of cholinergic receptors. In a extension of a Masland and Ames (1976) experiment, saturating concentrations of antagonists blocked the effects of exogenous acetylcholine or nicotine applied during synaptic blockade. Consequently, a noncholinergic pathway may be sufficient to account for at least some directional selectivity. This putative pathway interacts with the cholinergic pathway before spike generation, since physostigmine eliminated directional selectivity at contrasts lower than those saturating responses. This elimination apparently resulted from cholinergic-induced saturation, since reduction of contrast restored directional selectivity. Under picrotoxin, directional selectivity was lost in 33% of the cells regardless of contrast. However, 47% maintained their preferred direction despite saturating concentrations of picrotoxin, and 20% reversed the preferred and null directions. Therefore, models based solely on a GABAergic implementation of Barlow and Levick's asymmetric-inhibition model or solely on a cholinergic implementation of asymmetric-excitation models are not complete models of directional selectivity in the rabbit. We propose an alternate model for this retinal property.

Keywords

Directional selectivityRetinal ganglion cellsGABAAcetylcholineCholinesterase
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 1 , January 1997 , pp. 39 - 54
Copyright
Copyright © Cambridge University Press 1997

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References

Ames, A.A. III, & Nesbett, F.B. (1981). In vitro retina as an experimental model of the central nervous system. Journal of Neurochemisiry 37, 867–877.CrossRefGoogle ScholarPubMed
Amthor, F.R. & Grzywacz, N.M. (1991). The nonlinearity of the inhibition underlying retinal directional selectivity. Visual Neuroscience 6, 197–206.CrossRefGoogle ScholarPubMed
Amthor, F.R. & Grzywacz, N.M. (1993 a). Inhibition in directionally selective ganglion cells of the rabbit retina. Journal of Neurophysiology 69, 2174–2187.CrossRefGoogle ScholarPubMed
Amthor, F.R. & Grzywacz, N.M. (1993 b). Directional selectivity in vertebrate retinal ganglion cells. In Visual Motion and Its Role in the Stabilization of Gaze, Reviews of Oculomotor Research, Vol. 5, ed. Miles, F. & Wallman, J., pp. 79–100. Amsterdam, The Netherlands: Elsevier.Google Scholar
Amthor, F.R. & Grzywacz, N.M. (1995). Morphological and physiological basis of starburst-ACh amacrine input to directionally selective (DS) ganglion cells in rabbit retina. Neuroscience Abstracts 21, 508.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.CrossRefGoogle ScholarPubMed
Amthor, F.R. & Oyster, C.W. (1995). Spatial organization of retinal information about the direction of image motion. Proceedings of the National Academy of Sciences of the U.S.A. 92, 4002–4005.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Amthor, F.R., Takahashi, E.S. & Oyster, C.W. (1989 a). Morphologies of rabbit retinal ganglion cells with complex receptive fields. Journal of Comparative Neurology 280, 97–121.Google Scholar
Amthor, F.R., Takahashi, E.S. & Oyster, C.W. (1989 b). Morphologies of rabbit retinal ganglion cells with concentric receptive fields. Journal of Comparative Neurology 280, 72–96.CrossRefGoogle ScholarPubMed
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
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.CrossRefGoogle ScholarPubMed
Barlow, H.B. & Levick, W.R. (1965). The mechanism of directionally selective units in the rabbit's retina. Journal of Physiology 178, 477–504.CrossRefGoogle ScholarPubMed
Borg-Graham, L.J. & Grzywacz, N.M. (1991). A model of the direction selectivity circuit in retina: Transformations by neurons singly and in concert. In Single Neuron Computation, ed. McKenna, T., Davis, J. & Zornetzer, S.F., pp. 347–375. Orlando, Florida: Academic Press.Google Scholar
Brandon, C. (1987). Cholinergic neurons in the rabbit retina: Dendritic branching and ultrastructural connectivity. Brain Research 426, 119–130.Google Scholar
Brandstatter, J.H., Greferath, U., Euler, T. & Wassle, H. (1995). Co-stratification of GABAA receptors with the directionally selective circuitry of the rat retina. Visual Neuroscience 12, 345–358.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 U.S.A. 85, 6187–6191.Google Scholar
Bülthoff, H.H. & Bülthoff, I. (1987). GABA-antagonist inverts movement and object detection in flies. Brain Research 407, 152–158.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Criswell, M.H. & Brandon, C. (1992). Cholinergic and GABAergic neurons occur in both the distal and proximal turtle retina. Brain Research 577, 101–111.CrossRefGoogle ScholarPubMed
Dowling, J.E. (1987). The Retina: An Approachable Part of the Brain. Cambridge, Massachusetts: Harvard University Press.Google Scholar
Egelhaaf, M., Borst, A. & Pilz, B. (1990). The role of GABA in detecting visual motion. Brain Research 509, 156–160.Google Scholar
Famiglietti, E.V. Jr. (1983 a). “Starburst” amacrine cells and cholinergic neurons: Mirror-symmetric On and Off amacrine cells of rabbit retina. Brain Research 261, 138–144.Google Scholar
Famiglietti, E.V. Jr. (1983 b) 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. Jr., (1991). Synaptic organization of starburst amacrine cells in rabbit retina: Analysis of serial thin sections by electron microscopy and graphic reconstruction. Journal of Comparative Neurology 309, 40–70.Google Scholar
Grzywacz, N.M. & Amthor, F.R. (1993). Facilitation in directionally selective ganglion cells of the rabbit retina. Journal of Neurophysiology 69, 2188–2199.Google Scholar
Grzywacz, N.M., Amthor, F.R. & Dacheux, R.F. (1995). Are cholinergic synapses to directionally selective ganglion cells spatially asymmetric? Investigative Ophthalmology and Visual Science 36, 865.Google Scholar
Grzywacz, N.M., Amthor, F.R. & Merwine, D.K. (1994). Directional hyperacuity in ganglion cells of the rabbit retina. Visual Neuroscience 11, 1019–1025.CrossRefGoogle ScholarPubMed
Grzywacz, N.M. & Koch, C. (1987). Functional properties of models for direction selectivity in the retina. Synapse 1, 417–434.Google Scholar
Guiloff, G.D. & Kolb, H. (1992 a). Neurons immunoreactive to choline acetyltransferase in the turtle retina. Vision Research 32, 2023–2030.CrossRefGoogle ScholarPubMed
Guiloff, G.D. & Kolb, H. (1992 b). Ultrastructural and immunocytochemical analysis of the circuitry of two putative directionally selective ganglion cells in turtle retina. Journal of Comparative Neurology 347, 321–339.CrossRefGoogle Scholar
Johnson, R.A. & Wichern, D.W. (1992). Applied Multivariate Statistical Analysis, 3rd edition. Englewood Cliffs, New Jersey: Prentice Hall.Google Scholar
Kittila, C.A. & Massey, S.C. (1995). Effect of ON pathway blockade on directional selectivity in the rabbit retina. Journal of Neurophysiology 73, 703–712.CrossRefGoogle Scholar
Kittila, C.A. & Massey, S.C. (1997). The pharmacology of directionally selective ganglion cells in the rabbit retina. Journal of Neurophysiology (in press).CrossRefGoogle ScholarPubMed
Koch, C., Poggio, T. & Torre, V. (1982). Retinal ganglion cells: A functional interpretation of dendritic morphology. Philosophical Transactions of the Royal Society B (London) 298, 227–264.Google Scholar
Kosaka, T., Tauchi, M. & Dahl, J.L. (1988). Cholinergic neurons containing GABA-like and/or glutamic acid decarboxylase-like immunoreactivities in various brain regions of the rat. Experimental Brain Research 70, 605–617.Google Scholar
Linn, D.M. & Massey, S.C. (1992). GABA inhibits ACh release from the rabbit retina: A direct effect or feedback to bipolar cells? Visual Neuroscience 8, 97–106.Google Scholar
Masland, R.H. & Ames, A.A. III, (1976). Responses to acetylcholine of ganglion cells in an isolated mammalian retina. Journal of Neurophysiology 39, 1220–1235.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.CrossRefGoogle ScholarPubMed
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, 1663–1643.CrossRefGoogle ScholarPubMed
Merwine, D.K., Amthor, F.R. & Grzywacz, N.M. (1995). The interaction between center and surround in rabbit retinal ganglion cells. Journal of Neurophysiology 73, 1547–1567.CrossRefGoogle ScholarPubMed
Millar, T.J. & Morgan, I.G. (1987). Cholinergic amacrine cells in the rabbit retina synapse onto other cholinergic amacrine cells. Neuroscience Letters 74, 281–285.Google Scholar
Mosinger, J. & Yazulla, S. (1987). Double-label analysis of GAD- and GABA-like immunoreactivity in the rabbit retina. Vision Research 27, 23–30.CrossRefGoogle ScholarPubMed
Nicoll, R.A. (1978). Pentobarbital: Differential postsynaptic action on sympathetic ganglion cells. Science 199, 451–452.Google Scholar
Ögmen, H. (1991). On the mechanisms underlying directional selectivity. Neural Computation 3, 333–349.Google Scholar
O'Malley, D.M., Sandell, J.H. & Masland, R.H. (1992). Co-release of acetylcholine and GABA by the starburst amacrine cells. Journal of Neuroscience 12, 1394–1408.Google Scholar
Poznanski, R.R. (1992). Modelling the electrotonic structure of starburst amacrine cells in the rabbit retina: A functional interpretation of dendritic morphology. Bulletin of Mathematical Biology 54, 905–928.CrossRefGoogle ScholarPubMed
Sernagor, E. & Grzywacz, N.M. (1995). Emergence of complex receptive field properties of ganglion cells in the developing turtle retina. Journal of Neurophysiology 73, 1355–1364.Google Scholar
Smith, R.D., Grzywacz, N.M. & Borg-Graham, L. (1996). Is the input to a gabaergic synapse the sole asymmetry in turtle's retinal directional selectivity? Visual Neuroscience 13, 423–429.CrossRefGoogle ScholarPubMed
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, 101–119.Google ScholarPubMed
Torre, V. & Poggio, T. (1978). A synaptic mechanism possibly underlying directional selectivity to motion. Proceedings of the Royal Society B (London) 202, 409–416.Google Scholar
Vaney, D.I. (1990). The mosaic of amacrine cells in the mammalian retina. In Progress in Retinal Research, Vol. 9, ed. Osborne, N. & Chader, J., pp. 49–100. Oxford, England: Pergamon Press.Google Scholar
Vaney, D.I. & Young, H.M. (1988). GABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina. Brain Research 438, 369–373.Google Scholar
Werblin, F., Maguire, G., Lukasiewicz, P., Eliasof, S. & Wu, S.M. (1988). Neural interactions mediating the detection of motion in the retina of the tiger salamander. Visual Neuroscience 1, 317–329.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
Wyszecki, G. & Stiles, W.S. (1982). Color Science: Concepts and Methods, Quantitative Data and Formulae, 2nd edition. New York: John Wiley & Sons.Google Scholar
Yang, G. & Masland, R.H. (1992). Direct visualization of the dendritic and receptive fields of directionally selective retinal ganglion cells. Science 258, 1949–1952.CrossRefGoogle ScholarPubMed
Yang, G. & Masland, R.H. (1994). Receptive fields and dendritic structure of directionally selective retinal ganglion cells. Journal of Neuroscience 14, 5267–5280.CrossRefGoogle ScholarPubMed
Young, H.M. & Vaney, D.I. (1991). Rod-signal interneurons in the rabbit retina: 1. Rod bipolar cells. Journal of Comparative Physiology 310, 139–153.Google Scholar
Zhou, Z.J. & Fain, G.L. (1995). Neurotransmitter receptors of starburst amacrine cells in rabbit retinal slices. Journal of Neuroscience 15, 5334–5345.Google Scholar