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Directional hyperacuity in ganglion cells of the rabbit retina

Published online by Cambridge University Press:  02 June 2009

Norberto M. Grzywacz ,
Franklin R. Amthor  and
David K. Merwine
Norberto M. Grzywacz
Affiliation:
The Smith-Kettlewell Eye Research Institute, 2232 Webster Street, San Francisco
Franklin R. Amthor
Affiliation:
Department of Psychology and Neurobiology Research Center, University of Alabama at Birmingham, Birmingham
David K. Merwine
Affiliation:
Department of Physiological Optics, School of Optometry, University of Alabama at Birmingham, Birmingham
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Abstract

Biological visual systems can detect positional changes that are finer than these systems' acuity to sine-wave gratings, a property known as hyperacuity. Some systems can even detect changes finer that the photoreceptor spacing. We report here that rabbit's directionally selective ganglion cells not only detect positional changes in the hyperacuity range, but also discriminate the direction of their motion. Our experiments show that directional selectivity occurs for edges of light moving as little as 1.1 μm (26” of visual angle) across the retina. This distance corresponds to a hyperacuity, since the acuity to sine-wave gratings of rabbit's On-Off DS ganglion cells is about 125 μm (50′). In addition, this distance is smaller than the minimal spacing between rabbit photoreceptors (1.9 μm or 46”), as estimated from cell-density studies (Young & Vaney, 1991). Such a hyperacuity suggests low-noise high-gain signal transmission from photoreceptors to ganglion cells and that directional selectivity can arise in small portions of retinal dendritic processes.

Keywords

HyperacuityDirectional selectivityGanglion cellRetinaRabbit
Type
Short Communications
Information
Visual Neuroscience , Volume 11 , Issue 5 , September 1994 , pp. 1019 - 1025
Copyright
Copyright © Cambridge University Press 1994

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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 Neurochemistry 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). Inhibition in directionally selective ganglion cells of the rabbit retina. Journal of Neurophysiology 69, 2174–2187.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). Morphologies of rabbit retinal ganglion cells with complex receptive fields. Journal of Comparative Neurology 280, 97–121.CrossRefGoogle ScholarPubMed
Ariel, M. & Daw, N.W. (1982). Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells. Journal of Physiology 324, 161–185.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
Boro-Graham, L.J. & Grzywacz, N.M. (1992). 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.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Dacheux, R.F. & Raviola, E. (1986). The rod pathway in the rabbit retina: A depolarizing bipolar and amacrine cell. Journal of Neuroscience 6, 331–345.CrossRefGoogle ScholarPubMed
Elliot, P.B. (1964). Tables of d′. In Signal Detection and Recognition by Human Observers, ed. Swets, J.A., pp. 651–684. New York, New York: John Wiley.Google Scholar
Fain, G.L. (1977). The threshold signal of photoreceptors. In Vertebrate Photoreception, ed. Barlow, H.B. & Fatt, P., pp. 305–323. London, England: Academic Press.Google Scholar
Fain, G.L., Granda, A.M. & Maxwell, J.H. (1977). The voltage signal of photoreceptors at visual threshold. Nature 265, 181–183.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (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.CrossRefGoogle ScholarPubMed
Green, D.M. & Swets, J.A. (1966). Signal Detection Theory and Psychophysics. New York, New York: John Wiley.Google Scholar
Grzywacz, N.M. & Amthor, F.R. (1989). A model for neural directional selectivity that exhibits robust direction of motion computation. In Advances in Neural Information I. Processing Systems I., ed. Touretzky, D.S., pp. 477–484. San Mateo, California: Morgan Kaufman.Google Scholar
Grzywacz, N.M., Amthor, F.R. & Mistler, L.A. (1990). Applicability of quadratic and threshold models to motion discrimination in the rabbit retina. Biological Cybernetics 64, 41–49.CrossRefGoogle ScholarPubMed
Grzywacz, N.M. & Amthor, F.R. (1993). Facilitation in directionally selective ganglion cells of the rabbit retina. Journal of Neurophysiology 69, 2188–2199.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 ScholarPubMed
Lee, B.B., Wehrhahn, C., Westheimer, G. & Kremers, J. (1993). Macaque ganglion cell responses to stimuli that elicit hyperacuity in man: Detection of small displacements. Journal of Neuroscience 13, 1001–1009.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
O'Malley, D.M. & Masland, R.H. (1993). Responses of the starburst amacrine cells to moving stimuli. Journal of Neurophysiology 69, 730–738.CrossRefGoogle ScholarPubMed
Oyster, C.W. (1968). The analysis of image motion by the rabbit retina. Journal of Physiology 199, 613–635.CrossRefGoogle ScholarPubMed
Shapley, R. & Victor, J. (1986). Hyperacuity in cat retinal ganglion cells. Science 231, 999–1002.CrossRefGoogle ScholarPubMed
Smith, R.G. & Sterling, P. (1990). Cone receptive field in cat retina computed from microcircuitry. Visual Neuroscience 5, 453–461.CrossRefGoogle ScholarPubMed
Swindale, N.V. & Cynader, M.S. (1986). Vernier acuity of neurones in cat visual cortex. Nature 319, 591–593.CrossRefGoogle 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
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.CrossRefGoogle ScholarPubMed
Westheimer, G. & McKee, S.P. (1977). Spatial configuration for visual hyperacuity. Vision Research 17, 941–947.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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
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 ScholarPubMed