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

Published online by Cambridge University Press:  02 June 2009

Randall D. Smith ,
Norberto M. Grzywacz  and
Lyle J. Borg-Graham
Randall D. Smith
Affiliation:
Center for Biological Information Processing, Massachusetts Institute of Technology, Cambridge
Norberto M. Grzywacz
Affiliation:
Smith-Kettlewell Eye Research Institute, San Francisco
Lyle J. Borg-Graham
Affiliation:
Center for Biological Information Processing, Massachusetts Institute of Technology, Cambridge
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Abstract

We examined the effects of picrotoxin and pentylenetetrazol (PTZ) on the responses to motions of ON-OFF directionally selective (DS) ganglion cells of the turtle's retina. These drugs are antagonists of the inhibitory neurotransmitter GABA. For continuous motions, picrotoxin markedly reduced the overall directionality of the cells. In 21% of the cells, directional selectivity was lost regardless of speed and contrast. However, other cells maintained their preferred direction despite saturating concentrations of picrotoxin. And in most cells, loss, maintenance, or even reversal of preferred and null directions could occur as speed and contrast were modulated. In 50% of the cells, reversal of preferred and null directions occurred at some condition of visual stimuli. However, picrotoxin did not tend to alter the preferred-null axis for directional selectivity. For apparent motions, picrotoxin made motion facilitation, which normally occurs exclusively in preferred-direction responses, to become erratic and often occur during null-direction motions. Finally, PTZ had effects similar to picrotoxin but with less potency. The results in this paper indicated that models of directional selectivity based solely on a GABAergic implementation of Barlow and Levick's asymmetric-inhibition model do not apply to the turtle retina. Alternative models may comprise multiple directional mechanisms and/or a symmetric inhibitory one, but not asymmetric facilitation.

Keywords

Directional selectivityRetinal ganglion cellsGABAPreferred-direction facilitationNull-direction inhibition
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 3 , May 1996 , pp. 423 - 439
Copyright
Copyright © Cambridge University Press 1996

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References

Adolph, A.R. (1988). Center-surround, orientation, and directional properties of turtle retinal horizontal cells. Biological Cybernetics 58, 373–385.CrossRefGoogle ScholarPubMed
Allan, A.M. & Harris, R.A. (1986). γ-Aminobutyric acid agonists and antagonists alter chloride flux across brain membranes. Molecular Pharmacology 29, 497–505.Google 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., 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. & Adolph, A.R. (1985). Neurotransmitter inputs to directionally sensitive turtle retinal ganglion cells. Journal of Neurophysiology 54, 1123–1143.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
Borg-Graham, L.J. & Grzywacz, N.M. (1990). An isolated turtle retina preparation allowing direct approach to ganglion cells and photo-receptors, and transmitted light-microscopy. Investigative Ophthalmology and Visual Science 31, 211.Google Scholar
Borg-Graham, L.J. & Grzywacz, N.M. (1991). Whole-cell patch recordings and analysis of the input onto turtle directionally selective (DS) ganglion cells. Investigative Ophthalmology and Visual Science 32, 2067.Google Scholar
Borg-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
Bowling, D.B. (1980). Light responses of ganglion cells in the retina of the turtle. Journal of Physiology 209, 173–196.CrossRefGoogle Scholar
Brandon, C. (1987). Cholinergic neurons in the rabbit retina: Dendritic branching and ultrastructural connectivity. Brain Research 426, 119–130.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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
Criswell, M.H. & Brandon, C. (1992). Cholinergic and GABAergic neurons occur in both the distal and proximal turtle retinal. Brain Research 577, 101–111.CrossRefGoogle Scholar
De Voe, R.D., Carras, P.L., Criswell, M.H. & Guy, R.B. (1989). Not by ganglion cells alone: Directional selectivity is widespread in identified cells of the turtle retina. In Neurobiology of the Inner Retina, ed. Weller, R. & Osborne, N. M., pp. 235–246, NATO A.S.I. Series, Vol. H31. Berlin, Germany: Springer Verlag.CrossRefGoogle Scholar
Dowling, J.E. (1987). The Retina: An Approachable Part of the Brain. Cambridge, Massachusetts: Harvard University Press.Google Scholar
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
Feigenspan, A., Wassle, H. & Bormann, J. (1993). Pharmacology of GABA receptor Cl- channels in rat retinal bipolar cells. Nature 361, 159–162.CrossRefGoogle ScholarPubMed
Feldman, R.S. & Quenzer, L.F. (1984). Fundamentals of Neuropsy-chopharmacology. Sunderland, Massachusetts: Sinauer Associates.Google Scholar
Friedman, D.L. & Redburn, D.A. (1990). Evidence for functionally distinct subclasses of gamma-aminobutyric acid receptors in rabbit retina. Journal of Neurochemisiry 55, 1189–1199.CrossRefGoogle ScholarPubMed
Granda, A.M. & Fulbrook, J.E. (1989). Classification of turtle retinal ganglion cells. Journal of Neurophysiology 62, 723–737.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
Grzywacz, N.M., Amthor, F.R. & Borg-Graham, L.J. (1993). Does synaptic facilitation mediate motion facilitation in the retina? In Computation and Neural Systems 1992, ed. Eeckman, F. H. & Bower, J. M., pp. 159–163. Boston, Massachusetts: Kluwer Academic Press.CrossRefGoogle Scholar
Grzywacz, N.M. & Koch, C. (1987). Functional properties of models for direction selectivity in the retina. Synapse 1, 417–434.CrossRefGoogle ScholarPubMed
Guiloff, G.D. & Kolb, H. (1992). Neurons immunoreactive to choline acetyllransferase in the turtle retina. Vision Research 32, 2023–2030.CrossRefGoogle ScholarPubMed
Jensen, R.J. & De Voe, R.D. (1983). Comparisons of direclionally selective with other ganglion cells of the turtle retina: Intracellular recording and staining. Journal of Comparative Neurology 217, 271–287.CrossRefGoogle ScholarPubMed
Johnson, R.A. & Wichern, D.W. (1992). Applied Multivariate Statistical Analysis, Third Edition. Englewood Cliffs, New Jersey: Prentice Hall.Google Scholar
Kalichman, M.W. (1982). Pharmacological investigation of convulsant gamma-aminobutyric acid (GABA) antagonists in amygdala-kindled rats. Epilepsia 23, 163–171.CrossRefGoogle ScholarPubMed
Katz, B. & Miledi, R. (1968). The role of calcium in neuromuscular facilitation. Journal of Physiology 195, 481–492.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
Lam, D. M.-K. & Steinman, L. (1971). The uptake of [γ 3H]-amino-butyric acid in the goldfish retina. Proceedings of the National Academy of Sciences of the U.S.A. 68, 2777–2781.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Lukasiewicz, P.D. & Werblin, F.S. (1994). A novel GABA receptor modulates synaptic transmission from bipolar to ganglion and amacrine cells in the tiger salamander retina. Journal of Neuroscience 14, 1213–1223.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
Newberry, N.R. & Nicoll, R.A. (1984). A bicuculline-resistant inhibitory post-synaptic potential in rat hippocampal pyramidal cells in vitro. Journal of Physiology (London) 348, 239–254.CrossRefGoogle ScholarPubMed
Newberry, N.R. & Nicoll, R.A. (1985). Comparison of the action of baclofen with γ-aminobulyric acid on rat hippocampal pyramidal cells in vitro. Journal of Physiology (London) 360, 161–185.CrossRefGoogle Scholar
Nicoll, R.A. & Padjen, A. (1976). Pentylenetetrazol: An antagonist of GABA at primary afferents of the isolated frog spinal cord. Neuropharmacology 15, 69–71.CrossRefGoogle ScholarPubMed
Ögmen, H. (1991). On the mechanisms underlying directional selectivity. Neural Computation 3, 333–349.CrossRefGoogle ScholarPubMed
Olsen, R.W. (1981). GABA-benzodiazepine-barbiturate receptor interactions. Journal of Neurochemistry 37, 1–13.CrossRefGoogle ScholarPubMed
Olsen, R.W. (1982). Drug interactions at the GABA receptor ionophore complex. Annual Review of Pharmacology and Toxicology 22, 245–277.CrossRefGoogle ScholarPubMed
Pan, Z.H. & Slaughter, M.M. (1991). Control of retinal information coding by GABAB receptors. Journal of Neuroscience 11, 1810–1821.CrossRefGoogle ScholarPubMed
Parnas, L. & Parnas, H. (1986). Calcium is essential but insufficient for transmitter release: The calcium voltage hypothesis. Journal of Physiology (Paris) 81, 289–305.Google ScholarPubMed
Perlman, L., Normann, R.A., Chandler, J.P. & Lipetz, L.E. (1990). Effects of calcium ions on L-Type horizontal cells in the isolated turtle retina. Visual Neuroscience 4, 53–62.CrossRefGoogle ScholarPubMed
Poggio, T. & Reichardt, W.E. (1976). Visual control of orientation behaviour in the fly: Part II: Towards the underlying neural interactions. Quarterly Review of Biophysics 9, 377–438.CrossRefGoogle ScholarPubMed
Poznanski, R.R. (1992). Modelling the electrotonic structure of star-burst amacrine cells in the rabbit retina: A functional interpretation of dendritic morphology. Bulletin of Mathematical Biology 54, 905–928.CrossRefGoogle Scholar
Qian, H. & Dowling, J.E. (1993). Novel GABA response from rod-driven retinal horizontal cells. Nature 361, 162–164.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.CrossRefGoogle ScholarPubMed
Simmonds, M.A. (1982). Classification of some GABA antagonists with regard to site of action and potency in slices of rat cuneate nucleus. European Journal of Pharmacology 80, 347–358.CrossRefGoogle ScholarPubMed
Smith, R.D., Grzywacz, N.M., & Borg-Graham, L.J. (1991 a). Picro-toxin's effect on contrast dependence of turtle retinal direction selectivity. Investigative Ophthalmology and Visual Science 32, 1263.Google Scholar
Smith, R.D., Grzywacz, N.M. & Borg-Graham, L.J. (1991 b). GABA and facilitation in turtle retinal directional selectivity. Society for Neuroscience Abstracts 17, 1376.Google Scholar
Tachibana, M. & Kaneko, A. (1984). γ-Aminobutyric acid acts at axon terminals of turtle photoreceptors: Difference in sensitivity among cell types. Proceedings of the National Academv of Sciences of the U.S.A. 81, 7961–7964.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, ed. Osborne, N. & Chader, J. pp. 49–100. Oxford, UK: 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
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