Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-26T07:25:28.027Z Has data issue: false hasContentIssue false
  • English
  • Français

Robust directional computation in on-off directionally selective ganglion cells of rabbit retina

Published online by Cambridge University Press:  28 September 2007

NORBERTO M. GRZYWACZ  and
FRANKLIN R. AMTHOR
NORBERTO M. GRZYWACZ
Affiliation:
Department of Biomedical Engineering and Neuroscience Graduate Program, University of Southern California, Los Angeles, California
FRANKLIN R. AMTHOR
Affiliation:
Department of Psychology, University of Alabama at Birmingham, Birmingham Alabama
Get access Rights & Permissions [Opens in a new window]

Abstract

The spatial and temporal interactions in the receptive fields of On-Off directionally selective (DS) ganglion cells endow them with directional selectivity. Using a variety of stimuli, such as sinusoidal gratings, we show that these interactions make directional selectivity of the DS ganglion cell robust with respect to stimulus parameters such as contrast, speed, spatial frequency, and extent of motion. Moreover, unlike the directional selectivity of striate-cortex cells, On-Off DS ganglion cells display directional selectivity to motions not oriented perpendicularly to the contour of the objects. We argue that these cells may achieve such high robustness by combining multiple mechanisms of directional selectivity.

Keywords

Directional SelectivitySpeed TuningPlaidGanglion CellsRetina
Type
Research Article
Information
Visual Neuroscience , Volume 24 , Issue 4 , July 2007 , pp. 647 - 661
Copyright
© 2007 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.)

References

REFERENCES

Adelson, E.H. & Movshon, J.A. (1982). Phenomenal coherence of moving visual patterns. Nature 300, 523–525.Google Scholar
Ames, A., III & Nesbett, F.B. (1981). In vitro retina as an experimental model of the central nervous system. Journal of Neurochemistry 37, 867–877.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 20, 217.Google Scholar
Amthor, F.R., Grzywacz, N.M. & Dacheux, R.F. (1999). Whole cell patch clamp recordings of on-off directionally selective rabbit retinal ganglion cells to photic and current inputs. Investigative Ophthalmology & Visual Science 40, S589.Google Scholar
Amthor, F.R., Tootle, J.S. & Grzywacz, N.M. (2005a). Stimulus-dependent correlated firing in directionally selective retinal ganglion cells. Visual Neuroscience 22, 769–787.Google Scholar
Amthor, F.R., Tootle, J.S. & Gawne, T.J. (2005b). Retinal ganglion cell coding in simulated active vision. Visual Neuroscience 22, 789–806.Google Scholar
Amthor, F.R. & Grzywacz, N.M. (1988). The time course of inhibition and the velocity independence of direction selectivity in the rabbit retina. Investigative Ophthalmology & Visual Science 29, 225.Google Scholar
Amthor, F.R. & Grzywacz, N.M. (1991). The nonlinearity of the inhibition underlying retinal directional selectivity. Visual Neuroscience 6, 197–206.Google Scholar
Amthor, F.R. & Grzywacz, N.M. (1992). Response of rabbit directionally selective ganglion cells to moving gratings and plaids. Investigative Ophthalmology & Visual Science 33, 907.Google Scholar
Amthor, F.R. & Grzywacz, N.M. (1993). Inhibition in On-Off directionally selective ganglion cells in the rabbit retina. Journal of Neurophysiology 69, 2174–2187.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.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., Oyster, C.W. & Takahashi, E.S. (1984). Morphology of ON-OFF direction-selective ganglion cells in the rabbit retina. Brain Research 298, 187–190.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. (1982). Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells. Journal of Physiology (London) 324, 161–185.Google Scholar
Barlow, H.B. & Levick, W.R. (1965). The mechanism of directionally selective units in the rabbit's retina. Journal of Physiology (London) 178, 477–504.Google 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 (London) 276, 277–298.Google Scholar
Dacheux, R.F., Chimento, M.F. & Amthor, F.R. (2003). Synaptic input to the On-Off directionally selective ganglion cell in the rabbit retina. Journal of Comparative Neurology 456, 267–278.Google Scholar
Elliot, P.B. (1964). Tables of d'. In Signal Detection and Recognition by Human Observers, ed. Swets, J.A., pp. 651–684. New York: John Wiley.
Euler, T., Detwiler, P.B. & Denk, W. (2002). Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418, 845–852.Google Scholar
Famiglietti, E.V. (2002). A structural basis for omnidirectional connections between starburst amacrine cells and directionally selective ganglion cells in rabbit retina, with associated bipolar cells. Visual Neuroscience 19, 145–162.Google Scholar
Fennema, C. & Thompson, W. (1979). Velocity determination in scenes containing several moving objects. Computer Graphics and Image Processing 9, 301–315.Google Scholar
Fried, S.I., Munch, T.A. & Werblin, F.S. (2002). Mechanisms and circuitry underlying directional selectivity in the retina. Nature 420, 411–414.Google Scholar
Green, D.M. & Swets, J.A. (1966). Signal Detection Theory and Psychophysics. New York: John Wiley.
Grzywacz, N.M. & Amthor, F.R. (1993). Facilitation in On-Off directionally selective ganglion cells in the rabbit retina. Journal of Neurophysiology 69, 2188–2199.Google Scholar
Grzywacz, N.M. & Merwine, D.K. (2002a). Neural basis of motion perception. In Encyclopedia of Cognitive Science, Vol. 3, 86–98. Cambridge, UK: Macmillan Press.
Grzywacz, N.M. & Merwine, D.K. (2002b). Directional selectivity. In Handbook of Brain Theory and Neural Networks, Second Edition, ed. Arbib, M.A., pp. 354–358. Cambridge, MA: MIT Press.
Grzywacz, N.M. & Koch, C. (1987). Functional properties of models for direction selectivity in the retina. Synapse 1, 417–434.Google Scholar
Grzywacz, N.M., Amthor, F.R. & Dacheux, R.F. (1995). Are cholinergic synapses to directionally selective ganglion cells spatially asymmetric? Investigative Ophthalmology & Visual Science 36, S865.Google Scholar
Grzywacz, N.M., Amthor, F.R. & Merwine, D.K. (1994a). Directional hyperacuity in ganglion cells of the rabbit retina. Visual Neuroscience 11, 1019–1025.Google Scholar
Grzywacz, N.M., Amthor, F.R. & Merwine, D.K. (1998a). Necessity of acetylcholine for retinal directionally selective responses to drifting gratings in rabbit. Journal of Physiology 512, 575–581.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.Google Scholar
Grzywacz, N.M. & Poggio, T. (1990). Computation of Motion by Real Neurons. In An Introduction to Neural and Electronic Networks, ed. Zornetzer, S.F., Davis, J.L. & Lau, C., pp. 379–403. Orlando: Academic Press.
Grzywacz, N.M., Harris, J.M. & Amthor, F.R. (1994b). Computational and neural constraints for the measurement of local visual motion. In Visual Detection of Motion, ed. Smith, A.T. & Snowden, R.J., pp. 19–50. San Diego: Academic Press.
Grzywacz, N.M., Merwine, D.K. & Amthor, F.R. (1998b). Complementary roles of two excitatory pathways in retinal directional selectivity. Visual Neuroscience 15, 1119–1127.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
He, S. & Levick, W.R. (2000). Spatial-temporal response characteristics of the ON-OFF direction selective ganglion cells in the rabbit retina. Neuroscience Letters 285, 25–28.Google Scholar
He, S., Levick, W.R. & Vaney, D.I. (1998). Distinguishing direction selectivity from orientation selectivity in the rabbit retina. Visual Neuroscience 15, 439–447.Google Scholar
Holub, R.A. & Morton-Gibson, M. (1981). Response of visual cortical neurons of the cat to moving sinusoidal gratings: Response-contrast functions and spatiotemporal integration. Journal of Neurophysiology 46, 1244–1259.Google Scholar
Horn, B. & Shunck, B. (1981). Determining optical flow. Artificial Intelligence 17, 185–203.Google Scholar
Ikeda, H. & Wright, M.J. (1975). Spatial and temporal properties of ‘sustained’ and ‘transient’ neurones in area 17 of the cat's visual cortex. Experimental Brain Research 22, 363–383.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.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
Lee, S. & Zhou, Z.J. (2006). The synaptic mechanism of direction selectivity in distal processes of starburst amacrine cells. Neuron 51, 787–799.Google Scholar
Levick, W.R., Oyster, C.W. & Takahashi, E. (1969). Rabbit lateral geniculate nucleus: Sharpener of directional information. Science 165, 712–714.Google Scholar
Levick, W.R. (1967). Receptive fields and trigger features of ganglion cells in the visual streak of the rabbit's retina. Journal of Physiology 188, 285–307.Google Scholar
Masland, R.H., Mills, J.W. & Cassidy, C. (1984). The functions of acetylcholine in the rabbit retina. Proceedings of the Royal Society London B 223, 121–139.Google Scholar
Merwine, D.K., Amthor, F.R. & Grzywacz, N.M. (1995). The interaction between center and surround of rabbit retinal ganglion cells. Journal of Neurophysiology 73, 1547–1567.Google Scholar
Merwine, D.K., Amthor, F.R. & Grzywacz, N.M. (1998). Non-monotonic contrast behavior in directionally selective ganglion cells and evidence for its dependence on their GABAergic input. Visual Neuroscience 15, 1129–1136.Google Scholar
Movshon, J.A., Adelson, E.H., Gizzi, M.S. & Newsome, W.T. (1985). The analysis of moving visual patterns. In Pattern Recognition Mechanisms, ed. Chagas, C., Gattas, R. & Gross, C.G., pp. 117–151. Rome: Vatican Press.
Oesch, N., Euler, T. & Taylor, W.R. (2005). Direction-selective dendritic action potentials in rabbit retina. Neuron 47, 739–750.Google Scholar
Oyster, C.W. (1968). The analysis of image motion by the rabbit retina. Journal of Physiology 199, 613–635.Google Scholar
Poggio, T. & Reichardt, W.E. (1973). Considerations on models of movement detection. Kybernetik 13, 223–227.Google Scholar
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.Google Scholar
Pu, M.-L. & Amthor, F.R. (1990a). Dendritic morphologies of retinal ganglion cells projecting to the Nucleus of the Optic Tract in rabbit. Journal of Comparative Neurology 302, 657–674.Google Scholar
Pu, M.-L. & Amthor, F.R. (1990b). Dendritic morphologies of retinal ganglion cells projecting to the Lateral Geniculate Nucleus in rabbit. Journal of Comparative Neurology 302, 675–693.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., Amthor, F.R. & Keyser, K.T. (2005). MLA-sensitive cholinergic receptors involved in the detection of complex moving stimuli in retina. Visual Neuroscience 21, 861–872.Google Scholar
Rodman, H.R. & Albright, T.D. (1989). Single-unit analysis of pattern-motion selective properties in the middle temporal visual area (MT). Experimental Brain Research 75, 53–64.Google Scholar
Salinas, E. & Abbott, L.F. (1994). Vector reconstruction from firing rates. Journal of Computational Neuroscience 1, 89–107.Google Scholar
Schmidt, M., Humphrey, M. & Wassle, H. (1987). Action and localization of acetylcholine in the cat retina. Neuroscience Letters 59, 235–240.Google Scholar
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, 423–439.Google Scholar
Stasheff, S.F. & Masland, R.H. (2002). Functional inhibition in direction-selective retinal ganglion cells: Spatiotemporal extent and intralaminar interactions. Journal of Neurophysiology 88, 1026–1039.Google Scholar
Taylor, W.R. & Vaney, D.I. (2002). Diverse synaptic mechanisms generate direction selectivity in the rabbit retina. Journal of Neuroscience 22, 7712–7720.Google Scholar
Taylor, W.R., He, S., Levick, W.R. & Vaney, D.I. (2000). Dendritic computation of direction selectivity by retinal ganglion cells. Science 289, 2256–2257.Google Scholar
Tjepkes, D.S. & Amthor, F.R. (2000). The role of NMDA channels in rabbit retinal directional selectivity. Visual Neuroscience 17, 291–302.Google Scholar
Tolhurst, D.J. & Movshon, J.A. (1975). Spatial and temporal contrast sensitivity of striate cortical neurons. Nature 257, 674–675.Google Scholar
Vaney, D.I. & Taylor, W.R. (2002). Direction selectivity in the retina. Current Opinions in Neurobiology 12, 405–410.Google Scholar
Vaney, D.I., He, S., Taylor, W.R. & Levic, W.R. (2001). Direction-selective ganglion cells in the retina. In Motion Vision, Computational, Neural and Ecological Constraints, ed. Zanker, J. & Zeil, J., pp. 13–56. Berlin: Springer-Verlag.
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
Yates, F. (1934). Contingency tables involving small numbers and the c2 test. Journal of the Royal Statistical Society Supplement 1, 217–235.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