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Stimulus-dependent correlated firing in directionally selective retinal ganglion cells

Published online by Cambridge University Press:  03 February 2006

FRANKLIN R. AMTHOR ,
JOHN S. TOOTLE  and
NORBERTO M. GRZYWACZ
FRANKLIN R. AMTHOR
Affiliation:
Department of Psychology, University of Alabama at Birmingham, Birmingham, Alabama
JOHN S. TOOTLE
Affiliation:
Department of Psychology, University of Alabama at Birmingham, Birmingham, Alabama
NORBERTO M. GRZYWACZ
Affiliation:
Department of Biomedical Engineering, Neuroscience Graduate Program, University of Southern California, Center for Visual Science and Technology, Los Angeles, California
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Abstract

Synchronous spiking has been postulated to be a meta-signal in visual cortex and other CNS loci that tags neuronal spike responses to a single entity. In retina, however, synchronized spikes have been postulated to arise via mechanisms that would largely preclude their carrying such a code. One such mechanism is gap junction coupling, in which synchronous spikes would be a by-product of lateral signal sharing. Synchronous spikes have also been postulated to arise from common-source inputs to retinal ganglion cells having overlapping receptive fields, and thus code for stimulus location in the overlap area. On–Off directionally selective ganglion cells of the rabbit retina exhibit a highly precise tiling pattern in which gap junction coupling occurs between some neighboring, same-preferred-direction cells. Depending on how correlated spikes arise, and for what purpose, one could postulate that synchronized spikes in this system (1) always arise in some subset of same-direction cells because of gap junctions, but never in non-same-preferred-directional cells; (2) never arise in same-directional cells because their receptive fields do not overlap, but arise only in different-directional cells whose receptive fields overlap, as a code for location in the overlap region; or (3) arise in a stimulus-dependent manner for both same- and different-preferred-direction cells for a function similar to that postulated for neurons in visual cortex. Simultaneous, extracellular recordings were obtained from neighboring On–Off directionally selective (DS) ganglion cells having the same and different preferred directions in an isolated rabbit retinal preparation. Stimulation by large flashing spots elicited responses from DS ganglion-cell pairs that typically showed little synchronous firing. Movement of extended bars, however, often produced synchronous spikes in cells having similar or orthogonal preferred directions. Surprisingly, correlated firing could occur for the opposite contrast polarity edges of moving stimuli when the leading edge of a sweeping bar excited the receptive field of one cell as its trailing edge stimulated another. Pharmacological manipulations showed that the spike synchronization is enhanced by excitatory cholinergic amacrine-cell inputs, and reduced by inhibitory GABAergic inputs, in a motion-specific manner. One possible interpretation is that this synchronous firing could be a signal to higher centers that the outputs of the two DS ganglion cells should be “bound” together as responding to a contour of a common object.

Keywords

Rabbit retinaDirectional selectivityGanglion cellCorrelated firingBinding problem
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 6 , November 2005 , pp. 769 - 787
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

Alonso, J.M., Usrey, W.M., & Reid, R.C. (1996). Precisely correlated firing in cells of the lateral geniculate nucleus. Nature 383, 815–819.CrossRefGoogle Scholar
Alonso, J.M., Usrey, W.M., & Reid, R.C. (2001). Rules of connectivity between geniculate cells and simple cells in cat primary visual cortex. Journal of Neuroscience 21, 4002–4015.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(6), 2174–2187.Google Scholar
Amthor, F.R. & Grzywacz, N.M. (1994). 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., Keyser, K.T. & Dacheux, R.F. (1997). Contribution of cholinergic amacrine cells to directional selectivity in rabbit retinal ganglion cells. Invest. Ophthal. Vis. Sci. 38, S949.Google Scholar
Amthor, F.R., Grzywacz, N.M., & Merwine, D.K. (1996). Extra-receptive field facilitation in On–Off DS ganglion cells of the rabbit retina. Visual Neuroscience 13(2), 303–310.CrossRefGoogle 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.CrossRefGoogle Scholar
Amthor, F.R. & Oyster, C.W. (1995). Spatial organization of retinal information about movement detection. Proceedings of the National Academy of Sciences of the USA 92(9), 4002–4005.CrossRefGoogle 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.CrossRefGoogle 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 Scholar
Amthor, F.R., Tootle, J.S., & Yildirim, A. (2003). A new transparent multi-unit recording array system fabricated by in-house laboratory technology. Journal of Neuroscience Methods 126, 209–211.CrossRefGoogle Scholar
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. (1982a). Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells. Journal of Physiology 324, 161–185.Google Scholar
Ariel, M. & Daw, N.W. (1982b). Effects of cholinergic drugs on receptive field properties of rabbit retinal ganglion cells. Journal of Physiology 324, 135–160.Google Scholar
Arnett, D. & Spraker, T.E. (1981). Cross-correlation analysis of the maintained discharge of rabbit retinal ganglion cells. Journal of Physiology 317, 29–47.CrossRefGoogle Scholar
Balboa, R.M. & Grzywacz, N.M. (2000). Occlusions and their relationship with the distribution of contrasts in natural images. Vision Research 40, 2661–2669.CrossRefGoogle Scholar
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 Scholar
Bearse, M.A., Jr., Shimada, Y., & Sutter, E.E. (2000). Distribution of oscillatory components in the central retina. Documenta Ophthalmologica 100, 185–205.CrossRefGoogle Scholar
Bloomfield, S.A. (1992). Relationship between receptive and dendritic field size of amacrine cells in the rabbit retina. Journal of Neurophysiology 68(3), 711–725.Google Scholar
Brivanlou, I.H., Warland, D.K., & Meister, M. (1998). Mechanisms of concerted firing among retinal ganglion cells. Neuron 20, 527–539.CrossRefGoogle Scholar
Brody, C.D. (1999a). Correlations without synchrony. Neural Computation 11, 1537–1551.Google Scholar
Brody, C.D. (1999b). Disambiguating different covariation types. Neural Computation 11, 1527–1535.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 276, 277–298.CrossRefGoogle Scholar
Castelo-Branco, M., Neuenschwander, S., & Singer, W. (1998). Synchronization of visual responses between the cortex, lateral geniculate nucleus, and retina in the anesthetized cat. Journal of Neuroscience 18, 6395–6410.Google Scholar
Dan, Y., Alonso, J.M., Usrey, W.M., & Reid, R.C. (1998). Coding of visual information by precisely correlated spikes in the lateral geniculate nucleus. Nature Neuroscience 1, 501–507.CrossRefGoogle Scholar
DeCharms, R.C. & Merzenich, M.M. (1996). Primary cortical representation of sounds by the coordination of action-potential timing. Nature 381, 610–613.CrossRefGoogle Scholar
DeVries, S.H. (1999). Correlated firing in rabbit retinal ganglion cells. Journal of Neurophysiology 81(2), 908–920.Google Scholar
Engel, A.K., Konig, P., Kreiter, A.K., Schillen, T.B., & Singer, W. (1992a). Temporal coding in the visual cortex: New vistas on integration in the nervous system. Trends in Neurosciences 15, 218–226.Google Scholar
Engel, A.K., Konig, P., & Singer, W. (1992b). Direct physiological evidence for scene segmentation by temporal coding. Proceedings of the National Academy of Sciences of the U.S.A. 88, 9136–9140.Google Scholar
Engel, A.K., Roelfsema, P.R., Fries, P., Brecht, M., & Singer, W. (1997). Role of the temporal domain for response selection and perceptual binding. Cerebral Cortex 7, 571–582.CrossRefGoogle Scholar
Euler, T., Detwiler, P.B., & Denk, W. (2002). Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418, 845–852.CrossRefGoogle Scholar
Famiglietti, E.V., Jr. (1983). On and off pathways through amacrine cells in mammalian retina: The synaptic connections of “starburst” amacrine cells. Vision Research 23, 1265–1279.CrossRefGoogle Scholar
Famiglietti, E.V., Jr. & Kolb, H. (1976). Structural basis for ON- and OFF-center responses in retinal ganglion cells. Science 194, 193–195.CrossRefGoogle Scholar
Feigenspan, A., Wassle, H., & Bormann, J. (1993). Pharmacology of GABA receptor Cl-channels in rat retinal bipolar cells. Nature 361, 159–162.CrossRefGoogle Scholar
Fernandez, E., Ferrandez, J.-M., Ammermuller, J., & Normann, R.A. (2000). Population coding in spike trains of simultaneously recorded retinal ganglion cells. Brain Research 887, 222–229.CrossRefGoogle Scholar
Field, D.J., Hayes, A., & Hess, R.F. (1993). Contour integration by the human visual system: Evidence for a local “association field”. Vision Research 33, 173–193.CrossRefGoogle Scholar
Fried, S.I., Munch, T.A., & Werblin, F.S. (2002). Mechanisms and circuitry underlying directional selectivity in the retina. Nature 420, 411–414.CrossRefGoogle Scholar
Friedman-Hill, S.R., Robertson, L.C., & Treisman, A.. (1995). Parietal contributions to visual feature binding: Evidence from a patient with bilateral lesions. Science 269, 853–855.CrossRefGoogle Scholar
Gerstein, G.L., Bedenbaugh, P., & Aertsen, A.M.H.J. (1989). Neuronal assemblies. IEEE Transactions on Biomedical Engineering 36, 4–14.CrossRefGoogle Scholar
Gilbert, C., Ito, M., Kapadia, M., & Westheimer, G. (2000). Interactions between attention, context and learning in primary visual cortex. Vision Research 40, 1217–1226.CrossRefGoogle Scholar
Grzywacz, N.M. & Amthor, F.R. (1993). Facilitation in On–Off directionally selective ganglion cells in the rabbit retina. Journal of Neurophysiology 69(6), 2188–2199.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 512.2, 575–581.Google Scholar
Grzywacz, N.M., Merwine, D.K., & Amthor, F.R. (1998b). Complementary roles of two excitatory pathways in retinal directional selectivity. Visual Neuroscience 15(6), 1119–1128.Google Scholar
Grzywacz, N.M. & Sernagor, E. (2000). Spontaneous activity in developing turtle retinal ganglion cells: Statistical analysis. Visual Neuroscience 17, 229–241.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., Jin, Z.F., & Masland, R.H. (1999). The nondiscriminating zone of directionally selective retinal ganglion cells: Comparison with dendritic structure and implications for mechanism. Journal of Neuroscience 19, 8049–8056.Google Scholar
Hess, R. & Field, D. (1999). Integration of contours: New insights. Trends in Cognitive Science 3, 480–486.CrossRefGoogle Scholar
Jensen, O. & Lisman, J.E. (1998). An oscillatory short-term memory buffer can account for data on the Sternberg task. Journal of Neuroscience 15, 10688–10699.Google Scholar
Jensen, R.J. (1995). Receptive-field properties of displaced starburst amacrine cells change following axotomy-induced degeneration of ganglion cells. Visual Neuroscience 12, 177–184.CrossRefGoogle Scholar
Kenyon, G.T. & Marshak, D.W. (1998). Gap junctions with amacrine cells provide a feedback pathway for ganglion cells within the retina. Proceedings of the Royal Society B (London) 265, 919–925.CrossRefGoogle Scholar
Kittila, C.A. & Massey, S.C. (1995). Effect of ON pathway blockade on directional selectivity in the rabbit retina. Journal of Neurophysiology 73(2), 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
Knapp, A.G. & Mistler, L.A. (1983). Response properties of cells in rabbit's lateral geniculate nucleus during reversible blockade of retinal on-center channel. Journal of Neurophysiology 50, 1236–1245.Google Scholar
Konig, P., Engel, A.K., & Singer, W. (1996). Integrator or coincidence detector? The role of the cortical neuron revisited. Trends in Neuroscience 19, 130–137.CrossRefGoogle Scholar
Levick, W.R., Oyster, C.W., & Takahashi, E. (1969). Rabbit lateral geniculate nucleus: Sharpener of directional information. Science 165, 712–714.CrossRefGoogle Scholar
Lukasiewicz, P.D., Maple, B.R., & Werblin, F.S. (1994). A novel GABA receptor on bipolar cell terminals in the tiger salamander retina. Journal of Neuroscience 14, 1202–1212.Google Scholar
Lukasiewicz, P.D. & Shields, C.R. (1998). A diversity of GABA receptors in the retina. Seminars in Cell and Developmental Biology 9, 293–299.CrossRefGoogle Scholar
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.Google Scholar
Marc, R.E. & Jones, B.W. (2002). Molecular phenotyping of retinal ganglion cells. Journal of Neuroscience 22(2), 413–427.Google Scholar
Masland, R.H., Mills, J.W., & Cassidy, C. (1984). The functions of acetylcholine in the rabbit retina. Proceedings Royal Society B (London) 223, 121–139.CrossRefGoogle Scholar
Mastronarde, D.N. (1983). Correlate firing of cat retinal ganglion cells. I. Spontaneously active inputs to X- and Y-cells. Journal of Neuorphysiology 49(2), 303–324.Google Scholar
Meister, M., Lagnado, L., & Baylor, D.A. (1995). Concerted signaling by retinal ganglion cells. Science 270, 1207–1210.CrossRefGoogle Scholar
Merwine, D.K., Amthor, F.R., & Grzywacz, N.M. (1995). Interaction between center and surround in rabbit retinal ganglion cells. Journal of Neurophysiology 73, 1547–1567.Google Scholar
Moore, C. & Cavanagh, P. (1998). Recovery of 3D volume from 2-tone images of novel objects. Cognition 67, 45–71.CrossRefGoogle Scholar
Neuenschwander, S., Castelo-Branco, M., Baron, J., & Singer, W. (2002). Feed-forward synchronization: Propagation of temporal patterns along the retinothalamocortical pathway. Philosophical Transactions of the Royal Society B (London) 357, 1869–1876.CrossRefGoogle Scholar
Neuenschwander, S., Castelo-Branco, M., & Singer, W. (1999). Synchronous oscillations in the cat retina. Vision Research 39, 2485–2497.CrossRefGoogle Scholar
Nirenberg, S., Carcieri, S.M., Jacobs, A.L., & Latham, P.E. (2001). Retinal ganglion cells act largely as independent encoders. Nature 411, 698–701.CrossRefGoogle Scholar
Oyster, C.W. (1968). The analysis of image motion by the rabbit retina. Journal of Physiology 199, 613–635.CrossRefGoogle Scholar
Qian, H. & Dowling, J.E. (1993). Novel GABA responses from rod-driven retinal horizontal cells. Nature 361, 162–164.CrossRefGoogle 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(6), 861–872.CrossRefGoogle Scholar
Riesenhuber, M. & Poggio, T. (1999). Are cortical models really bound by the “binding problem”? Neuron 24, 87–93.Google Scholar
Ruderman, D.L. & Bialek, W. (1994). Statistics of natural images: Scaling in the woods. Physics Review and Letters 73, 814–817.CrossRefGoogle Scholar
Sillito, A.M., Jones, H.E., Gerstein, G.L., & West, D.C. (1994). Feature-linked synchronization of thalamic relay cell firing induced by feedback from the visual cortex. Nature 369, 479–482.CrossRefGoogle Scholar
Slaughter, M.M. & Pan, Z.H. (1992). The physiology of GABAB receptors in the vertebrate retina. Progress in Brain Research 90, 47–60.CrossRefGoogle Scholar
Softky, W.R. & Koch, C. (1993). The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs. Journal of Neuroscience 13, 334–350.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(17), 7712–7720.Google Scholar
Tononi, G., Sporns, O., & Edelman, G.M. (1992). Reentry and the problem of integrating multiple cortical areas: Simulation of dynamic integration in the visual system. Cerebral Cortex 2, 310–335.CrossRefGoogle Scholar
Treisman, A. (1996). The binding problem. Current Opinion in Neurobiology 6, 171–178.CrossRefGoogle Scholar
Usrey, W.M., Alonso, J.-M., & Reid, R.C. (2000). Synaptic interactions between thalamic inputs to simple cells in cat visual cortex. Journal of Neuroscience 20, 5461–5467.Google Scholar
Usrey, W.M., Reppas, J.B., & Reid, R.C. (1998). Paired-spike interactions and synaptic efficacy of retinal inputs to the thalamus. Nature 395, 384–387.Google Scholar
Usrey, W.M., Reppas, J.B., & Reid, R.C. (1999). Specificity and strength of retinogeniculate connections. Journal of Neurophysiology 82, 3527–3540.Google Scholar
Vaney, D.I. (1990). Biocytin dye-coupling reveals subpopulations of direction-selective ganglion cells in rabbit retina. Proceedings of the Australian Neuroscience Society 1, 136.Google Scholar
Vaney, D.I. (1990). The mosaic of amacrine cells in the mammalian retina. In Osborne, N. & Chader, J. (Eds.), Progress in Retinal Research (vol. 9), (pp. 49–100). Oxford, England: Pergamon.
Vaney, D.I. (1994). Territorial organization of direction-selective ganglion cells in rabbit retina. Journal of Neuroscience 14(11), 6301–6313.Google Scholar
Vaney, D.I. & Taylor, W.R. (2002). Direction selectivity in the retina. Current Opinion in Neurobiology 12, 405–410.CrossRefGoogle Scholar
Veruki, M.L. & Hartveit, E. (2002). AII (Rod). amacrine cells form a network of electrically coupled interneurons in the mammalian retina. Neuron 33, 935–946.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
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.CrossRefGoogle Scholar
Zhu, S.C. & Mumford, D. (1997). Prior learning and Gibbs reaction-diffusion. IEEE Transactions on Pattern Analysis and Machine Intelligence 19, 1236–1250.Google Scholar
Zucker, C.L., Nilson, J.E., Ehinger, B., & Grzywacz, M.N. (2005). Compartmental localization of γ-aminobutyric acid type b receptors in the cholinergic circuitry of the rabbit retina. Journal of Comparative Neurology 493, 448–459.CrossRefGoogle Scholar