Hostname: page-component-8448b6f56d-m8qmq Total loading time: 0 Render date: 2024-04-23T12:25:10.759Z Has data issue: false hasContentIssue false

Properties of stimulus-dependent synchrony in retinal ganglion cells

Published online by Cambridge University Press:  20 December 2007

SUSMITA CHATTERJEE
Affiliation:
Department of Biomedical Engineering, University of Southern California, Los Angeles, California
DAVID K. MERWINE
Affiliation:
Department of Biomedical Engineering, University of Southern California, Los Angeles, California
FRANKLIN R. AMTHOR
Affiliation:
Department of Psychology, University of Alabama at Birmingham, Birmingham, Alabama
NORBERTO M. GRZYWACZ
Affiliation:
Department of Biomedical Engineering, University of Southern California, Los Angeles, California Neuroscience Graduate Program, University of Southern California, Los Angeles, California

Abstract

Neighboring retinal ganglion cells often spike synchronously, but the possible function and mechanism of this synchrony is unclear. Recently, the strength of the fast correlation between ON-OFF directionally selective cells of the rabbit retina was shown to be stimulus dependent. Here, we extend that study, investigating stimulus-dependent correlation among multiple ganglion-cell classes, using multi-electrode recordings. Our results generalized those for directionally selective cells. All cell pairs exhibiting significant spike synchrony did it for an extended edge but rarely for full-field stimuli. The strength of this synchrony did not depend on the amplitude of the response and correlations could be present even when the cells' receptive fields did not overlap. In addition, correlations tended to be orientation selective in a manner predictable by the relative positions of the receptive fields. Finally, extended edges and full-field stimuli produced significantly greater and smaller correlations than predicted by chance respectively. We propose an amacrine-network model for the enhancement and depression of correlation. Such an apparently purposeful control of correlation adds evidence for retinal synchrony playing a functional role in vision.

Type
Research Article
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

Ackert, J.M., Wu, S.H., Lee, J.C., Abrams, J., Hu, E.H., Perlman, I. & Bloomfield, S.A. (2006). Light-induced changes in spike synchronization between coupled ON direction selective ganglion cells in the mammalian retina. Journal of Neuroscience 26, 42064215.CrossRefGoogle Scholar
Aertsen, A.M., Gerstein, G.L., Habib, M.K. & Palm, G. (1989). Dynamics of neuronal firing correlation: modulation of effective connectivity. Journal of Neurophysiology 61, 900917.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, 40024015.CrossRefGoogle Scholar
Alonso, J.M., Usrey, W.M. & Reid, R.C. (1996). Precisely correlated firing in cells of the lateral geniculate nucleus. Nature 383, 815819.CrossRefGoogle 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, 7296.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, 87121.Google Scholar
Amthor, F.R., Tootle, J.S. & Grzywacz, N.M. (2005). Stimulus-dependent correlated firing in directionally selective retinal ganglion cells. Visual Neuroscience 22, 769787.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, 209219.CrossRefGoogle Scholar
Arnett, D. & Spraker, T.E. (1981). Cross-correlation analysis of the maintained discharge of rabbit retinal ganglion cells. Journal of Physiology 317, 2947.CrossRefGoogle Scholar
Atick, J.J. & Redlich, A.N. (1990). Towards a theory of early visual processing. Neural Computation 2, 308320.CrossRefGoogle Scholar
Balboa, R.M. & Grzywacz, N.M. (2000a). The minimal local-asperity hypothesis of early retinal lateral inhibition. Neural Computation 12, 14851517.Google Scholar
Balboa, R.M. & Grzywacz, N.M. (2000b). The role of early retinal lateral inhibition: More than maximizing luminance information. Visual Neuroscience 17, 7789.Google Scholar
Balboa, R.M. & Grzywacz, N.M. (2000c). Occlusions and their relationship with the distribution of contrasts in natural images. Vision Research 40, 26612669.Google Scholar
Barlow, R.B., Birge, R.R., Kaplan, E. & Tallent, J.R. (1993). On the molecular origin of photoreceptor noise. Nature 366, 6466.CrossRefGoogle Scholar
Barnes, S. & Werblin, F. (1986). Gated currents generate single spike activity in amacrine cells of the tiger salamander retina. Proceeding of the National Academy of Sciences 83, 15091512.CrossRefGoogle Scholar
Bloomfield, S.A. (1992). Relationship between receptive and dendritic field size of amacrine cells in the rabbit retina. Journal of Neurophysiology 68, 711725.CrossRefGoogle Scholar
Boycott, B.B. & Wassle, H. (1974). The morphological types of ganglion cells of the domestic cat's retina. Journal of Physiology 240, 397419.CrossRefGoogle Scholar
Brainard, D.H. (1997). The Psychophysics Toolbox. Spatial Vision 10, 433436.CrossRefGoogle Scholar
Brivanlou, I.H., Warland, D.K. & Meister, M. (1998). Mechanisms of concerted firing among retinal ganglion cells. Neuron 20, 527539.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, 277298.CrossRefGoogle Scholar
Chatterjee, S., Merwine, D.K. & Grzywacz, N.M. (2006). Stimulus-dependent response correlations between rabbit retinal ganglion cells [abstract]. Journal of Vision 6, 62a.Google Scholar
Cook, P.B. & Werblin, F.S. (1994). Spike initiation and propagation in wide field transient amacrine cells of the salamander retina. Journal of Neuroscience 14, 38523861.CrossRefGoogle Scholar
Dacey, D.M. (1989). Axon-bearing amacrine cells of the macaque monkey retina. Journal of Comparative Neurology 284, 275293.CrossRefGoogle 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 6, 501517.CrossRefGoogle Scholar
DeVries, S.H. (1999). Correlated firing in rabbit retinal ganglion cells. Journal of Neurophysiology 81, 908920.CrossRefGoogle Scholar
Dowling, J.E. (1987). The Retina, an Approachable Part of the Brain. Cambridge, MA: Harvard University Press.
Engel, A.K., Kreiter, A.K., Konig, P. & Singer, W. (1991). Synchronization of oscillatory neuronal responses between straite and extrastraite visual cortical areas of the cat. Proceedings of the National Academy of Sciences 88, 60486052.CrossRefGoogle 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 Neuroscience 15, 218226.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 88, 91369140.Google Scholar
Erwin, E. & Miller, K.D. (1998). Correlation-based development of occularly matched orientation and ocular dominance maps: Determination of required input activities. Journal of Neuroscience 18, 98709895.Google Scholar
Euler, T., Schneider, H. & Wassle, H. (1996). Glutamate responses of bipolar cells in a slice preparation of the rat retina. Journal of Neuroscience 16, 29342944.CrossRefGoogle Scholar
Ferster, D., Chung, S. & Wheat, H. (1996). Orientation selectivity of thalamic input to simple cells of cat visual cortex. Nature 380, 249252.CrossRefGoogle Scholar
Gray, C.M., Konig, P., Engel, A.K. & Singer, W. (1989). Oscillatory responses in cat visual cortex exhibits inter-columnar synchronizations which reflect global stimulus properties. Nature 338, 334337.CrossRefGoogle Scholar
Grzywacz, N.M. & Amthor, F.R. (2007). Robust directional computation in on-off directionally selective ganglion cells of rabbit retina. Visual Neuroscience 24, 647661.CrossRefGoogle Scholar
Grzywacz, N.M. & Balboa, R.M. (2002). A bayesian framework for sensory adaptation. Neural Computation 14, 543559.CrossRefGoogle Scholar
Grzywacz, N.M. & Sernagor, E. (2000). Spontaneous activity in developing turtle retinal ganglion cells: statistical analysis. Visual Neuroscience 17, 229241.CrossRefGoogle Scholar
Guillory, K.S. & Normann, R.A. (1999). A 100-channel system for real time detection and storage of extracellular spike waveforms. Journal of Nueroscience Methods 91, 2129.CrossRefGoogle Scholar
Hu, E.H. & Bloomfield, S.A. (2003). Gap junctional coupling underlies the short-latency spike synchrony of retinal alpha ganglion cells. Journal of Neuroscience 23, 67686777.Google Scholar
Hubel, D.H. & Wiesel, T.N. (1962). Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. Journal of Physiology 160, 106154.CrossRefGoogle Scholar
Ichinose, T. & Lukasiewicz, P.D. (2005). Inner and outer retinal pathways both contribute to surround inhibition of salamander ganglion cells. Journal of Physiology 565, 517535.CrossRefGoogle Scholar
Johnson, R. & Wichern, D. (1992). Applied Multivariate Statistical Methods. Englewood Cliffs, NJ: Prentice Hall.
Kenyon, G.T., Moore, B., Jeffs, J., Denning, K.S., Stephens, G.J., Travis, B.J., George, J.S., Theiler, J. & Marshak, D.W. (2003). A model of high-frequency oscillatory potentials in retinal ganglion cells. Visual Neuroscience 20, 465480.CrossRefGoogle Scholar
Kishida, K. & Naka, K.I. (1967). Amino acids and the spikes from the retinal ganglion cells. Science 156, 648650.CrossRefGoogle Scholar
Kolb, H., Nelson, R. & Mariani, A. (1981). Amacrine cells, bipolar cells and ganglion cells of the cat retina: A Golgi study. Vision Research 21, 10811114.CrossRefGoogle Scholar
Li, W., Trexler, E.B. & Massey, S.C. (2002). Glutamate receptors at rod bipolar ribbon synapses in the rabbit retina. Journal of Comparative Neurology 448, 230248.CrossRefGoogle Scholar
Liu, F., Merwine, D.K. & Grzywacz, N.M. (2006). Statistically robust detection of spontaneous, non-stereotypical neural signals. Journal of Neuroscience Methods 153, 299311.CrossRefGoogle Scholar
MacNeil, M.A., Heussy, J.K., Dacheux, R.F., Raviola, E. & Masland, R.H. (1999). The shapes and numbers of amacrine cells: Matching of photofilled with Golgi-stained cells in the rabbit retina and comparison with other mammalian species. Journal of Comparatives Neurology 413, 305326.3.0.CO;2-E>CrossRefGoogle Scholar
MacNeil, M.A. & Masland, R.H. (1998). Extreme diversity among amacrine cells: Implications for function. Neuron 20, 971982.CrossRefGoogle Scholar
Mangel, S. (1991). Analysis of the horizontal cell contribution to the receptive field surround of ganglion cells in the rabbit retina. Journal of Physiology 442, 211234.CrossRefGoogle Scholar
Massey, S.C. & Miller, R.F. (1988). Glutamate receptors of ganglion cells in the rabbit retina: evidence for glutamate as a bipolar cell transmitter. Journal of Physiology 405, 635655.CrossRefGoogle Scholar
Mastronarde, D.N. (1983). Correlate firing of cat retinal ganglion cells. I. Spontaneously active inputs to X-and Y-cells. Journal of Neurophysiology 49, 303324.Google Scholar
McCarthy, S.T. & Owen, W.G. (1996). Preferential representation of natural scenes in the salamander retina. Investigative Ophthalmology and Visual Science 37, 5674.Google Scholar
Meister, M. (1996). Multineuronal codes in retinal signaling. Proceedings of the National Academy of Sciences 93, 609614.CrossRefGoogle Scholar
Meister, M., Lagnado, L. & Baylor, D.A. (1995). Concerted signaling by retinal ganglion cells. Science 270, 12071210.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, 15471567.CrossRefGoogle Scholar
Miller, R.F., Dacheux, R.F. & Frumkes, T.E. (1977). Amacrine cells in Necturus retina: Evidence for independent gamma-aminobutyric. Science 198, 748750.CrossRefGoogle Scholar
Minke, B., Wu, C.-F. & Pak, W.L. (1975). Induction of photoreceptor voltage noise in the dark in Drosophila mutant. Nature (London) 258, 8487.CrossRefGoogle Scholar
Naka, K.I. & Witkovsky, P. (1972). Dogfish ganglion cell discharge resulting from extrinsic polarization of the horizontal cells. Journal of Physiology 223, 449460.CrossRefGoogle Scholar
Neuenschwander, S., Castelo-Branco, M. & Singer, W. (1999). Synchronous oscillations in the cat retina. Vision Research 39, 24852497.CrossRefGoogle Scholar
Neuenschwander, S. & Singer, W. (1996). Long-range synchronization of oscillatory light responses in the cat retina and lateral geniculate nucleus. Nature 379, 728733.CrossRefGoogle Scholar
Nirenberg, S., Carcieri, S.M., Jacobs, A.L. & Latham, P.E. (2001). Retinal ganglion cells act largely as independent encoders. Nature 411, 698701.CrossRefGoogle Scholar
Pelli, D.G. (1997). The Video Toolbox software for visual psychophysics: Transforming numbers into movies. Spatial Vision 10, 437442.CrossRefGoogle Scholar
Ratliff, F. (1965). Mach bands: Quantitative Studies on Neural Networks in the Retina. San Francisco: Holden-Day.
Reid, R.C. & Alonso, J.M. (1995). Specificity of monosynaptic connections from thalamus to visual cortex. Nature 378, 281284.CrossRefGoogle Scholar
Reifsnider, E.S. & Tranchina, D. (1995). Background contrast modulates kinetics and lateral spread of responses to superimposed stimuli in outer retina. Visual Neuroscience 12, 11051126.CrossRefGoogle Scholar
Rodieck, R.W. & Stone, J. (1965). Response of cat retinal ganglion cells to moving visual patterns. Journal of Neurophysiology 28, 819832.CrossRefGoogle Scholar
Schwarz, C. & Bolz, J. (1991). Functional specificity of the long-range horizontal connections in cat visual cortex: A cross-correlation study. Journal of Neuroscience 11, 29953007.CrossRefGoogle Scholar
Singer, W. & Gray, C.M. (1995). Visual feature integration and the temporal correlation hypothesis. Annual Review of Neuroscience 18, 555586.CrossRefGoogle Scholar
Slaughter, M.M. & Miller, R.F. (1983). Bipolar cells in the mudpuppy retina use an excitatory amino acid neurotransmitter. Nature 303, 537538.CrossRefGoogle Scholar
Sprent, P. (1993). Applied Nonparametric Statistical Methods. London: Chapman & Hall.
Srinivasan, M.V., Laughlin, S.B. & Dubs, A. (1982). Predictive coding: A fresh review of inhibition in the retina. Proceedings of the Royal Society B: Biological Sciences 216, 27459.Google Scholar
Stafford, D.K. & Dacey, D.M. (1997). Physiology of the A1 amacrine: A spiking, axon-bearing interneuron of the macaque monkey retina. Visual Neuroscience 14, 507522.CrossRefGoogle Scholar
Thibos, L.N. & Werblin, F.S. (1978). The response properties of the steady antagonistic surround in the mudpuppy retina. Journal of Physiology 278, 7999.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, 54615467.CrossRefGoogle Scholar
Usrey, W.M. & Reid, R.C. (1999). Synchronous activity in the visual system. Annual Review of Physiology 61, 435456.CrossRefGoogle 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, 384387.CrossRefGoogle Scholar
Vitanova, L., Haverkamp, S. & Wassle, H. (2004). Immunocytochemical localization of glycine and glycine receptors in the retina of the frog Rana ridibunda. Cell Tissue Research 317, 227235.CrossRefGoogle Scholar
Volgyi, B., Xin, D., Amarillo, Y. & Bloomfield, S.A. (2001). Morphology and physiology of the polyaxonal amacrine cells in the rabbit retina. Journal of Comparative Neurology 440, 109125.CrossRefGoogle Scholar
Werblin, F.S. (1974). Control of retinal sensitivity. II. lateral interactions at the outer plexiform layer. Journal of General Physiology 63, 6287.Google Scholar
Werblin, F.S. & Copenhagen, D.R. (1974). Control of retinal sensitivity. III. Lateral interactions at the inner plexiform layer. Journal of General Physiology 63, 88110.Google Scholar
Wu, S.M., Gao, F. & Maple, B.R. (2000). Functional architecture of synapses in the inner retina: segregation of visual signals by stratification of bipolar cell axon terminals. Journal of Neuroscience 20, 44624470.CrossRefGoogle Scholar
Xin, D. & Bloomfield, S.A. (1997). Tracer coupling pattern of amacrine and ganglion cells in the rabbit retina. Journal of Comparative Neurology 383, 512528.3.0.CO;2-5>CrossRefGoogle Scholar
Yang, G. & Masland, R.H. (1994). Receptive fields and dendritic structure of directionally selective retinal ganglion cells. Journal of Neuroscience 14, 52675280.CrossRefGoogle Scholar
Zhou, C. & Dacheux, R.F. (2004). All amacrine cells in the rabbit retina possess AMPA-, NMDA-, GABA-, and glycine-activated currents. Visual Neuroscience 21, 131188.Google Scholar