Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-05T04:51:53.444Z Has data issue: false hasContentIssue false
  • English
  • Français

A high frequency resonance in the responses of retinal ganglion cells to rapidly modulated stimuli: A computer model

Published online by Cambridge University Press:  04 October 2006

J.A. MILLER ,
K.S. DENNING ,
J.S. GEORGE ,
D.W. MARSHAK  and
G.T. KENYON
J.A. MILLER
Affiliation:
Applied Modern Physics, Los Alamos National Laboratory, Los Alamos, New Mexico Neuroscience Interdepartmental Program, University of California at Los Angeles, Los Angeles, California
K.S. DENNING
Affiliation:
Applied Modern Physics, Los Alamos National Laboratory, Los Alamos, New Mexico Computational Neurobiology, University of California at San Diego, San Diego, California
J.S. GEORGE
Affiliation:
Applied Modern Physics, Los Alamos National Laboratory, Los Alamos, New Mexico
D.W. MARSHAK
Affiliation:
Department of Neurobiology and Anatomy, University of Texas Medical School, Houston, Texas
G.T. KENYON
Affiliation:
Applied Modern Physics, Los Alamos National Laboratory, Los Alamos, New Mexico
Get access Rights & Permissions [Opens in a new window]

Abstract

Brisk Y-type ganglion cells in the cat retina exhibit a high frequency resonance (HFR) in their responses to large, rapidly modulated stimuli. We used a computer model to test whether negative feedback mediated by axon-bearing amacrine cells onto ganglion cells could account for the experimentally observed properties of HFRs. Temporal modulation transfer functions (tMTFs) recorded from model ganglion cells exhibited HFR peaks whose amplitude, width, and locations were qualitatively consistent with experimental data. Moreover, the wide spatial distribution of axon-mediated feedback accounted for the observed increase in HFR amplitude with stimulus size. Model phase plots were qualitatively similar to those recorded from Y ganglion cells, including an anomalous phase advance that in our model coincided with the amplification of low-order harmonics that overlapped the HFR peak. When axon-mediated feedback in the model was directed primarily to bipolar cells, whose synaptic output was graded, or else when the model was replaced with a simple cascade of linear filters, it was possible to produce large HFR peaks but the region of anomalous phase advance was always eliminated, suggesting the critical involvement of strongly non-linear feedback loops. To investigate whether HFRs might contribute to visual processing, we simulated high frequency ocular tremor by rapidly modulating a naturalistic image. Visual signals riding on top of the imposed jitter conveyed an enhanced representation of large objects. We conclude that by amplifying responses to ocular tremor, HFRs may selectively enhance the processing of large image features.

Keywords

CatAlpha ganglion cellY ganglion cellAmacrine cellGap junctionSimulation
Type
Research Article
Information
Visual Neuroscience , Volume 23 , Issue 5 , September 2006 , pp. 779 - 794
Copyright
2006 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

Ariel, M., Daw, N.W., & Rader, R.K. (1983). Rhythmicity in rabbit retinal ganglion cell responses. Vision Research 23, 1485–1493.CrossRefGoogle Scholar
Dacey, D.M. & Brace, S. (1992). A coupled network for parasol but not midget ganglion cells in the primate retina. Visual Neuroscience 9, 279–290.CrossRefGoogle Scholar
De Carli, F., Narici, L., Canovaro, P., Carozzo, S., Agazzi, E., & Sannita, W.G. (2001). Stimulus- and frequency-specific oscillatory mass responses to visual stimulation in man. Clinical Electroencephalography 32, 145–151.Google Scholar
Euler, T. & Masland, R.H. (2000). Light-evoked responses of bipolar cells in a mammalian retina. Journal of Neurophysiology 83, 1817–1829.Google Scholar
Euler, T. & Wassle, H. (1998). Different contributions of GABAA and GABAC receptors to rod and cone bipolar cells in a rat retinal slice preparation. Journal of Neurophysiology 79, 1384–1395.Google Scholar
Fahey, P.K. & Burkhardt, D.A. (2001). Effects of light adaptation on contrast processing in bipolar cells in the retina. Visual Neuroscience 18, 581–597.CrossRefGoogle Scholar
Foerster, M.H., van de Grind, W.A., & Grusser, O.J. (1977). The response of cat horizontal cells to flicker stimuli of different area, intensity and frequency. Experimental Brain Research 29, 367–385.Google Scholar
Freed, M.A. (2000). Rate of quantal excitation to a retinal ganglion cell evoked by sensory input. Journal Neurophysiology 83, 2956–2966.Google Scholar
Freed, M.A., Pflug, R., Kolb, H., & Nelson, R. (1996). ON-OFF amacrine cells in cat retina. Journal of Comparative Neurology 364, 556–566.Google Scholar
Freed, M.A., Smith, R.G., & Sterling, P. (2003). Timing of quantal release from the retinal bipolar terminal is regulated by a feedback circuit. Neuron 38, 89–101.Google Scholar
Freed, M.A. & Sterling, P. (1988). The ON-alpha ganglion cell of the cat retina and its presynaptic cell types. Journal of Neuroscience 8, 2303–2320.Google Scholar
Frishman, L.J., Freeman, A.W., Troy, J.B., Schweitzer-Tong, D.E., & Enroth-Cugell, C. (1987). Spatiotemporal frequency responses of cat retinal ganglion cells. Journal of General Physiology 89, 599–628.Google Scholar
Frishman, L.J., Saszik, S., Harwerth, R.S., Viswanathan, S., Li, Y., Smith, E.L., 3rd, Robson, J.G., & Barnes, G. (2000). Effects of experimental glaucoma in macaques on the multifocal ERG. Multifocal ERG in laser-induced glaucoma. Documenta Ophthalmologica 100, 231–251.Google Scholar
Frishman, L.J. & Sieving, P.A. (1995). Evidence for two sites of adaptation affecting the dark-adapted ERG of cats and primates. Vision Research 35, 435–442.Google Scholar
Greschner, M., Bongard, M., Rujan, P., & Ammermuller, J. (2002). Retinal ganglion cell synchronization by fixational eye movements improves feature estimation. Nature Neuroscience 5, 341–347.Google Scholar
Hennig, M.H., Kerscher, N.J., Funke, K., & Worgotter, F. (2002). Stochastic resonance in visual cortical neurons: Does the eye-tremor actually improve visual acuity?. Neurocomputing 10th Computational Neuroscience Meeting (CSN 01) Computational Neuroscience: Trends in Research 2002, July 2001, Monterey, CA, USA 44/46, 115–120.Google Scholar
Hurley, J.B. (2002). Shedding light on adaptation. Journal of General Physiology 119, 125–128.Google Scholar
Ishikane, H., Gangi, M., Honda, S., & Tachibana, M. (2005). Synchronized retinal oscillations encode essential information for escape behavior in frogs. Nature Neuroscience 8, 1087–1095. Epub 2005 Jul. 3.Google Scholar
Ishikane, H., Kawana, A., & Tachibana, M. (1999). Short- and long-range synchronous activities in dimming detectors of the frog retina. Visual Neuroscience 16, 1001–1014.Google Scholar
Jacoby, R., Stafford, D., Kouyama, N., & Marshak, D. (1996). Synaptic inputs to ON parasol ganglion cells in the primate retina. Journal of Neuroscience 16, 8041–8056.Google Scholar
Kenyon, G.T., Harvey, N.R., Stephens, G.J., & Theiler, J. (2004a). Dynamic segmentation of gray-scale images in a computer model of the mammalian retina. Proceedings SPIE: Applications of Digital Image Processing XXVII, Denver.
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 London Series B Biological Sciences 265, 919–925.Google Scholar
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, 465–480.Google Scholar
Kenyon, G.T., Theiler, J., George, J.S., Travis, B.J., & Marshak, D.W. (2004b). Correlated firing improves stimulus discrimination in a retinal model. Neural Computation 16, 2261–2291.Google Scholar
Kenyon, G.T., Travis, B.J., Theiler, J., George, J.S., Stephens, G.J., & Marshak, D.W. (2004c). Stimulus-specific oscillations in a retinal model. IEEE Transactions on Neural Networks 15, 1083–1091.Google Scholar
Kolb, H. & Nelson, R. (1993). OFF-alpha and OFF-beta ganglion cells in cat retina: II. Neural circuitry as revealed by electron microscopy of HRP stains. Journal of Comparative Neurology 329, 85–110.Google Scholar
Lee, B.B., Pokorny, J., Smith, V.C., & Kremers, J. (1994). Responses to pulses and sinusoids in macaque ganglion cells. Vision Research 34, 3081–3096.Google Scholar
Martin, P.R., Lee, B.B., White, A.J., Solomon, S.G., & Ruttiger, L. (2001). Chromatic sensitivity of ganglion cells in the peripheral primate retina. Nature 410, 933–936.Google Scholar
Martinez-Conde, S., Macknik, S.L., & Hubel, D.H. (2004). The role of fixational eye movements in visual perception. Nature Reviews Neuroscience 5, 229–2240.Google Scholar
Meister, M. & Berry, M.J., 2nd. (1999). The neural code of the retina. Neuron 22, 435–450.Google Scholar
Neuenschwander, S., Castelo-Branco, M., & Singer, W. (1999). Synchronous oscillations in the cat retina. Vision Research 39, 2485–2497.Google Scholar
Neuenschwander, S. & Singer, W. (1996). Long-range synchronization of oscillatory light responses in the cat retina and lateral geniculate nucleus. Nature 379, 728–732.Google Scholar
O'Brien, B.J., Isayama, T., Richardson, R., & Berson, D.M. (2002). Intrinsic physiological properties of cat retinal ganglion cells. Journal of Physiology 538, 787–802.Google Scholar
O'Brien, B.J., Richardson, R.C., & Berson, D.M. (2003). Inhibitory network properties shaping the light evoked responses of cat alpha retinal ganglion cells. Visual Neuroscience 20, 351–361.Google Scholar
Passaglia, C.L., Enroth-Cugell, C., & Troy, J.B. (2001). Effects of remote stimulation on the mean firing rate of cat retinal ganglion cells. Journal of Neuroscience 21, 5794–5803.Google Scholar
Peichl, L. (1991). Alpha ganglion cells in mammalian retinae: Common properties, species differences, and some comments on other ganglion cells. Visual Neuroscience 7, 155–169.Google Scholar
Press, W.H., Flannery, B.P., Teukolsky, S.A., & Vetterling, W.T. (1986). Numerical Recipes. Cambridge: Cambridge University Press.
Reich, D.S., Victor, J.D., Knight, B.W., Ozaki, T., & Kaplan, E. (1997). Response variability and timing precision of neuronal spike trains in vivo. Journal of Neurophysiology 77, 2836–2841.Google Scholar
Robinson, D.W. & Chalupa, L.M. (1997). The intrinsic temporal properties of alpha and beta retinal ganglion cells are equivalent. Current Biology 7, 366–374.Google Scholar
Schnapf, J.L., Nunn, B.J., Meister, M., & Baylor, D.A. (1990). Visual transduction in cones of the monkey Macaca fascicularis. Journal of Physiology 427, 681–713.Google Scholar
Shapley, R. (1997). Retinal physiology: Adapting to the changing scene. Current Biology 7, R421–423.Google Scholar
Shapley, R.M. & Victor, J.D. (1978). The effect of contrast on the transfer properties of cat retinal ganglion cells. Journal of Physiology 285, 275–298.Google Scholar
Shapley, R.M. & Victor, J.D. (1979). Nonlinear spatial summation and the contrast gain control of cat retinal ganglion cells. Journal of Physiology 290, 141–161.Google Scholar
Shapley, R.M. & Victor, J.D. (1981). How the contrast gain control modifies the frequency responses of cat retinal ganglion cells. Journal of Physiology 318, 161–179.Google Scholar
Shields, C.R. & Lukasiewicz, P.D. (2003). Spike-Dependent GABA Inputs to Bipolar Cell Axon Terminals Contribute to Lateral Inhibition of Retinal Ganglion Cells. Journal of Neurophysiology 89, 2449–2458.Google Scholar
Smith, R.G. (1995). Simulation of an anatomically defined local circuit: The cone-horizontal cell network in cat retina. Visual Neuroscience 12, 545–561.Google Scholar
Solessio, E., Vigh, J., Cuenca, N., Rapp, K., & Lasater, E.M. (2002). Membrane properties of an unusual intrinsically oscillating, wide-field teleost retinal amacrine cell. Journal of Physiology 544, 831–847.Google Scholar
Solomon, S.G., Martin, P.R., White, A.J., Ruttiger, L., & Lee, B.B. (2002). Modulation sensitivity of ganglion cells in peripheral retina of macaque. Vision Research 42, 2893–2898.Google Scholar
Spekreijse, H., van Norren, D., & van den Berg, T.J. (1971). Flicker responses in monkey lateral geniculate nucleus and human perception of flicker. Proceedings of the National Academy of Science USA 68, 2802–2805.Google Scholar
Swanson, W.H., Ueno, T., Smith, V.C., & Pokorny, J. (1987). Temporal modulation sensitivity and pulse-detection thresholds for chromatic and luminance perturbations. Journal of the Optical Society of America A 4, 1992–2005.Google Scholar
Troy, J.B., Schweitzer-Tong, D.E., & Enroth-Cugell, C. (1995). Receptive-field properties of Q retinal ganglion cells of the cat. Visual Neuroscience 12, 285–300.Google 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. (1999). Specificity and strength of retinogeniculate connections. Journal of Neurophysiology 82, 3527–3540.Google Scholar
Vaney, D.I. (1991). Many diverse types of retinal neurons show tracer coupling when injected with biocytin or Neurobiotin. Neuroscience Letters 125, 187–190.Google Scholar
Vaney, D.I. (1994). Patterns of neuronal coupling in the retina. Progress in Retinal and Eye Research 13, 301–355.Google Scholar
Victor, J.D. & Shapley, R.M. (1979). Receptive field mechanisms of cat X and Y retinal ganglion cells. Journal of General Physiology 74, 275–98.Google Scholar
Vigh, J., Solessio, E., Morgans, C.W., & Lasater, E.M. (2003). Ionic Mechanisms Mediating Oscillatory Membrane Potentials in Wide-field Retinal Amacrine Cells. Journal of Neurophysiology 90, 431–443.Google Scholar
Wachtmeister, L. (1998). Oscillatory potentials in the retina: What do they reveal. Progress in Retinal and Eye Research 17, 485–521.Google Scholar
Wachtmeister, L. & Dowling, J.E. (1978). The oscillatory potentials of the mudpuppy retina. Investigations in Ophthalmological and Visual Science 17, 1176–1188.Google Scholar