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Retinal bipolar cells: Contrast encoding for sinusoidal modulation and steps of luminance contrast

Published online by Cambridge University Press:  25 February 2005

DWIGHT A. BURKHARDT ,
PATRICK K. FAHEY  and
MICHAEL A. SIKORA
DWIGHT A. BURKHARDT
Affiliation:
Departments of Psychology and Graduate Program of Neuroscience, University of Minnesota, Minneapolis
PATRICK K. FAHEY
Affiliation:
Departments of Psychology and Graduate Program of Neuroscience, University of Minnesota, Minneapolis
MICHAEL A. SIKORA
Affiliation:
Departments of Psychology and Graduate Program of Neuroscience, University of Minnesota, Minneapolis
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Abstract

Contrast encoding for sinusoidal modulations of luminance contrast was investigated by intracellular recording in the intact salamander retina. In what appears to be the first study of this kind for vertebrate bipolar cells, responses of the central receptive-field mechanism of cone-driven cells to modulation of 3 Hz were analyzed quantitatively via both signal averaging and a Fast Fourier Transform (FFT) while the retina was light adapted to 20 cd/m2. Depolarizing and hyperpolarizing bipolar cells showed very similar encoding. Both responded with sinusoidal waveforms whose amplitude varied linearly with modulation depths ranging up to 7–8%. The slope of the modulation/response curve was very steep in this range. Thus, the contrast gain was high, reaching values of 6–7, and the half-maximal response was achieved at modulations of 9% or less. At modulations above ∼15%, the responses typically showed strong compressive nonlinearity and the waveform was increasingly distorted. At maximum modulation, the higher harmonics of the FFT constituted about 30% of the amplitude of the fundamental. Measurements were also made for cones and horizontal cells. Both cell types showed predominantly linear responses and low contrast gain, in marked contrast to bipolar cells. These results suggest that the high contrast gain and strong nonlinearity of bipolar cells largely arise postsynaptic to cone transmitter release. Further experiments were performed to compare responses to contrast steps versus those to sinusoidal modulation. In the linear range, we show that the contrast gains of cones and horizontal cells are low and virtually identical for both steps and sinusoidal modulations. In bipolar cells, on the other hand, the contrast gain is about two times greater for steps than that for the 3-Hz sine waves. These results suggest that mechanisms intrinsic to bipolar cells act like a high-pass filter with a short time constant to selectively emphasize contrast transients over slower changes in contrast.

Keywords

Retinal bipolar cellsContrast encodingConesHorizontal cellsRetinaTiger salamander
Type
Research Article
Information
Visual Neuroscience , Volume 21 , Issue 6 , November 2004 , pp. 883 - 893
Copyright
© 2004 Cambridge University Press

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References

REFERENCES

Armstrong-Gold, C.E. & Rieke, F. (2003). Bandpass filtering at the rod to second-order cell synapse in salamander (Ambystoma tigrinum) retina. Journal of Neuroscience 23, 3796–3806.Google Scholar
Awatramani, G. & Slaughter, M.M. (2000). Origin of transient and sustained responses responses in ganglion cells of the retina. Journal of Neuroscience 15, 7087–7095.Google Scholar
Baccus, S.A. & Meister, M. (2002). Fast and slow contrast adaptation in retinal circuitry. Neuron 36, 909–919.Google Scholar
Burkhardt, D.A. & Fahey, P.K. (1998). Contrast enhancement and distributed encoding by bipolar cells in the retina. Journal of Neurophysiology 80, 1070–1081.Google Scholar
Burkhardt, D.A., Fahey, P.K., & Sikora, M. (1998). Responses of ganglion cells to contrast steps in the light-adapted retina of the tiger salamander. Visual Neuroscience 15, 219–229.Google Scholar
Capovilla, M., Hare, W.A., & Owen, W.G. (1987). Voltage gain of signal transfer from retinal rods to bipolar cells in the tiger salamander retina. Journal of Physiology 391, 125–140.Google Scholar
Chichilnisky, E.J. & Kalmar, R.S. (2002). Functional symmetries in ON and OFF ganglion cells of primate retina. Journal of Neuroscience 22, 2737–2747.Google Scholar
Copenhagen, D.R. (2004). Excitation in the retina: The flow, filtering, and molecules of visual signaling in the glutamatergic pathways from photoreceptors to ganglion cells. In The Visual Neurosciences, Vol. 1, ed. Chalupa, L.M. & Werner, J.S., pp. 320–333. Cambridge, Massachusetts: MIT Press.
DeVries, S.H. (2000). Bipolar cells use kainate and AMPA receptors to filter visual information. Neuron 28, 847–856.Google Scholar
Dong, C.J. & Werblin, F.S. (1998). Temporal contrast enhancement via GABAC feedback at bipolar terminals in the tiger salamander retina. Journal of Neurophysiology 79, 2171–2180.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.Google Scholar
Fahey, P.K. & Burkhardt, D.A. (2003). Center-surround organization in bipolar cells: Symmetry for opposing contrasts. Visual Neuroscience 20, 1–10.Google Scholar
Falk, G. (1989). Signal transmission from rods to bipolar and horizontal cells: A synthesis. Progress in Retinal Research 8, 255–279.Google Scholar
Hare, W.A. & Owen, W.G. (1990). Spatial organization of the bipolar cell's receptive field in the retina of the tiger salamander. Journal of Physiology (London) 421, 223–245.Google Scholar
Hare, W.A. & Owen, W.G. (1996). Receptive field of the retinal bipolar cell: A pharmacological study in the tiger salamander. Journal of Neurophysiology 76, 2005–2019.Google Scholar
Laughlin, S.B. (1981). A simple coding procedure enhances a neuron's information capacity. Zeitschrift für Naturforschung 36c, 910–912.Google Scholar
Lee, B.B., Dacey, D.M., Smith, V.C., & Pokorny, J. (2003). Journal of Vision 3, 513–526.
Lukasiewicz, P.D. & Shields, C.R. (1998). Different combinations of GABA A and GABA C receptors confer distinct temporal properties to retinal synaptic receptors. Journal of Neurophysiology 79, 3157–3167.Google Scholar
Naka, K.I. (1977). Functional organization of catfish retina. Journal of Neurophysiology 40, 26–43.Google Scholar
Naka, K.I., Marmarelis, P.Z., & Chan, R.Y. (1975). Functional and morphological identification of catfish retinal neurons. Journal of Neurophysiology 38, 92–131.Google Scholar
Nelson, R. & Kolb, H. (2004). ON and OFF pathways in the vertebrate retina and visual system. In The Visual Neurosciences, Vol. 1, ed. Chalupa, L.M. & Werner, J.S., pp. 260–278. Cambridge, Massachusetts: MIT Press.
Rieke, F. (2001). Temporal contrast adaptation in salamander bipolar cells. The Journal of Neuroscience 21, 9445–9454.Google Scholar
Ruderman, D.L. & Bialek, W. (1994). Statistics of natural images: Scaling in the woods. Physical Review Letters 73, 814–817.Google Scholar
Sakai, H.M. & Naka, K.-I. (1987). Signal transmission in the catfish retina. V. Sensitivity and circuit. Journal of Neurophysiology 58, 1329–1350.Google Scholar
Sakai, H.M. & Naka, K.I. (1988). Neuron network in catfish retina: 1968–1987. In Progress in Retinal Research, Vol. 7, ed. Osborne, N. & Chader, J., pp. 149–208. Oxford: Pergamon.
Sakai, H.M., Wang, J.L., & Naka, K.I. (1995). Contrast gain control in the lower vertebrate retinas. Journal of General Physiology 105, 815–835.Google Scholar
Shapley, R. & Enroth-Cugell, C. (1984). Visual adaptation and retinal gain control. In Progress in Retinal Research, Vol. 3, ed. Osborne, N.N. & Chader, C.T., 263–346. Oxford: Pergamon.
Shiells, R.A. & Falk, G. (1999). A rise in intracellular Ca2+ underlies light adaptation in dogfish retinal ‘on’ bipolar cells. Journal of Physiology 514.2, 343–350.Google Scholar
Shiells, R.A. & Falk, G. (2000). Activation of Ca2+-calmodulin kinase II induces desensitization by background light in dogfish “on” bipolar cells. Journal of Physiology 528.2, 327–338.Google Scholar
Slaughter, M.M. & Awatramani, G.B. (2002). On bipolar cells: Following the footsteps of transduction. Advances in Experimental Medicine and Biology 514, 477–492.Google Scholar
Smith, V.C., Pokorny, J., Lee, B.B., & Dacey, D.M. (2001). Primate horizontal cell dynamics: An analysis of sensitivity regulation in the outer retina. Journal of Neurophysiology 85, 545–558.Google Scholar
Sterling, P. (2004). How retinal circuits optimize the transfer of visual information. In The Visual Neurosciences, Vol. 1, ed. Chalupa, L.M. & Werner, J.S., pp. 234–259. Cambridge, Massachusetts: MIT Press.
Thoreson, W.B. & Burkhardt, D.A. (2003). Contrast encoding in retinal bipolar cells: Current vs. voltage. Visual Neuroscience 20, 19–28.Google Scholar
Vu, T.Q., McCarthy, S.T., & Owen, W.G. (1997). Linear transduction of natural stimuli by dark-adapted and light-adapted rods of the salamander, Ambystoma tigrinum. Journal of Physiology 505, 193–204.Google Scholar
Werblin, F.S. (1991). Synaptic connections, receptive fields, and patterns of activity in the tiger salamander retina. Investigative Ophthalmology 32, 459–483.Google Scholar
Wu, S.M. (1990). Signal transmission and adaptation-induced modulation of photoreceptor synapses in the retina. Progress in Retinal Research 9, 27–44.Google Scholar
Wu, S.M. (1994). Synaptic transmission in the outer retina. Annual Review of Physiology 56, 141–168.Google Scholar
Wu, S.M. (2003). Intracelluar light responses and synaptic organization of the vertebrate retina. In Adler's Physiology of the Eye (10th edition), ed. Kaufman, P.K. & Alm, A., pp. 422–438. St. Louis, Missouri: Mosby.
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, 4462–4470.Google Scholar
Yang, X.-L. & Wu, S.M. (1991a). Coexistence and function of glutamate receptor subtypes in the horizontal cells of the tiger salamander retina. Visual Neuroscience 7, 377–382.Google Scholar
Yang, X.L. & Wu, S.M. (1991b). Feedforward lateral inhibition in retinal bipolar cells: input-output relation of the horizontal cell-depolarizing bipolar cell synapse. Proceedings of the National Academy of Sciences of the U.S.A. 88, 3310–3313.Google Scholar
Yang, X.-L. & Wu, S.M. (1996). Response sensitivity and voltage gain of the rod- and cone-horizontal cell synapses in dark- and light-adapted tiger salamander retina. Journal of Neurophysiology 76, 3863–3874.Google Scholar
Yu, W. & Miller, R.F. (1996). The mechanism by which NBQX enhances NMDA currents in retinal ganglion cells. Brain Research 709, 184–196.Google Scholar