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Contrast processing by ON and OFF bipolar cells

Published online by Cambridge University Press:  19 November 2010

DWIGHT A. BURKHARDT
DWIGHT A. BURKHARDT*
Affiliation:
Department of Psychology, University of Minnesota, Minneapolis, Minnesota Graduate Program in Neuroscience, University of Minnesota, Minneapolis, Minnesota
*
*Address correspondence and reprint requests to: Dwight A. Burkhardt, University of Minnesota, n218 Elliott Hall, 75 E. River Road, Minneapolis, MN 55455. E-mail: burkh001@umn.edu
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Abstract

Much of what is currently known about the visual response of retinal bipolar cells is based on studies of rod-dominant responses to flashes in the dark in the isolated retina. This minireview summarizes quantitative findings on contrast processing in the intact light-adapted retina based on intracellular recording from more than 400 cone-driven bipolar cells in the tiger salamander: 1) In the main, the contrast responses of ON and OFF cells are surprisingly similar, suggesting a need to refine the view that ON and OFF cells provide the selective substrates for processing of positive and negative contrasts, respectively. 2) Overall, the response is quite nonlinear, showing very high gain for small contrasts, some 10–15 times greater than that of cones, but then quickly approaches saturation for higher contrasts. 3) Under optimal conditions of light adaptation, both classes of bipolar cells show evidence for efficient coding with respect to the contrasts in natural images. 4) There is a marked diversity within both the ON and OFF bipolar cell populations and an absence of discrete subtypes. The dynamic ranges bracket the range of contrasts in nature. 5) For both ON and OFF cells, the receptive field organization shows a striking symmetry between center and surround for responses of the same polarity and thus opposite contrast polarities. 6) The latency difference between ON and OFF cells is about 30 ms, which seems qualitatively consistent with a delay due to the G-protein cascade in ON bipolar cells. 7) In sum, we report quantitative evidence for at least 11 transformations in signal processing that occur between the voltage response of cones and the voltage response of bipolar cells.

Keywords

Retinal bipolar cellsContrast encodingConesHorizontal cellsRetinaTiger salamander

Information

Type
Review Article
Information
Visual Neuroscience , Volume 28 , Issue 1 , January 2011 , pp. 69 - 75
Copyright
Copyright © Cambridge University Press 2010

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References

Armstrong-Gold, C.E. & Rieke, F. (2003). Bandpass filtering at the rod to second-order cell synapse in salamander (Ambystoma tigrinum) retina. The Journal of Neuroscience 23, 3796–3806.CrossRefGoogle Scholar
Burkhardt, D.A. (1994). Light adaptation and photopigment bleaching in cone photoreceptors in situ in the retina of the turtle. The Journal of Neuroscience 14, 1091–1105.CrossRefGoogle ScholarPubMed
Burkhardt, D.A. & Fahey, P.K. (1998). Contrast enhancement and distributed encoding by bipolar cells in the retina. Journal of Neurophysiology 80, 1070–1081.CrossRefGoogle ScholarPubMed
Burkhardt, D.A. & Fahey, P.K. (1999). Contrast rectification and distributed encoding by ON-OFF amacrine cells in the retina. Journal of Neurophysiology 81, 1676–1688.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Burkhardt, D.A., Fahey, P.K. & Sikora, M.A. (2004). Retinal bipolar cells: Contrast encoding for sinusoidal modulation and steps of luminance contrast. Visual Neuroscience 21, 883–893.CrossRefGoogle ScholarPubMed
Burkhardt, D.A., Fahey, P.K. & Sikora, M.A. (2006). Natural images and contrast encoding in bipolar cells in the retina of the land- and aquatic-phase tiger salamander. Visual Neuroscience 23, 35–47.CrossRefGoogle ScholarPubMed
Burkhardt, D.A., Fahey, P.K. & Sikora, M.A. (2007). Retinal bipolar cells: Temporal filtering of signals from cone photoreceptors. Visual Neuroscience 24, 765–774.CrossRefGoogle ScholarPubMed
Cadetti, L. & Thoreson, W.B. (2006). Feedback effects of horizontal cell membrane potential on cone calcium currents studied with simultaneous recordings. Journal of Neurophysiology 95, 1992–1995.CrossRefGoogle ScholarPubMed
Connaughton, V.P., Graham, D. & Nelson, R. (2004). Identification and morphological classification of horizontal, bipolar, and amacrine cells within the zebrafish retina using the DiOlistic technique. The Journal of Comparative Neurology 477, 371–385.CrossRefGoogle 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. Cambrdige, MA: MIT Press.Google Scholar
Copenhagen, D.R., Ashmore, J.F. & Schnapf, J.K. (1983). Kinetics of synaptic transmission from photoreceptors to horizontal and bipolar cells in turtle retina. Vision Research 23, 363–369.CrossRefGoogle ScholarPubMed
Dacey, D., Packer, O.S., Diller, L., Brainard, D., Peterson, B. & Lee, B. (2000). Center surround receptive field structure of cone bipolar cells in primate retina. Vision Research 40, 1801–1811.CrossRefGoogle ScholarPubMed
DeVries, S.H. (2000). Bipolar cells use kainate and AMPA receptors to filter visual information. Neuron 28, 847–856.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
Fahey, P.K. & Burkhardt, D.A. (2003). Center-surround organization in bipolar cells: Symmetry for opposing contrasts. Visual Neuroscience 20, 1–10.CrossRefGoogle ScholarPubMed
Frumkes, T.E. & Miller, R.F. (1978). Pathways and polarities of synaptic interaction in the inner retina of the mudpuppy. II. Insights revealed by analysis of latency and threshold. Brain Research 161, 13–24.CrossRefGoogle Scholar
Gollisch, T. & Meister, M. (2010). Eye smarter than scientists believed: Neural computations in circuits of the retina. Neuron 65, 150–164.CrossRefGoogle ScholarPubMed
Grant, G.B. & Dowling, J.E. (1996). ON bipolar cell responses in the teleost retina are generated by two distinct mechanisms. Journal of Neurophysiology 76, 3842–3849.CrossRefGoogle ScholarPubMed
Hare, W.A. & Owen, W.G. (1990). Spatial organization of the bipolar cell’s receptive field in the retina of the tiger salamander. The Journal of Physiology (London) 421, 223–245.CrossRefGoogle ScholarPubMed
Hare, W.A. & Owen, W.G. (1992). Effects of 2-amino-4-phosphonobutyric acid on cells in the distal layers of the tiger salamander’s retina. The Journal of Physiology 445, 741–757.CrossRefGoogle ScholarPubMed
Jackman, S.L., Choi, S.-Y., Thoreson, W.B., Rabl, K., Bartoletti, T.M. & Kramer, R.H. (2009). Role of the synaptic ribbon in transmitting the cone light response. Nature Neuroscience 12, 303–310.CrossRefGoogle ScholarPubMed
Koike, C., Obara, T., Uriu, Y., Numata, T., Sanuki, R., Miyata, K., Koyasu, T., Ueno, S., Tani, A., Ueda, H., Kondo, M., Mori, Y., Tachibana, M. & Furkawa, T. (2010). TRMP1 is a component of the retinal ON bipolar transduction channel in the mGluR6 cascade. Proceedings of the National Academy of Sciences of the United States of America 107, 332–337.CrossRefGoogle Scholar
Kuffler, S.W. (1953). Discharge patterns and functional organization of mammalian retina. Journal of Neurophysiology 16, 37–68.CrossRefGoogle ScholarPubMed
Laughlin, S.B. (1987). Form and function in retinal processing. Trends in Neuroscience 10, 478–483.CrossRefGoogle Scholar
Li, W. & DeVries, S.H. (2006). Bipolar cell pathways for color and luminance vision in a dichromatic mammalian retina. Nature Neuroscience 9, 669–675.CrossRefGoogle Scholar
Masland, R.H. (2001). The fundamental plan of the retina. Nature Neuroscience 4, 877–886.CrossRefGoogle ScholarPubMed
Miller, R.F. (2008). Cell communication mechanisms in the vertebrate retina. Investigative Ophthalmology and Visual Science 49, 5184–5198.CrossRefGoogle ScholarPubMed
Nawy, S. (2000). Regulation of the on bipolar cell mGluR6 pathway by Ca2+. The Journal of Neuroscience 20, 4471–4479.CrossRefGoogle ScholarPubMed
Nelson, R. (1973). A comparison of electrical properties of neurons in Necturus retina. Journal of Neurophysiology 36, 519–535.CrossRefGoogle ScholarPubMed
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, MA: MIT Press.Google Scholar
Packer, S., Verweij, J., Li, P., Schnapf, J.L. & Dacey, D.M. (2010). Blue-yellow opponency in primate S cone photoreceptors. The Journal of Neuroscience 30, 568–572.CrossRefGoogle ScholarPubMed
Rabl, K., Cadetti, L. & Thoreson, W.B. (2006). Paired-pulse depression of photoreceptor synapses. The Journal of Neuroscience 26, 2555–2563.CrossRefGoogle ScholarPubMed
Rieke, F. (2001). Temporal contrast adaptation in salamander bipolar cells. The Journal of Neuroscience 21, 9445–9454.CrossRefGoogle ScholarPubMed
Slaughter, M.M. & Miller, R.F. (1981). 2-Amino-4-phosphonobutyric acid: A new pharmacological tool for retina research. Science 211, 182–185.CrossRefGoogle ScholarPubMed
Snellman, J., Kaur, T., Shen, Y. & Nawy, S. (2008). Regulation of ON bipolar activity. Progress in Retinal and Eye Research 27, 450–463.CrossRefGoogle 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, MA: MIT Press.Google Scholar
Thoreson, W.B. (2007). Kinetics of synaptic transmission at ribbon synapses of rods and cones. Molecular Neurobiology 36, 205–223.CrossRefGoogle ScholarPubMed
Thoreson, W.B., Babai, R. & Bartoletti, T.M. (2008). Feedback from horizontal cells to rod photoreceptors in vertebrate retina. The Journal of Neuroscience 28, 5691–5695.CrossRefGoogle ScholarPubMed
Thoreson, W.B. & Burkhardt, D.A. (2003). Contrast encoding in retinal bipolar cells: Current vs. voltage. Visual Neuroscience 20, 19–28.CrossRefGoogle ScholarPubMed
Thoreson, W.B. & Miller, R.F. (1993). Membrane currents evoked by excitatory amino acid agonists in ON bipolar cells of the mudpuppy retina. Journal of Neurophysiology 70, 1326–1338.CrossRefGoogle Scholar
Thoreson, W.B. & Witkovsky, P. (1999). Glutamate receptors and circuits in the vertebrate retina. Progress in Retinal and Eye Research 18, 765–810.CrossRefGoogle ScholarPubMed
Toyoda, J. & Shimbo, K. (1999). Color processing in lower vertebrates. In The Retinal Basis of Vision, ed. Toyoda, J., Murakami, M., Kaneko, A. & Saito, T., pp. 199–213. Amsterdam, The Netherlands: Elsevier Science.Google Scholar
Wassle, H. (2004). Parallel processing in the mammalian retina. Nature Reviews. Neuroscience 5, 747–757.CrossRefGoogle ScholarPubMed
Wassle, H., Puller, P., Muller, F., & Haverkamp, S. (2009). Cone contacts, mosaics, and territories of bipolar cells in the mouse retina. The Journal of Neuroscience 29, 106–117.CrossRefGoogle ScholarPubMed
Werblin, F.S. & Dowling, J.E. (1968). Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. Journal of Neurophysiology 32, 339–355.CrossRefGoogle Scholar
Witkovsky, P. & Stone, S. (1987). Center-surround organization of Xenopus horizontal cells and its modification by gamma-aminobutyric acid and strontium. Experimental Biology 1, 1–12.Google Scholar
Wu, S.M. (2010). Synaptic organization of the vertebrate retina: General principles and species-specific variations. Investigative Ophthalmology and Visual Science 51, 1264–1274.CrossRefGoogle ScholarPubMed
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. The Journal of Neuroscience 20, 4462–4470.CrossRefGoogle ScholarPubMed
Wunk, D.F. & Werblin, F.S. (1979). Synaptic inputs to ganglion cells in the tiger salamander retina. The Journal of General Physiology 73, 265–286.CrossRefGoogle ScholarPubMed
Zhang, A.J. & Wu, S.M. (2009). Receptive fields of retinal bipolar cells are mediated by heterogeneous synaptic activity. The Journal of Neuroscience 29, 787–797.Google Scholar
Zhang, J. & Wu, S.M. (2003). Goa labels ON bipolar cells in the tiger salamander retina. The Journal of Comparative Neurology 461, 276–289.CrossRefGoogle Scholar