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Zebrafish inner retina: Local signals for spatial position, luminance, and color contrast

Published online by Cambridge University Press:  09 August 2012

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

The retina of the zebrafish (Danio rerio) provides an unusually favorable preparation for genetic and developmental studies of the retina. Although the retina has been studied extensively for two decades, the neuronal response of the inner retina is largely unknown. This report describes a prominent local field potential of the inner retina, the Proximal Negative Response (PNR). It is best evoked by small (100 μm) precisely positioned spots of light and is exceedingly sensitive to negative luminance contrast. The polarity, waveform, and other properties of the PNR suggest that it arises primarily from ON-OFF neurons of the proximal retina. The dominant response to negative contrast and its enhancement by light adaptation is believed due to a dominant presynaptic input from OFF bipolar cells. Color contrast was investigated by analyzing responses to a green bar moving on green versus red backgrounds. Over an intermediate range of irradiance, the response to green on red was larger than the response to green on green, thereby providing evidence for the encoding of color contrast. The present findings complement the classic principle of color contrast for human vision known as Kirschmann’s third law and bring to mind the view of Walls that color contrast may have been the driving force for the evolution of color vision in lower vertebrates. In sum, the PNR of zebrafish provides clear evidence for the encoding of color and luminance contrast in the inner retina. It exhibits the defining properties common to many other vertebrates, reinforcing the view that the zebrafish may further serve as a model for retinal function and that the PNR may provide a new approach for studies of development, genetics, and retinal degeneration in zebrafish.

Keywords

Zebrafish retinaProximal negative responseColor contrastLuminance contrast
Type
Research Articles
Information
Visual Neuroscience , Volume 29 , Issue 4-5 , September 2012 , pp. 229 - 236
Copyright
Copyright © Cambridge University Press 2012

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References

Alpern, M. (1964). Relation between brightness and color contrast. Journal of the Optical Society of America 54, 1491–1492.CrossRefGoogle Scholar
Berliner, A. (1949). Lectures in Visual Psychology. Chicago, IL: Professional Press.Google Scholar
Boring, E.G. (1942). Sensation and Perception in the History of Experimental Psychology. New York: Appelton-Century.Google Scholar
Burkhardt, D.A. (1970). Proximal negative response of frog retina. Journal of Neurophysiology 33, 405–420.CrossRefGoogle ScholarPubMed
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. (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
Burkhardt, D.A. & Mooney, R. (1977). Electrical responses in the inner retina of teleosts and reptiles. Vision Research 17, 154–156.CrossRefGoogle ScholarPubMed
Burkhardt, D.A. & Whittle, P. (1973). Intensity coding in the frog retina. The Journal of General Physiology 61, 305–322.CrossRefGoogle ScholarPubMed
Connaughton, V.P. (2011). Bipolar cells in the zebrafish retina. Visual Neuroscience 28, 77–93.CrossRefGoogle ScholarPubMed
Connaughton, V.P. & Dowling, J.E. (1997). Comparative morphology of distal neurons in larval and adult zebrafish. Vision Research 38, 13–18.CrossRefGoogle Scholar
Connaughton, V.P., Graham, D. & Nelson, R. (2004). Identification and morphological classification of horizontal, bipolar and amacrine cells within the zebrafish retina. The Journal of Comparative Neurology 477, 371–385.CrossRefGoogle ScholarPubMed
Connaughton, V.P. & Nelson, R. (2010). Spectral responses in zebrafish horizontal cells include a tetraphasic response and a novel UV-dominated response. Journal of Neurophysiology 104, 2407–2422.CrossRefGoogle Scholar
Dowling, J.E. (1987). The Retina: An Approachable Part of the Brain. Cambridge, MA: Belknap Press.Google Scholar
Emran, F., Rihel, J., Adolph, A.R., Woong, K.Y., Kraves, S. & Dowling, J.E. (2007). OFF ganglion cells cannot drive the optokinetic reflex in zebrafish. Proceedings of the National Academy of Sciences of the United States of America 104, 19126–19131.CrossRefGoogle ScholarPubMed
Fadool, J.M. & Dowling, J.E. (2008). Zebrafish: A model system for the study of eye genetics. Progress in Retinal and Eye Research 27, 89–110.CrossRefGoogle 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 ScholarPubMed
Gordon, J. & Shapley, R. (2006). Brightness contrast inhibits color induction: Evidence for a new kind of color theory. Spatial Vision 19, 133–146.Google ScholarPubMed
Grimes, W.N. (2012). Amacrine cell-mediated input to bipolar cells: Variations on a common mechanistic theme. Visual Neuroscience 29, 41–49.CrossRefGoogle ScholarPubMed
Gustafson, E.C., Stevens, E.R., Wolosker, H. & Miller, R.F. (2006). Endogenous D-serine contributes to NMDA-receptor-mediated light-evoked responses in the vertebrate retina. Journal of Neurophysiology 98, 122–130.CrossRefGoogle Scholar
Holden, A.L. (1972). Proximal negative response in pigeon retina. The Journal of Physiology 221, 173–188.CrossRefGoogle ScholarPubMed
Hughes, A., Saszik, S., Bilotta, J., Demarco, P.L. & Patterson, W.F. (1998). Cone contributions to the photopic spectral sensitivity of the zebrafish ERG. Visual Neuroscience 15, 1029–1037.CrossRefGoogle Scholar
Kirschmann, A. (1891). Uber die quantitativen Verhaltnisse des simultanen Helligkeits- und Farben-Contrastes. Philosophical Studies 6, 417–491.Google Scholar
Legge, G.E., Parish, D.H., Luebker, A. & Wurm, L. (1990). Psychophysics of reading. XI. Comparing color contrast and luminance contrast. Journal of the Optical Society of America A 7, 2002–2010.CrossRefGoogle ScholarPubMed
Li, L. & Dowling, J.E. (1997). A dominant form of inherited retinal degeneration caused by a non-photoreceptor cell-specific mutation. Proceedings of the National Academy of Sciences of the United States of America 94, 11645–11650.CrossRefGoogle ScholarPubMed
Li, L. & Dowling, J.E. (2000). Effects of dopamine depletion on visual sensitivity of zebrafish. The Journal of Neuroscience 20, 1893–1903.CrossRefGoogle ScholarPubMed
Mangrum, W.I., Dowling, J.E. & Cohen, E.D. (2002). A morphological classification of ganglion cells in the zebrafish retina. Visual Neuroscience 19, 767–779.CrossRefGoogle ScholarPubMed
Miller, R.F. (1979). The neuronal basis of ganglion cell receptive field organization and the physiology of amacrine cells. In The Neuroscience Fourth Study Section, ed. Schmidt, F.O. & Worden, F.G., pp. 227–245. Cambridge, MA: MIT Press.Google Scholar
Miller, R.F. (2008). Cell communication mechanisms in the vertebrate retina. Investigative Ophthalmology and Visual Science 49, 5184–5198.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
Nelson, R.F. & Singla, N. (2009). A spectral model for signal elements isolated from zebrafish photopic electroretinogram. Visual Neuroscience 26, 349–363.CrossRefGoogle ScholarPubMed
Ogden, T.E. (1973). Proximal negative response of the primate retina. Vision Research 13, 797–808.CrossRefGoogle ScholarPubMed
Patterson, W.P., McDowell, A.L., Hughes, A. & Bilotta, J. (2002). Opponent and nonopponent contributions to the zebrafish electroretinogram using heterochromatic flicker photometry. Journal of Comparative Physiology A Neuroethology, Sensory, Neural, and Behavioral Physiology 188, 283–293.CrossRefGoogle Scholar
Randlett, O., Norden, C. & Harris, W.A. (2011). The vertebrate retina: A model for neuronal polarization in vivo. Developmental Neurobiology 71, 567–583.CrossRefGoogle Scholar
Robinson, J., Schmitt, E.A., Harosi, F., Reece, R.J. & Dowling, J.E. (1993). Zebrafish ultraviolet visual pigment: Absorption spectrum, sequence, and localization. Proceedings of the National Academy of Sciences of the United States of America 90, 6009–6012.CrossRefGoogle ScholarPubMed
Saszik, S., Alexander, A.L., Lawrence, T. & Bilotta, J. (2002). APB differentially affects the cone contributions to the zebrafish ERG. Visual Neuroscience 19, 521–529.CrossRefGoogle Scholar
Schmitt, E.A. & Dowling, J.E. (1999). Early retinal development in the zebrafish, Danio rerio: Light and electron microscopic analyses. The Journal of Comparative Neurology 404, 515–536.3.0.CO;2-A>CrossRefGoogle ScholarPubMed
Walls, G.L. (1963). The Vertebrate Eye and its Adaptive Radiation. New York: Hafner.Google Scholar
Wong, K.Y., Gray, J., Hayward, C.J.C., Adolph, A.R. & Dowling, J.E. (2004). Glutaminergic mechanisms in the outer retina of larval zebrafish: Analysis of electroretinogram b- and d-waves using a novel preparation. Zebrafish 1, 121–131.CrossRefGoogle 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
Zhang, A.-J. & Wu, S.M. (2010). Responses and receptive fields of amacrine and ganglion cells in the tiger salamander retina. Vision Research 50, 614–622.CrossRefGoogle Scholar