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Channeling of red and green cone inputs to the zebrafish optomotor response

Published online by Cambridge University Press:  02 August 2005

MICHAEL B. ORGER  and
HERWIG BAIER
MICHAEL B. ORGER
Affiliation:
Department of Physiology, Program in Neuroscience, University of California—San Francisco, San Francisco
HERWIG BAIER
Affiliation:
Department of Physiology, Program in Neuroscience, University of California—San Francisco, San Francisco
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Abstract

Visual systems break scenes down into individual features, processed in distinct channels, and then selectively recombine those features according to the demands of particular behavioral tasks. In primates, for example, there are distinct pathways for motion and form processing. While form vision utilizes color information, motion pathways receive input from only a subset of cone photoreceptors and are generally colorblind. To explore the link between early channeling of visual information and behavioral output across vertebrate species, we measured the chromatic inputs to the optomotor response of larval zebrafish. Using cone-isolating gratings, we found that there is a strong input from both red and green cones but not short-wavelength cones, which nevertheless do contribute to another behavior, phototaxis. Using a motion-nulling method, we measured precisely the input strength of gratings that stimulated cones in combination. The fish do not respond to gratings that stimulate different cone types out of phase, but have an enhanced response when the cones are stimulated together. This shows that red and green cone signals are pooled at a stage before motion detection. Since the two cone inputs are combined into a single ‘luminance’ channel, the response to sinusoidal gratings is colorblind. However, we also find that the relative contributions of the two cones at isoluminance varies with spatial frequency. Therefore, natural stimuli, which contain a mixture of spatial frequencies, are likely to be visible regardless of their chromatic composition.

Keywords

Cone photoreceptorMotion visionPsychopysicsZebrafish
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 3 , May 2005 , pp. 275 - 281
Copyright
2005 Cambridge University Press

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References

REFERENCES

Baylor, D. (1996). How photons start vision. Proceedings of the National Academy of Sciences of the U.S.A. 93, 560–565.CrossRefGoogle Scholar
Brainard, D.H. (1997). The Psychophysics Toolbox. Spatial Vision 10, 433–436.CrossRefGoogle Scholar
Branchek, T. (1984). The development of photoreceptors in the zebrafish, brachydanio rerio. II. Function. Journal of Comparative Neurology 224, 116–122.Google Scholar
Branchek, T. & Bremiller, R. (1984). The development of photoreceptors in the zebrafish, Brachydanio rerio. I. Structure. Journal of Comparative Neurology 224, 107–115.Google Scholar
Burrill, J.D. & Easter, S.S., Jr. (1994). Development of the retinofugal projections in the embryonic and larval zebrafish (Brachydanio rerio). Journal of Comparative Neurology 346, 583–600.CrossRefGoogle Scholar
Cavanagh, P. & Anstis, S. (1991). The contribution of color to motion in normal and color-deficient observers. Vision Research 31, 2109–2148.CrossRefGoogle Scholar
Chichilnisky, E.J., Heeger, D., & Wandell, B.A. (1993). Functional segregation of color and motion perception examined in motion nulling. Vision Research 33, 2113–2125.CrossRefGoogle Scholar
Daw, N.W. (1967). Goldfish retina: Organization for simultaneous color contrast. Science 158, 942–944.CrossRefGoogle Scholar
Dougherty, R.F., Press, W.A., & Wandell, B.A. (1999). Perceived speed of colored stimuli. Neuron 24, 893–899.CrossRefGoogle Scholar
Gahtan, E. & Baier, H. (2004). Of lasers, mutants, and see-through brains: Functional neuroanatomy in zebrafish. Journal of Neurobiology 59, 147–161.CrossRefGoogle Scholar
Hammett, S.T., Ledgeway, T., & Smith, A.T. (1993). Transparent motion from feature- and luminance-based processes. Vision Research 33, 1119–1122.CrossRefGoogle Scholar
Hawken, M.J., Gegenfurtner, K.R., & Tang, C. (1994). Contrast dependence of colour and luminance motion mechanisms in human vision. Nature 367, 268–270.CrossRefGoogle Scholar
Hughes, A., Saszik, S., Bilotta, J., Demarco, P.J., Jr., & Patterson, W.F., II (1998). Cone contributions to the photopic spectral sensitivity of the zebrafish ERG. Visual Neuroscience 15, 1029–1037.CrossRefGoogle Scholar
Kaiser, W. (1974). The spectral sensitivity of the honey bee's optomotor walking response. Journal of Comparative Physiology 90, 405–408.CrossRefGoogle Scholar
Krauss, A. & Neumeyer, C. (2003). Wavelength dependence of the optomotor response in zebrafish (Danio rerio). Vision Research 43, 1273–1282.Google Scholar
Livingstone, M. & Hubel, D. (1988). Segregation of form, color, movement, and depth: Anatomy, physiology, and perception. Science 240, 740–749.CrossRefGoogle Scholar
Lu, Z.L., Lesmes, L.A., & Sperling, G. (1999). The mechanism of isoluminant chromatic motion perception. Proceedings of the National Academy of Sciences of the U.S.A. 96, 8289–8294.CrossRefGoogle Scholar
Maaswinkel, H. & Li, L. (2003). Spatio-temporal frequency characteristics of the optomotor response in zebrafish. Vision Research 43, 21–30.CrossRefGoogle Scholar
Marc, R.E. & Sperling, H.G. (1977). Chromatic organization of primate cones. Science 196, 454–456.CrossRefGoogle Scholar
Marks, W.B., Dobelle, W.H., & Macnichol, E.F., Jr. (1964). Visual pigments of single primate cones. Science 143, 1181–1183.CrossRefGoogle Scholar
Nathans, J., Thomas, D., & Hogness, D.S. (1986). Molecular genetics of human color vision: The genes encoding blue, green, and red pigments. Science 232, 193–202.CrossRefGoogle Scholar
Nawrocki, L., BreMiller, R., Streisinger, G., & Kaplan, M. (1985). Larval and adult visual pigments of the zebrafish, Brachydanio rerio. Vision Research 25, 1569–1576.CrossRefGoogle Scholar
Orger, M.B., Gahtan, E., Muto, A., Page-McCaw, P., Smear, M.C., & Baier, H. (2004). Behavioral screening assays. Methods in Cell Biology 77, 53–68.CrossRefGoogle Scholar
Orger, M.B., Smear, M.C., Anstis, S.M., & Baier, H. (2000). Perception of Fourier and non-Fourier motion by larval zebrafish. Nature Neuroscience 3, 1128–1133.Google Scholar
Pelli, D.G. (1997). The VideoToolbox software for visual psychophysics: transforming numbers into movies. Spatial Vision 10, 437–442.CrossRefGoogle Scholar
Pichaud, F., Briscoe, A., & Desplan, C. (1999). Evolution of color vision. Current Opinion in Neurobiology 9, 622–627.CrossRefGoogle Scholar
Ramachandran, V.S. & Gregory, R.L. (1978). Does colour provide an input to human motion perception? Nature 275, 55–56.Google Scholar
Robinson, J., Schmitt, E.A., & Dowling, J.E. (1995). Temporal and spatial patterns of opsin gene expression in zebrafish (Danio rerio). Visual Neuroscience 12, 895–906.CrossRefGoogle Scholar
Robinson, J., Schmitt, E.A., Harosi, F.I., 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 U.S.A. 90, 6009–6012.CrossRefGoogle Scholar
Rock, I. & Smith, D. (1986). The optomotor response and induced motion of the self. Perception 15, 497–502.CrossRefGoogle Scholar
Ruppertsberg, A.I., Wuerger, S.M., & Bertamini, M. (2003). The chromatic input to global motion perception. Visual Neuroscience 20, 421–428.CrossRefGoogle Scholar
Saszik, S., Bilotta, J., & Givin, C.M. (1999). ERG assessment of zebrafish retinal development. Visual Neuroscience 16, 881–888.CrossRefGoogle Scholar
Schaerer, S. & Neumeyer, C. (1996). Motion detection in goldfish investigated with the optomotor response is “color blind”. Vision Research 36, 4025–4034.CrossRefGoogle Scholar
Seidemann, E., Poirson, A.B., Wandell, B.A., & Newsome, W.T. (1999). Color signals in area MT of the macaque monkey. Neuron 24, 911–917.CrossRefGoogle Scholar
Wandell, B.A., Poirson, A.B., Newsome, W.T., Baseler, H.A., Boynton, G.M., Huk, A., Gandhi, S., & Sharpe, L.T. (1999). Color signals in human motion-selective cortex. Neuron 24, 901–909.CrossRefGoogle Scholar
Werblin, F.S. & Dowling, J.E. (1969). Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. Journal of Neurophysiology 32, 339–355.Google Scholar
Wheeler, T.G. (1979). Retinal ON and OFF responses convey different chromatic information to the CNS. Brain Research 160, 145–149.CrossRefGoogle Scholar
Yokoyama, S. & Radlwimmer, F.B. (2001). The molecular genetics and evolution of red and green color vision in vertebrates. Genetics 158, 1697–1710.Google Scholar
Zeki, S.M. (1977). Colour coding in the superior temporal sulcus of rhesus monkey visual cortex. Proceedings of the Royal Society B (London) 197, 195–223.CrossRefGoogle Scholar