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

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.

[1]  J. Dowling,et al.  Zebrafish ultraviolet visual pigment: absorption spectrum, sequence, and localization. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[2]  W. B. Marks,et al.  Visual Pigments of Single Primate Cones , 1964, Science.

[3]  Stuart Anstis,et al.  The contribution of color to motion in normal and color-deficient observers , 1991, Vision Research.

[4]  T. G. Wheeler Retinal ON and OFF responses convey different chromatic information to the CNS , 1979, Brain Research.

[5]  R. Marc,et al.  Chromatic organization of primate cones. , 1977, Science.

[6]  Akira Muto,et al.  Behavioral screening assays in zebrafish. , 2004, Methods in cell biology.

[7]  Karl R. Gegenfurtner,et al.  Contrast dependence of colour and luminance motion mechanisms in human vision , 1994, Nature.

[8]  D. Hubel,et al.  Segregation of form, color, movement, and depth: anatomy, physiology, and perception. , 1988, Science.

[9]  C. Neumeyer,et al.  Wavelength dependence of the optomotor response in zebrafish (Danio rerio) , 2003, Vision Research.

[10]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[11]  H. Maaswinkel,et al.  Spatio-temporal frequency characteristics of the optomotor response in zebrafish , 2003, Vision Research.

[12]  Christa Neumeyer,et al.  Motion detection in goldfish investigated with the optomotor response is “color blind” , 1996, Vision Research.

[13]  Brian A Wandell,et al.  Color Signals in Human Motion-Selective Cortex , 1999, Neuron.

[14]  Brian A Wandell,et al.  Perceived Speed of Colored Stimuli , 1999, Neuron.

[15]  E. Seidemann,et al.  Color Signals in Area MT of the Macaque Monkey , 1999, Neuron.

[16]  J. Dowling,et al.  Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. , 1969, Journal of neurophysiology.

[17]  Marco Bertamini,et al.  The chromatic input to global motion perception , 2003, Visual Neuroscience.

[18]  I Rock,et al.  The Optomotor Response and Induced Motion of the Self , 1986, Perception.

[19]  S. Yokoyama,et al.  The molecular genetics and evolution of red and green color vision in vertebrates. , 2001, Genetics.

[20]  A. T. Smith,et al.  Transparent motion from feature- and luminance-based processes , 1993, Vision Research.

[21]  S. Saszik,et al.  ERG assessment of zebrafish retinal development , 1999, Visual Neuroscience.

[22]  V. S. RAMACHANDRAN,et al.  Does colour provide an input to human motion perception? , 1978, Nature.

[23]  N. Daw,et al.  Goldfish Retina: Organization for Simultaneous Color Contrast , 1967, Science.

[24]  Luis A. Lesmes,et al.  The mechanism of isoluminant chromatic motion perception. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[25]  D. Baylor,et al.  How photons start vision. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[26]  G. Streisinger,et al.  Larval and adult visual pigments of the zebrafish, Brachydanio rerio , 1985, Vision Research.

[27]  J. Nathans,et al.  Molecular genetics of human color vision: the genes encoding blue, green, and red pigments. , 1986, Science.

[28]  Matthew C Smear,et al.  Perception of Fourier and non-Fourier motion by larval zebrafish , 2000, Nature Neuroscience.

[29]  S. Zeki,et al.  Colour coding in the superior temporal sulcus of rhesus monkey visual cortex , 1977, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[30]  T. Branchek The development of photoreceptors in the zebrafish, Brachydanio rerio. II. Function , 1984, The Journal of comparative neurology.

[31]  Franck Pichaud,et al.  Evolution of color vision , 1999, Current Opinion in Neurobiology.

[32]  W. Patterson,et al.  Cone contributions to the photopic spectral sensitivity of the zebrafish ERG , 1998, Visual Neuroscience.

[33]  Herwig Baier,et al.  Of lasers, mutants, and see-through brains: functional neuroanatomy in zebrafish. , 2004, Journal of neurobiology.

[34]  Walter Kaiser The spectral sensitivity of the honeybee's optomotor walking response , 2004, Journal of comparative physiology.

[35]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[36]  S. Easter,et al.  Development of the retinofugal projections in the embryonic and larval zebrafish (Brachydanio rerio) , 1994, The Journal of comparative neurology.

[37]  T. Branchek,et al.  The development of photoreceptors in the zebrafish, Brachydanio rerio. I. Structure , 1984, The Journal of comparative neurology.

[38]  J. Dowling,et al.  Temporal and spatial patterns of opsin gene expression in zebrafish (Danio rerio) , 1995, Visual Neuroscience.

[39]  Brian A. Wandell,et al.  Functional segregation of color and motion perception examined in motion nulling , 1993, Vision Research.