Teleost polarization vision: how it might work and what it might be good for

In this review, we will discuss the recent literature on fish polarization vision and we will present a model on how the retina processes polarization signals. The model is based on a general retinal-processing scheme and will be compared with the available electrophysiological data on polarization processing in the retina. The results of this model will help illustrate the functional significance of polarization vision for both feeding behaviour and navigation. First, we examine the linkage between structure and function in polarization vision in general.

[1]  Thomas W. Cronin,et al.  Behavioural evidence for polarisation vision in stomatopods reveals a potential channel for communication , 1999, Current Biology.

[2]  Craig W. Hawryshyn,et al.  Multidimensional polarization sensitivity in damselfishes , 2003, Journal of Comparative Physiology A.

[3]  K. R. Mckaye,et al.  Discrimination between Horizontally and Vertically Polarized Light by the Cichlid Fish Pseudotropheus macrophthalmus , 1978 .

[4]  A. Kaneko,et al.  Synaptic transmission from photoreceptors to bipolar and horizontal cells in the carp retina. , 1976, Cold Spring Harbor symposia on quantitative biology.

[5]  A. Blest,et al.  Membrane-associated actin in the rhabdomeral microvilli of crayfish photoreceptors , 1984, The Journal of cell biology.

[6]  The physical basis of reflective communication between fish, with special reference to the horse mackerel, Trachurus trachurus , 1997 .

[7]  Iñigo Novales Flamarique,et al.  Visual pigments and dichroism of anchovy cones: A model system for polarization detection. , 2002, Visual Neuroscience.

[8]  Thomas Labhart,et al.  Specialized photoreceptors at the dorsal rim of the honeybee's compound eye: Polarizational and angular sensitivity , 1980, Journal of comparative physiology.

[9]  T. Cronin,et al.  Polarization vision in cuttlefish in a concealed communication channel? , 1996, The Journal of experimental biology.

[10]  R. Wehner.  Polarization vision--a uniform sensory capacity? , 2001, The Journal of experimental biology.

[11]  R. Duvoisin,et al.  TRPM1 is required for the depolarizing light response in retinal ON-bipolar cells , 2009, Proceedings of the National Academy of Sciences.

[12]  Alan Fein,et al.  Photoreceptors, their role in vision , 1982 .

[13]  Craig W. Hawryshyn,et al.  Behavioural discrimination of polarized light in the damselfish Chromis viridis (family Pomacentridae) , 2005, Journal of Experimental Biology.

[14]  D. Varjú,et al.  Polarized Light in Animal Vision: Polarization Patterns in Nature , 2004 .

[15]  Akimichi Kaneko,et al.  pH Changes in the Invaginating Synaptic Cleft Mediate Feedback from Horizontal Cells to Cone Photoreceptors by Modulating Ca2+ Channels , 2003, The Journal of general physiology.

[16]  H Spekreijse,et al.  Spectral sensitivity of the feedback signal from horizontal cells to cones in goldfish retina , 1998, Visual Neuroscience.

[17]  Guy Wallis,et al.  A Species of Reef Fish that Uses Ultraviolet Patterns for Covert Face Recognition , 2010, Current Biology.

[18]  N Shashar,et al.  Squids (Loligo pealei and Euprymna scolopes) Can Exhibit Polarized Light Patterns Produced by Their Skin. , 1997, The Biological bulletin.

[19]  G. Svaetichin,et al.  Electric responses from the isolated retinas of fishes. , 1958, American journal of ophthalmology.

[20]  J. L. Schnapf,et al.  Surround Antagonism in Macaque Cone Photoreceptors , 2003, Journal of Neuroscience.

[21]  E. MacNichol,et al.  Inactivation of Horizontal Cells in Turtle Retina by Glutamate and Aspartate , 1972, Science.

[22]  E. Denton,et al.  Reflective Communication between Fish, with Special Reference to the Greater Sand Eel, Hyperoplus lanceolatus , 1994 .

[23]  M. Kamermans,et al.  Retinal parallel pathways: Seeing with our inner fish , 2009, Vision Research.

[24]  H Spekreijse,et al.  The dynamic characteristics of the feedback signal from horizontal cells to cones in the goldfish retina , 2001, The Journal of physiology.

[25]  C. Hawryshyn,et al.  Spectral and ultraviolet-polarisation sensitivity in juvenile salmonids: a comparative analysis using electrophysiology. , 2000, The Journal of experimental biology.

[26]  C. Groot.  On the orientation of young sockeye salmon (Oncorhynchus nerka) during their seaward migration out of lakes , 1965 .

[27]  Teruya Ohtsuka,et al.  Effects of chemicals on receptors and horizontal cells in the retina , 1972, The Journal of physiology.

[28]  N. Vardi,et al.  ON cone bipolar cells in rat express the metabotropic receptor mGluR6 , 1997, Visual Neuroscience.

[29]  Dr. habil. Gábor Horváth,et al.  Polarized Light in Animal Vision , 2004, Springer Berlin Heidelberg.

[30]  M. Kamermans,et al.  The contribution of the outer retina to color constancy: A general model for color constancy synthesized from primate and fish data , 2007, Visual Neuroscience.

[31]  S. Zeki.  Colour coding in the cerebral cortex: The responses of wavelength-selective and colour-coded cells in monkey visual cortex to changes in wavelength composition , 1983, Neuroscience.

[32]  H Spekreijse,et al.  The cone/horizontal cell network: A possible site for color constancy , 1998, Visual Neuroscience.

[33]  Nicholas W Roberts,et al.  Differences in the optical properties of vertebrate photoreceptor classes leading to axial polarization sensitivity. , 2004, Journal of the Optical Society of America. A, Optics, image science, and vision.

[34]  H Spekreijse,et al.  Receptive Field Organization of the S-Potential , 1968, Science.

[35]  A. Genin,et al.  Twilight transitions in coral reef fish: the input of light-induced changes in foraging behaviour , 2005, Animal Behaviour.

[36]  P. K. Brown.  Rhodopsin rotates in the visual receptor membrane. , 1972, Nature: New biology.

[37]  C. Hawryshyn,et al.  Spatial orientation of rainbow trout to plane-polarized light: The ontogeny of E-vector discrimination and spectral sensitivity characteristics , 1990, Journal of Comparative Physiology A.

[38]  C. Hawryshyn,et al.  Spatial orientation of trout to partially polarized light , 1990, Journal of Comparative Physiology A.

[39]  N. Shashar,et al.  Polarization vision helps detect transparent prey , 1998, Nature.

[40]  P Sterling,et al.  Localization of mGluR6 to dendrites of ON bipolar cells in primate retina , 2000, The Journal of comparative neurology.

[41]  J. Nicol,et al.  Studies on the photoreceptors of Anchoa mitchilli and A. hepsetus (Engraulidae) with particular reference to the cones , 1978 .

[42]  Marco Bertamini,et al.  When S-cones contribute to chromatic global motion processing , 2007, Visual Neuroscience.

[43]  William H Baldridge,et al.  Proton-Mediated Feedback Inhibition of Presynaptic Calcium Channels at the Cone Photoreceptor Synapse , 2005, The Journal of Neuroscience.

[44]  W. McFarland,et al.  Ultraviolet visual pigments in marine fishes of the family pomacentridae , 1994, Vision Research.

[45]  C. Hawryshyn,et al.  Degeneration and regeneration of ultraviolet cone photoreceptors during development in rainbow trout , 2006, The Journal of comparative neurology.

[46]  G. Buchsbaum,et al.  Trichromacy, opponent colours coding and optimum colour information transmission in the retina , 1983, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[47]  van Johannes Hateren,et al.  A model of spatiotemporal signal processing by primate cones and horizontal cells , 2007 .

[48]  H Barlow,et al.  Redundancy reduction revisited , 2001, Network.

[49]  C. Hawryshyn,et al.  Acquisition of polarized-light orientation in salmonids under laboratory conditions , 2003, Animal Behaviour.

[50]  H Nawa,et al.  Molecular characterization of a novel retinal metabotropic glutamate receptor mGluR6 with a high agonist selectivity for L-2-amino-4-phosphonobutyrate. , 1993, The Journal of biological chemistry.

[51]  S. Zeki.  Colour coding in the cerebral cortex: The reaction of cells in monkey visual cortex to wavelengths and colours , 1983, Neuroscience.

[52]  R. Cone.  Rotational diffusion of rhodopsin in the visual receptor membrane. , 1972, Nature: New biology.

[53]  M. Sanders.  Handbook of Sensory Physiology , 1975 .

[54]  R. Wehner,et al.  Restrictions on rotational and translational diffusion of pigment in the membranes of a rhabdomeric photoreceptor , 1977, The Journal of general physiology.

[55]  Thomas Labhart,et al.  Polarization-opponent interneurons in the insect visual system , 1988, Nature.

[56]  N. Shashar,et al.  Polarization contrast of zooplankton: A model for polarization-based sighting distance , 2006, Vision Research.

[57]  J. Nicol,et al.  Polarization of light reflected from the silvery exterior of the bleak, Alburnus alburnus , 1965, Journal of the Marine Biological Association of the United Kingdom.

[58]  M. Kamermans,et al.  Retinal processing and opponent mechanisms mediating ultraviolet polarization sensitivity in rainbow trout (Oncorhynchus mykiss) , 2008, Journal of Experimental Biology.

[59]  D. H. Kelly,et al.  Effects of sharp edges in a flickering field. , 1959, Journal of the Optical Society of America.

[60]  Nicholas W Roberts,et al.  A mechanism of polarized light sensitivity in cone photoreceptors of the goldfish Carassius auratus. , 2007, Biophysical journal.

[61]  C. Hawryshyn,et al.  Double-cone internal reflection as a basis for polarization detection in fish. , 1998, Journal of the Optical Society of America. A, Optics, image science, and vision.

[62]  Joseph J Atick,et al.  Could information theory provide an ecological theory of sensory processing? , 2011, Network.

[63]  C. Hawryshyn,et al.  Regeneration of ultraviolet-sensitive cones in the retinal cone mosaic of thyroxin-challenged post-juvenile rainbow trout (Oncorhynchus mykiss) , 2003, Journal of Experimental Biology.

[64]  R. Fujii.  Cytophysiology of fish chromatophores , 1993 .

[65]  L. Nittler,et al.  Meteoritic oxide grain from supernova found , 1998, Nature.

[66]  H. Kasukawa,et al.  Mechanism of light reflection in blue damselfish motile iridophore , 1987 .

[67]  C. Hawryshyn,et al.  Polarized-light sensitivity in rainbow trout (Oncorhynchus mykiss): characterization from multi-unit responses in the optic nerve , 1993, Journal of Comparative Physiology A.

[68]  W. Thoreson,et al.  Feedback from Horizontal Cells to Rod Photoreceptors in Vertebrate Retina , 2008, The Journal of Neuroscience.

[69]  M. Kamermans,et al.  Mutations in TRPM1 are a common cause of complete congenital stationary night blindness. , 2009, American journal of human genetics.

[70]  K. Naka,et al.  The generation and spread of S‐potentials in fish (Cyprinidae) , 1967, The Journal of physiology.

[71]  J. Alexander Heimel,et al.  A Transient Receptor Potential-Like Channel Mediates Synaptic Transmission in Rod Bipolar Cells , 2009, The Journal of Neuroscience.

[72]  A. L. Byzov,et al.  Amplification of graded potentials in horizontal cells of the retina , 1977, Vision Research.

[73]  H. V. Hateren,et al.  A cellular and molecular model of response kinetics and adaptation in primate cones and horizontal cells. , 2005 .

[74]  Maarten Kamermans,et al.  Lateral Gain Control in the Outer Retina Leads to Potentiation of Center Responses of Retinal Neurons , 2009, The Journal of Neuroscience.

[75]  C. Hawryshyn,et al.  Cone photoreceptor mechanisms and the detection of polarized light in fish , 1987, Journal of Comparative Physiology A.

[76]  Ewald Hering.  Outlines of a theory of the light sense , 1964 .

[77]  H. Spekreijse,et al.  Horizontal cells feed back to cones by shifting the cone calcium-current activation range , 1996, Vision Research.

[78]  Maarten Kamermans,et al.  Hemichannel-Mediated and pH-Based Feedback from Horizontal Cells to Cones in the Vertebrate Retina , 2009, PloS one.

[79]  K. Horch,et al.  Mechanism of Polarized Light Perception , 1966, Science.

[80]  G. D. Bernard,et al.  VISUAL PIGMENTS OF INVERTEBRATES , 1985 .

[81]  N. Vardi.  Alpha subunit of Go localizes in the dendritic tips of ON bipolar cells , 1998, The Journal of comparative neurology.

[82]  Shigetada Nakanishi,et al.  Developmentally regulated postsynaptic localization of a metabotropic glutamate receptor in rat rod bipolar cells , 1994, Cell.

[83]  S. Laughlin,et al.  Predictive coding: a fresh view of inhibition in the retina , 1982, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[84]  M Kamermans,et al.  Hemichannel-Mediated Inhibition in the Outer Retina , 2001, Science.

[85]  A. Snyder.  Physics of Vision in Compound Eyes , 1979 .