Skip to main content
Log in

Cone photoreceptor mechanisms and the detection of polarized light in fish

  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Summary

Although numerous studies have demonstrated the detection of polarized light in vertebrates, little is known of the photoreceptor mechanisms involved. Recent evidence, however, indicates that cyprinid fishes possess both ultraviolet (UV) and polarization sensitivity suggesting that some vertebrates, like many invertebrates, may employ UV-sensitive cone receptors in polarization sensitivity. In this report, we describe experiments that determine which spectral types of receptors participate in the detection of polarized light. We used a heart-rate conditioning technique to measure increment thresholds of immobilized goldfish for plane-polarized, narrow-band (10 nm half max.) spectral stimuli (380 nm, 460 nm, 540 nm, 660 nm). A typical experiment involved ‘isolating’ the activity of a cone photoreceptor mechanism by chromatic adaptation and measuring increment thresholds for spectral stimuli at e-vector orientations of the polarizer between 0° to 180° in 30° steps. The UV-, green- and red-sensitive cone receptor mechanisms showed clear evidence of polarization sensitivity while the blue-sensitive cone receptor mechanism was polarizationally insensitive. The average amplitude (base to peak height on Fig. 4) of the polarization sensitivity curves (UV-, green- and red-curves) was 0.67 log unit (standard deviation of 0.12 log unit), with the UV-sensitive cone receptor mechanism most sensitive to the vertical e-vector axis and the green- and red-sensitive cone receptor mechanisms most sensitive to the horizontal e-vector axis. The observation that different cone photoreceptor mechanisms have orthogonal polarization sensitivity in fish suggests that the perception of polarized light may enhance the capacity for visual discrimination in lower vertebrates.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ali MA, Anctil M (1976) Retinas of fishes: An atlas. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Avery JA, Bowmaker JK, Djamgoz MBA, Downing JLG (1982) Ultra-violet sensitive receptors in a freshwater fish. J Physiol (Lond) 334:23P

    Google Scholar 

  • Beauchamp RD, Rowe JS (1977) Goldfish spectral sensitivity: A conditioned heart-rate measure in restrained or curarized fish. Vision Res 17:617–624

    Google Scholar 

  • Beauchamp RD, Rowe JS, O'Reilly LA (1979) Goldfish spectral sensitivity: identification of the three cone mechanisms in heart-rate conditioned fish using colored adapting backgrounds. Vision Res 19:1295–1302

    Google Scholar 

  • Bernard GD, Wehner R (1977) Functional similarities between polarization vision and color vision. Vision Res 17:1019–1028

    Google Scholar 

  • Boehm G (1940) Über ein neues entoptisches Phänomen im polarisierten Licht. ‘Periphere’ Polarisationsbüschel. Acta Ophthalmol 18:143–169

    Google Scholar 

  • Cone RA (1972) Rotational diffusion of rhodopsin in the visual receptor membrane. Nature 236:39–43

    Google Scholar 

  • Delius JD, Perchard RJ, Emmerton JA (1976) Polarized light discrimination by pigeons and an electroretinographic correlate. J Comp Physiol Psychol 70:560–571

    Google Scholar 

  • Denton EJ (1959) The contributions of the oriented photosensitive and other molecules to the absorption of whole retina. Philos Trans R Soc Lond Ser B 150:78–94

    Google Scholar 

  • Dill PA (1971) Perception of polarized light by yearling sockeye salmon (Oncorhynchus nerka). J Fish Res Board Can 28:1319–1322

    Google Scholar 

  • Fein A, Szuts EZ (1982) Photoreceptors: Their role in vision. Cambridge University Press, Cambridge

    Google Scholar 

  • Fineran BA, Nicol JAC (1978) Studies on the photoreceptors ofAnchoa mitchilli andA. hepsetus (Engranlidae) with particular reference to the cones. Philos Trans R Soc Lond Ser B 283:25–60

    Google Scholar 

  • Forward RB Jr, Waterman TH (1973) Evidence for e-vector and light intensity pattern discrimination by the teleostDermogenys. J Comp Physiol 87:189–202

    Google Scholar 

  • Goldsmith TH (1975) The polarization sensitivity-dichroic absorption paradox in arthropod photoreceptors. In: Snyder AW, Menzel R (eds) Photoreceptor optics. Springer, Berlin Heidelberg New York, pp 392–409

    Google Scholar 

  • Groot C (1965) On the orientation of young sockeye salmon (Oncorhynchus nerka) during their seaward migration out of the lakes. Behaviour [Suppl] 14:198

    Google Scholar 

  • Haidinger W (1844) Über das direkte Erkennen des polarisierten Lichts und der Lage der Polarisationsebene. Ann Physik Chemie 63:29–39

    Google Scholar 

  • Harosi FI, Hashimoto Y (1983) Ultraviolet visual pigment in a vertebrate: a tetrachromatic cone system in the dace. Science 222:1021–1023

    Google Scholar 

  • Harosi FI, MacNichol EF Jr (1974) Visual pigments of goldfish cones: spectral properties and dichroism. J Gen Physiol 63:279–304

    Google Scholar 

  • Hawryshyn CW (1982) Studies of animal color vision; comments on some important theoretical considerations. Can J Zool 60:2968–2970

    Google Scholar 

  • Hawryshyn CW, Beauchamp RD (1982) Aberrant high blue sensitivity in goldfish. Invest Ophthalmol Visual Sci [Suppl] 22:282

    Google Scholar 

  • Hawryshyn CW, Beauchamp RD (1985) Ultraviolet photosensitivity in goldfish: an independent UV retinal mechanism. Vision Res 25:11–20

    Google Scholar 

  • Hawryshyn CW, McFarland WN (1986) Polarization sensitivity in a cyprinid fish. Invest Ophthal Visual Sci [Suppl] 27:77

    Google Scholar 

  • Ivanoff A, Waterman TH (1958) Factors, mainly depth and wavelength, affecting the degree of underwater light polarization. J Mar Res 16:283–307

    Google Scholar 

  • Jacobs GH (1982) Comparative color vision. Academic Press, New York, 209 pp

    Google Scholar 

  • Kawamura G, Shigata A, Yonemori T (1981) Response of teleost to the plane of polarized light as determined by the heart-beat rate. Bull Jpn Soc Sci Fish 47:727–729

    Google Scholar 

  • Kleerekoper H, Matis JH, Timms AM, Gensler P (1973) Locomotor response of the goldfish to polarized light and its e-vector. J Comp Physiol 86:27–36

    Google Scholar 

  • Kreithen ML, Keeton WT (1974) Detection of polarized light by the pigeon,Columba livia. J Comp Physiol 89:83–92

    Google Scholar 

  • Labhart T (1980) Specialized photoreceptors at the dorsal rim of the honeybee's compound eye: polarizational and angular sensitivity. J Comp Physiol 141:19–30

    Google Scholar 

  • Laties AM, Enoch JM (1971) An analysis of retinal receptor orientation. I. Angular relationship of neighboring photoreceptors. Invest Ophthalmol Visual Sci 10:69–77

    Google Scholar 

  • Lythgoe JN, Hemmings CC (1967) Polarized light and underwater vision. Nature 213:893–894

    Google Scholar 

  • Marc RE, Sperling HG (1976) The chromatic organization of the goldfish cone mosaic. Vision Res 16:1211–1224

    Google Scholar 

  • Menzel R, Snyder AW (1974) Polarized light detection in the beeApis mellifera. J Comp Physiol 88:247–270

    Google Scholar 

  • Poo MM, Cone RA (1974) Lateral diffusion of rhodopsin in the photoreceptor membrane. Nature 247:438–441

    Google Scholar 

  • Saidel WM, Lettvin JY, MacNichol EF Jr (1983) Processing of polarized light by squid photoreceptors. Nature 304:534–536

    Google Scholar 

  • Schmidt WJ (1938) Polarisationsoptische Analyse eines EiweißLipoid-Systems, erläutert am Außenglied der Sehzellen. Kolloid-Z 85:137–148

    Google Scholar 

  • Sears FW (1958) Optics. Addison-Wesley Publ Co, London

    Google Scholar 

  • Shaw SR (1969) Sense-cell structure and interspecies comparisons of polarized-light absorption in arthropod compound eyes. Vision Res 9:1031–1040

    Google Scholar 

  • Taylor DH, Adler K (1974) Spatial orientation by salamanders using plane-polarized light. Science 181:285–287

    Google Scholar 

  • Waterman TH (1975) Natural polarized light and e-vector discrimination by vertebrates. In: Evans GC, Bainbridge R, Rackham O (eds) Light as an ecological factor. II, Blackwell Press, Oxford, pp 305–335

    Google Scholar 

  • Waterman TH (1981) Polarization sensitivity. In: Autrum H (ed) Comparative physiology and evolution of vision in invertebrates b: Invertebrate visual centers and behavior I. (Handbook of sensory physiology, vol. VII/6B) Springer, Berlin Heidelberg New York, pp 281–469

    Google Scholar 

  • Waterman TH (1984) Natural polarized light and vision. In: Ali MA (ed) Photoreceptors and vision in invertebrates. Plenum Press, New York, pp 63–114

    Google Scholar 

  • Waterman TH, Aoki K (1974) E-vector sensitivity patterns in the goldfish optic tectum. J Comp Physiol 95:13–27

    Google Scholar 

  • Waterman TH, Forward RB Jr (1970) Field evidence for polarized light sensitivity in the fishZenarchopterus. Nature 228:85–87

    Google Scholar 

  • Waterman TH, Forward RB Jr (1972) Field demonstration of polarotaxis in the fishZenarchopterus. J Exp Zool 180:33–54

    Google Scholar 

  • Waterman TH, Hashimoto H (1974) E-vector discrimination by the goldfish optic tectum. J Comp Physiol 95:1–12

    Google Scholar 

  • Wehner R (1976) Polarized-light navigation by insects. Sci Am 235:106–115

    Google Scholar 

  • Wehner R (1983) The perception of polarized light. In: Consens DJ, Vince-Price D (eds) The biology of photoreception. Soc Exp Biol Symposium XXXVI, pp 331–369

  • Wehner R, Strasser S (1985) The Pol area of the honeybee's eye: behavioral evidence. Physiol Entomol 10:337–349

    Google Scholar 

  • Wehner R, Bernard GD, Geiger E (1975) Twisted and nontwisted rhabdoms and their significance for polarization detection in the bee. J Comp Physiol 104:225–245

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hawryshyn, C.W., McFarland, W.N. Cone photoreceptor mechanisms and the detection of polarized light in fish. J. Comp. Physiol. 160, 459–465 (1987). https://doi.org/10.1007/BF00615079

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00615079

Keywords

Navigation