Abstract
In many arthropod eyes the ommatidia contain two classes of retinular cells with orthogonally oriented microvilli. These receptors provide the basis for two-channel polarization vision. In several contexts such as navigation or the detection of polarization contrast, two channels may be insufficient. While solutions to this problem are known (e.g. in insects and stomatopod crustaceans) none have been found in the majority of decapods. To examine this issue further, the polarization sensitivity and the E-vector angle eliciting a maximum response (θ max) were measured at over 300 loci on the crayfish retinula. The polarization response ratio (which is proportional to polarization sensitivity) was similar at all locations on the retinula. Around the central pole of the eye, θ max was distributed about the vertical and horizontal axes. Along the dorsal rim, the distribution of θ max exhibits modes at 0°, 45° and 90° and a small mode at 135° relative to the dorso-ventral axis of the eyestalk (0°). Smaller numbers of cells (20 to 25%) with θ max near the diagonal were also found in anterior and posterior retinula areas. Thus crayfish visual interneurons, which integrate signals from multiple ommatidia may have access to a multi-channel polarization analyzer.
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Abbreviations
- A/D:
-
Analog to digital
- MΩ:
-
106 ohms
- PRR:
-
Polarization response ratio
- PS:
-
Polarization sensitivity
- R θ :
-
Response to polarized light at a particular E-vector
- θ :
-
E-vector angle
- θ max :
-
E-vector angle eliciting a maximum response
References
Armitage P, Berry G, Matthews JNS (2002) Statistical methods in medical research. Blackwell, Oxford, pp 112–137
Bernard GD, Wehner R (1977) Functional similarities between polarization vision and color vision. Vision Res 17:1019–1028
Cronin TW, Shashar N, Caldwell RL, Marshall J, Cheroska AG, Chiou T-H (2003) Polarization vision and its role in biological signaling. Integr Comp Biol 43:549–558
Cummins D, Goldsmith TH (1981) Cellular identification of the violet receptor in the crayfish eye. J Comp Physiol 142:199–202
Dacke M, Nordström P, Scholtz CH, Warrant EJ (2002) A specialized dorsal rim area for polarized light detection in the compound eye of the scarab beetle Pachysoma striatum. J Comp Physiol A 188:211–216
Glantz RM. (1996a) Polarization sensitivity in crayfish lamina monopolar neurons. J Comp Physiol A 178:413–425
Glantz RM (1996b) Polarization sensitivity in the crayfish optic lobe: Peripheral contributions to opponency and directionally selective motion detection. J Neurophysiol 76:3404–3414
Glantz RM (2001) Polarization analysis in the crayfish visual system. J Exp Biol 204:2383–2390
Glantz RM, McIsaac A (1998) Two-channel polarization analyzer in the sustaining fiber-dimming fiber ensemble of crayfish visual system. J Neurophysiol 80:2571–2583
Glantz RM, Schroeter JP (2006) Polarization contrast and motion detection. J Comp Physiol A 192:905–914
Glantz RM, Schroeter JP (2007) Orientation by polarized light in the crayfish dorsal light reflex:behavioral and neurophysiological studies. J Comp Physiol A 193:371–384
Goddard SM, Forward RB (1991) The role of the underwater polarized light pattern in the sun compass navigation of the grass shrimp, Palaemonetes vulgaris. J Comp Physiol A 169:479–491
Herrnkind W F (1968) Adaptive visually-directed orientation in Uca pugilator. Am Zool 8:585–598
Homberg U (2004) In search of the sky compass in the insect brain. Naturwiss 91(5):199–208
Kleinlogel S, Marshall NJ (2006) Electrophysiological evidence for linear polarization sensitivity in the compound eyes of the stomatopod crustacean Gonodactylus chiragra. J Exp Biol 209:4262–4272
Kleinlogel S, Marshall NJ, Horwood JM, Land MF (2003) Neuroarchitecture of the color and polarization vision system of the stomatopod Haptosquilla. J Comp Neurol 467:326–342
Labhart T (1986) The electrophysiology of photoreceptors in different eye regions of the desert ant, Cataglyphis bicolor. J Comp Physiol A 158:1–7
Labhart T, Meyer EP (2002) Neural mechanisms in insect navigation: polarization compass and odometer. Curr Opin Neurobiol 12:707–714
Labhart T, Petzold J, Helbling H (2001) Spatial integration in polarization-sensitive interneurons of crickets: a survey of evidence mechanisms and benefits. J Exp Biol 204:2423–2430
Mappes M, Homberg U (2004) Behavioral analysis of polarization vision in tethered flying locusts. J Comp Physiol A 190(1):61–68
Marshall NJ, Land MF, King CA, Cronin TW (1991) The compound eyes of mantis shrimps (Crustacea, Hoplocarida, Stomatopoda). I. Compound eye structure: the detection of polarized light. Philos Trans R Soc Lond B 334:33–56
Marshall J, Cronin TW, Shashar N, Land M (1999) Behavioral evidence for polarization vision in stomatopods reveals a potential channel for communication. Curr Biol 9:755–759
Muller KJ (1973) Photoreceptors in the crayfish compound eye: Electrical interactions between cells as related to polarized light sensitivity. J Physiol (Lond) 232:573–595
Nässel DR, Waterman TH (1977) Golgi EM evidence for visual information channelling in the crayfish lamina ganglionaris. Brain Res 130:556–563
Sabra R, Glantz RM (1985) Polarization sensitivity of crayfish photoreceptors is correlated with their termination sites in the lamina ganglionaris. J Comp Physiol A 156:315–318
Schiff H, Abbot BC, Manning RB (1985) Possible monocular range-finding mechanisms in stomatopods from different environmental light conditions. Comp Physiol Biochem A 80A:271–280
Shaw S (1966) Polarized light responses from crab retinula cells. Nature 211:92–93
Trevino DL, Larimer JL (1970) The responses of one class of neurons in the optic tract of the crayfish (Procambarus) to monochromatic light. Z Vergl Physiol 69:139–149
Waterman TH (1950) A light polarization analyzer in the compound eye of Limulus. Science 111:252–254
Waterman TH, Fernandez HR (1970) E-vector and wavelength discrimination by retinular cells of the crayfish Procambarus. Z Vergl Physiol 68:154–174
Waterman TH (1981) Polarization sensitivity. In: Autrum H (ed) Handbook of sensory physiology, vol VII/6. Springer, Heidelberg, pp 261–469
Waterman TH (1984) Natural polarized light and vision. In: Ali MA (ed) Photoreception and vision in invertebrates, Plenum, New York, pp 63–114
Wehner R (2001) Polarization vision: a uniform capacity? J Exp Biol 204:2589–2596
Acknowledgments
This study was supported by a grant from the National Science Foundation, IOB0613285. I thank the staff of Friday Harbor Labs (University of Washington) for their able assistance. All of the experiments were conducted with a humane concern for the animals’ welfare and in accordance with the University’s animal care regulations.
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Glantz, R.M. The distribution of polarization sensitivity in the crayfish retinula. J Comp Physiol A 193, 893–901 (2007). https://doi.org/10.1007/s00359-007-0242-x
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DOI: https://doi.org/10.1007/s00359-007-0242-x