Retinal processing and opponent mechanisms mediating ultraviolet polarization sensitivity in rainbow trout (Oncorhynchus mykiss)

Abstract

SUMMARYA number of teleost fishes have photoreceptor mechanisms to detect linearly polarized light. We studied the neuronal mechanism underlying this ability. It was found that a polarized signal could be detected in rainbow trout (Oncorhynchus mykiss) both in the electroretinogram (ERG) and in the compound action potential (CAP) measured in the optic nerve, indicating a strong retinal contribution to the processing of polarized light. The CAP recordings showed a W-shaped sensitivity curve, with a peak at 0°, 90°a nd 180°, consistent with processes for both vertical and horizontal orientation. By contrast, the ERG recordings reveal a more complex pattern. In addition to the peaks at 0°, 90° and 180°, two additional peaks appeared at 45° and 135°. This result suggests a specialized contribution of the outer retina in the processing of polarized light. The spectral sensitivity of the mechanisms responsible for these intermediate peaks was studied using chromatic adaptation. Here we show that long wavelength-sensitive (LWS) cone mechanism adaptation shifted the intermediate peaks towards 90°, whereas ultraviolet-sensitive (UVS) cone mechanism adaptation shifted the peaks away from 90° towards either 0° or 180°. These results provide further confirmation that the 90° peak is dominated by the LWS cone mechanism and the 0° and 180° peaks are dominated by the UVS cone mechanism. In addition, a pharmacological approach was used to examine the retinal neural mechanisms underlying polarization sensitivity. The effect of blocking negative feedback from horizontal cells to cones on the ERG was studied by making intraocular injections of low doses of cobalt, known to block this feedback pathway. It was found that the intermediate peaks seen in the ERG polarization sensitivity curves were eliminated after application of cobalt, suggesting that these peaks are due to outer retinal inhibition derived from feedback of horizontal cells onto cones. A simple computational model was developed to evaluate these results. The model consists of opponent and non-opponent processing elements for the two polarization detectors. This model provides a first approximation analysis suggesting that opponent processing occurs in the outer retina for polarization vision. Although it seems that polarization vision uses a slightly more complicated coding scheme than colour vision, the results presented in this paper suggest that opponent and non-opponent channels process polarization information.

Behavioural and physiological mechanisms of polarized light sensitivity in birds

“…These fish have a UV-sensitive mechanism with polarization sensitivity to a vertically aligned e-vector and a green-and red-sensitive receptor mechanism with maximum polarization sensitivity to a horizontally aligned e-vector [2,67,68,82,83]. The intermediate blue-sensitive receptor mechanism is insensitive to PL.…”

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

“…A second laser beam was passed through the receptor's long axis to measure axial dichroism and showed that MWS cones 1 had a dichroic ratio of 1.2 [20]. Although this is well below the polarization sensitivity of goldfish cones at 7 -8 [14], it was argued that the high polarization sensitivity is achieved by opponent interactions between polarization detectors [21]. Roberts & Needham [20] suggested that cone axial dichroism could be related to specializations in the outer segment of cone photoreceptors, such as disc membrane viscosity that aligns chromophores to predominately one axis of orientation and a slight tilting in the plane of absorbance of disc membrane.…”

“…Differential polarization sensitivity, in the UV-short wavelength part of the spectrum, is a product of the interaction between the a-band of the UVS cone mechanism-the vertical detector mechanism-and the b-band 2 of the MWS/LWS cone mechanisms-the horizontal detector mechanism [13,21].…”

“…It contains both ON and OFF responses. In Ramsden et al [21], only the CAP-ON responses were analysed. Finally, the HC recordings are intracellular recordings of HC polarization sensitivity in eyecup preparations.…”

Primary processes in sensory cells: current advances

“…Anchovies have tilted the discs in their cone photoreceptors by »90° so that the incident light enters each disc from the side (Heß et al 2006) and, presumably, hits retinal molecules that are more or less aligned with the disc membranes and preferably absorb light polarized in the membrane plane. This appears to be a solution to generate dichroic ciliary photoreceptors, but other strategies may also exist (Roberts and Needham 2007;Ramsden et al 2008). A new aspect of polarization vision is the recent discovery that marine mantis shrimps (stomatopod crustaceans; Marshall et al 2007) are able to detect circularly polarized light, and even to distinguish left-handed from right-handed circularly polarized light (Chiou et al 2008).…”