Retinal Region of Polarization Sensitivity Switches during Ontogeny of Rainbow Trout

Novales questions the conclusions presented by Sabbah et al. 2013 (J Neurosci 33:7428-7438). Here we address his comments.

1) Novales suggests that the variation in sensitivity across e-vector orientations is in the order of magnitude of a typical polarization sensitivity (PS) measurement error. He also argues that the statistical analysis presented is inadequate. This is incorrect. The amplitude of each PS function in a given treatment group was calculated, and the average+/- SD amplitude for each group was reported along with the results of randomization tests. Note that the figures show the average PS functions for the various treatment groups. Of course, the amplitude of the average PS function is smaller than the average amplitude calculated. The statistical analysis of PS amplitude data, together with the analysis of the symmetry of PS functions, showed clearly that there is a switch in enhanced PS from the ventral to the dorsal retina when parr transform into smolts.

2) Novales refers to the work of Beaudet et al. (1993) to claim that spectral sensitivity data presented in the current study differs considerably from the published literature. Indeed they do. Beaudet studied the spectral sensitivity of the whole retina. Since we show here that spectral sensitivity varies between various parts of the retina, differences will occur when comparing the whole-retina spectral sensitivity with the spectral sensitivity of the ventral and dorsal retina.

3) The predictions of Novales about spectral sensitivity in trout parr are based on the finding that the lower region of the ventral retina of parr is dominated by SWS opsin mRNA (Cheng and Novales Flamarique, 2007). These results were obtained in trout considerably smaller (3.7+/-1.2 g) than those used in the current study (17+/-4.3 g). Since opsin mRNA and pigment expression varies with age and body mass, the results of Cheng and Novales Flamarique (2007) cannot be used to make any meaningful prediction for the present study. In fact, electrophysiological experiments (Deutschlander et al., 2001) in fish with body masses closer to those used in the current study (3-15 g) provide evidence for UV sensitivity mediated by the UVS pigments both in the dorsal and ventral retina of parr, consistent with our spectral sensitivity results.

4) Novales suggests that intense bleaching of cones may change their transverse and axial dichroism (Roberts and Needham, 2007; Harosi and MacNichol, 1974). Such bleaching is highly unlikely in our recording conditions since we used relatively dim adapting lights and we performed our in situ experiments in the intact eye, where chromophores are continuously being replenished by the retinal pigment epithelium. Furthermore, bleaching is a sensitivity regulation mechanism working on the phototransduction cascade of individual cones and is therefore independent of the packing of cones. Therefore, the arguments of Novales are not relevant for the present study.

5) Novales asks for independent evidence of UV cones in smolts. Cheng and Novales Flamarique (2007) have shown that trout smolts lack UV cones in the central retina. These findings agree well with previous studies that have repeatedly demonstrated that UV cones are present only in the dorsotemporal retina of smolts (Beaudet et al., 1993; Allison et al., 2003). Those previous studies are highly conclusive and support our results of the reduced contribution of UVS cone pigments in the ventral retina of smolts. Repeating the histological analysis of the retinal distribution of UV cones or UVS pigments, as suggested by Novales, is therefore redundant.

References

Allison WT, Dann SG, Helvik JV, Bradley C, Moyer HD, Hawryshyn CW (2003) Ontogeny of ultraviolet-sensitive cones in the retina of rainbow trout (Oncorhynchus mykiss). J Comp Neurol 461:294-306.

Beaudet L, Browman HI, Hawryshyn CW (1993) Optic nerve response and retinal structure in rainbow trout of different sizes. Vision Res 33:1739-1746.

Cheng CL, Flamarique IN (2007) Chromatic organization of cone photoreceptors in the retina of rainbow trout: single cones irreversibly switch from UV (SWS1) to blue (SWS2) light sensitive opsin during natural development. J Exp Biol 210:4123-4135.

Deutschlander ME, Greaves DK, Haimberger TJ, Hawryshyn CW (2001) Functional mapping of ultraviolet photosensitivity during metamorphic transitions in a salmonid fish, Oncorhynchus mykiss. J Exp Biol 204:2401-2413.

Harosi FI, Macnichol. E. F. (1974) Visual pigments of goldfish cones - Spectral properties and dichroism. J Gen Physiol 63:279-304.

Roberts NW, Needham MG (2007) A mechanism of polarized light sensitivity in cone photoreceptors of the goldfish Carassius auratus. Biophys J 93:3241-3248.

Conflict of Interest:

None declared