Retinal Region of Polarization Sensitivity Switches during Ontogeny of Rainbow Trout

Shai Sabbah; Maheen F. Habib-Nayany; Zahra Dargaei; Frances E. Hauser; Maarten Kamermans; Craig W. Hawryshyn

doi:10.1523/JNEUROSCI.5815-12.2013

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Re:Unconvincing evidence for polarization sensitivity in rainbow trout
Shai Sabbah

Submitted on: 14 May 2013
Unconvincing evidence for polarization sensitivity in rainbow trout
Inigo Novales Flamarique

Submitted on: 29 April 2013

Submitted on: (14 May 2013)
Page navigation anchor for Re:Unconvincing evidence for polarization sensitivity in rainbow trout
Re:Unconvincing evidence for polarization sensitivity in rainbow trout
Shai Sabbah
Other Contributors:
Maarten Kamermans, Craig W. Hawryshyn
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 func...
Show More

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
Show Less

Competing Interests: None declared.
Submitted on: (29 April 2013)
Page navigation anchor for Unconvincing evidence for polarization sensitivity in rainbow trout
Unconvincing evidence for polarization sensitivity in rainbow trout
Inigo Novales Flamarique, Professor
The main conclusion by Sabbah et al. 2013 (J Neurosci 33:7428-7438), that the region of polarization sensitivity in the trout retina changes with ontogeny, cannot be supported based on the results presented, and is inconsistent with published literature. Compound action potential (CAP) recordings from rainbow trout of different sizes show that the error in sensitivity measurements is at least 0.1 to 0.2 log units. This is...
Show More

The main conclusion by Sabbah et al. 2013 (J Neurosci 33:7428-7438), that the region of polarization sensitivity in the trout retina changes with ontogeny, cannot be supported based on the results presented, and is inconsistent with published literature. Compound action potential (CAP) recordings from rainbow trout of different sizes show that the error in sensitivity measurements is at least 0.1 to 0.2 log units. This is evident when averaging results over a number of fish (Beaudet et al., 1993), or when taking repeated measures for a given wavelength or E-vector angle during the course of an experiment (Novales Flamarique, 1997). The error of the technique is therefore of similar magnitude to the differences presented as evidence for polarization sensitivity (see multiple traces in Fig. 2-4 that fit this criterion). In particular, all the data points presented for the smolt retina for any given curve (Fig. 4B,D) are within 0.2 log units of each other. No statistical analysis is presented by the authors, suggesting that the averages (e.g. Fig. 4D; LW adaptation) are not statistically different and, as such, the fish are not polarization sensitive. Examination of the spectral sensitivity curves reveals major discrepancies with published literature. Under a long wavelength adapting background, this size of parr fish should have a spectral sensitivity peak at 390 nm and another at 420-430 nm, with a trough in between (Beaudet et al. 1993). The authors, instead, find a peak at 360 nm and a drop at 430 nm (Fig. 5B) which is inconsistent with the absorbance characteristics and distributions of single cones in rainbow trout of this size. The lower half of the ventral retina of this size parr is dominated by S cones (Cheng and Novales Flamarique, 2007) and one would expect a peak in sensitivity around 430 nm and a shift of CAP responses in the ultraviolet toward a 400 nm peak, in accordance with the absorbance and relative numbers of UV and S cones in the retina. The results presented (Fig. 5A-D) would be expected from differential bleaching of L cones in the ventral and dorsal retina. L cones exhibit a main photoproduct peaking at 360 nm whose magnitude increases with bleaching, and whose presence is accompanied by reduced linear dichroism (Harosi and MacNichol, 1974), potentially leading to changes in axial polarization sensitivity. Differential bleaching of the ventral versus the dorsal retina would arise because of the lower density and packing of cones in the dorsal retina (Cheng and Novales Flamarique, 2007). Together, these observations, and the unknown contribution of the M cone (which was not chromatically adapted, Fig. 5A-D), could explain the unusual spectral sensitivity peaks reported, the minute modulation of polarization sensitivity assigned to the L cone, and the associated differences between ventral and dorsal polarization sensitivities (Fig. 4C,D). At best, the results for UV wavelengths are only partially due to the action of UV cones. Further support for the latter conclusion comes from published literature in which smolt trout of the size reported on had no UV cones in the main retina (Cheng and Novales Flamarique, 2007). The authors provide no independent evidence of UV cones in the fish studied. As such, and given the limitations of the technique used, problems with confounding variables, and misrepresentation of the literature (which duly challenges the evidence for polarization sensitivity in rainbow trout; Horvath and Varju, 2004), this manuscript cannot support its title.
References 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, Novales Flamarique I (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. Harosi FI, MacNichol EFJr (1974) Visual pigments of goldfish cones: spectral properties and dichroism. J Gen Physiol 63:279-304. Horvath G, Varju D (2004) Polarized light in animal vision: polarization patterns in nature. Berlin: Springer-Verlag. Novales Flamarique I (1997) Vertebrate detection of polarized light. University of Victoria PhD Dissertation.
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Competing Interests: None declared.

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Re:Unconvincing evidence for polarization sensitivity in rainbow trout
Shai Sabbah

Published on: 14 May 2013
Unconvincing evidence for polarization sensitivity in rainbow trout
Inigo Novales Flamarique

Published on: 29 April 2013

Published on: (14 May 2013)
Page navigation anchor for Re:Unconvincing evidence for polarization sensitivity in rainbow trout
Re:Unconvincing evidence for polarization sensitivity in rainbow trout
Shai Sabbah
Other Contributors:
Maarten Kamermans, Craig W. Hawryshyn
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 func...
Show More

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
Show Less

Competing Interests: None declared.
Published on: (29 April 2013)
Page navigation anchor for Unconvincing evidence for polarization sensitivity in rainbow trout
Unconvincing evidence for polarization sensitivity in rainbow trout
Inigo Novales Flamarique, Professor
The main conclusion by Sabbah et al. 2013 (J Neurosci 33:7428-7438), that the region of polarization sensitivity in the trout retina changes with ontogeny, cannot be supported based on the results presented, and is inconsistent with published literature. Compound action potential (CAP) recordings from rainbow trout of different sizes show that the error in sensitivity measurements is at least 0.1 to 0.2 log units. This is...
Show More

The main conclusion by Sabbah et al. 2013 (J Neurosci 33:7428-7438), that the region of polarization sensitivity in the trout retina changes with ontogeny, cannot be supported based on the results presented, and is inconsistent with published literature. Compound action potential (CAP) recordings from rainbow trout of different sizes show that the error in sensitivity measurements is at least 0.1 to 0.2 log units. This is evident when averaging results over a number of fish (Beaudet et al., 1993), or when taking repeated measures for a given wavelength or E-vector angle during the course of an experiment (Novales Flamarique, 1997). The error of the technique is therefore of similar magnitude to the differences presented as evidence for polarization sensitivity (see multiple traces in Fig. 2-4 that fit this criterion). In particular, all the data points presented for the smolt retina for any given curve (Fig. 4B,D) are within 0.2 log units of each other. No statistical analysis is presented by the authors, suggesting that the averages (e.g. Fig. 4D; LW adaptation) are not statistically different and, as such, the fish are not polarization sensitive. Examination of the spectral sensitivity curves reveals major discrepancies with published literature. Under a long wavelength adapting background, this size of parr fish should have a spectral sensitivity peak at 390 nm and another at 420-430 nm, with a trough in between (Beaudet et al. 1993). The authors, instead, find a peak at 360 nm and a drop at 430 nm (Fig. 5B) which is inconsistent with the absorbance characteristics and distributions of single cones in rainbow trout of this size. The lower half of the ventral retina of this size parr is dominated by S cones (Cheng and Novales Flamarique, 2007) and one would expect a peak in sensitivity around 430 nm and a shift of CAP responses in the ultraviolet toward a 400 nm peak, in accordance with the absorbance and relative numbers of UV and S cones in the retina. The results presented (Fig. 5A-D) would be expected from differential bleaching of L cones in the ventral and dorsal retina. L cones exhibit a main photoproduct peaking at 360 nm whose magnitude increases with bleaching, and whose presence is accompanied by reduced linear dichroism (Harosi and MacNichol, 1974), potentially leading to changes in axial polarization sensitivity. Differential bleaching of the ventral versus the dorsal retina would arise because of the lower density and packing of cones in the dorsal retina (Cheng and Novales Flamarique, 2007). Together, these observations, and the unknown contribution of the M cone (which was not chromatically adapted, Fig. 5A-D), could explain the unusual spectral sensitivity peaks reported, the minute modulation of polarization sensitivity assigned to the L cone, and the associated differences between ventral and dorsal polarization sensitivities (Fig. 4C,D). At best, the results for UV wavelengths are only partially due to the action of UV cones. Further support for the latter conclusion comes from published literature in which smolt trout of the size reported on had no UV cones in the main retina (Cheng and Novales Flamarique, 2007). The authors provide no independent evidence of UV cones in the fish studied. As such, and given the limitations of the technique used, problems with confounding variables, and misrepresentation of the literature (which duly challenges the evidence for polarization sensitivity in rainbow trout; Horvath and Varju, 2004), this manuscript cannot support its title.
References 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, Novales Flamarique I (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. Harosi FI, MacNichol EFJr (1974) Visual pigments of goldfish cones: spectral properties and dichroism. J Gen Physiol 63:279-304. Horvath G, Varju D (2004) Polarized light in animal vision: polarization patterns in nature. Berlin: Springer-Verlag. Novales Flamarique I (1997) Vertebrate detection of polarized light. University of Victoria PhD Dissertation.
Show Less

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