Limits...
Feedback from horizontal cells to cones mediates color induction and may facilitate color constancy in rainbow trout.

Sabbah S, Zhu C, Hornsby MA, Kamermans M, Hawryshyn CW - PLoS ONE (2013)

Bottom Line: Color vision is most beneficial when the visual system is color constant and can correct the excitations of photoreceptors for differences in environmental irradiance.We found that the efficiency of color induction in the cone output and optic nerve decreased significantly with the inhibition of HC-cone feedback.Therefore, our findings suggest not only that color induction originates as a result of HC-cone feedback, but also that this effect of HC-cone feedback is further amplified at downstream retinal elements, possibly through feedback mechanisms at the inner plexiform layer.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Queen's University, Kingston, Ontario, Canada. shai_sabbah@brown.edu

ABSTRACT
Color vision is most beneficial when the visual system is color constant and can correct the excitations of photoreceptors for differences in environmental irradiance. A phenomenon related to color constancy is color induction, where the color of an object shifts away from the color of its surroundings. These two phenomena depend on chromatic spatial integration, which was suggested to originate at the feedback synapse from horizontal cells (HC) to cones. However, the exact retinal site was never determined. Using the electroretinogram and compound action potential recordings, we estimated the spectral sensitivity of the photoresponse of cones, the output of cones, and the optic nerve in rainbow trout. Recordings were performed before and following pharmacological inhibition of HC-cone feedback, and were repeated under two colored backgrounds to estimate the efficiency of color induction. No color induction could be detected in the photoresponse of cones. However, the efficiency of color induction in the cone output and optic nerve was substantial, with the efficiency in the optic nerve being significantly higher than in the cone output. We found that the efficiency of color induction in the cone output and optic nerve decreased significantly with the inhibition of HC-cone feedback. Therefore, our findings suggest not only that color induction originates as a result of HC-cone feedback, but also that this effect of HC-cone feedback is further amplified at downstream retinal elements, possibly through feedback mechanisms at the inner plexiform layer. This study provides evidence for an important role of HC-cone feedback in mediating color induction, and therefore, likely also in mediating color constancy.

Show MeSH

Related in: MedlinePlus

Efficiency of color induction varies between the photoresponse of cones, output of cones, and optic nerve.(A) In the photoresponse of cones, the sensitivity ratio between UV and long wavelengths (580 nm/370 nm) under the Natural background (RN) did not differ significantly from that under the LW adaptation background (RLW), for both retina treated with saline (S + ASP) and retina treated with saline, aspartate and cobalt (S + ASP + Co). This suggests minimal efficiency of color induction in the photoresponse of cones, regardless of whether HC-cone feedback is inhibited or not. (B) In the output of cones and (C) optic nerve, the sensitivity ratio between UV and long wavelengths (640 nm/370 nm) under the Natural background was significantly smaller than under the LW adaptation background, for saline-treated retina (S) but not for retina treated with saline and cobalt (S + Co). This suggests relatively high efficiency of color induction in the output of cones and optic nerve. This efficiency, however, decreased with the application of cobalt and became insignificant. Note that the relationship between the sensitivity ratio under the Natural and LW adaptation conditions is in agreement with the estimation of the quantum catches of cone pigments. Filled symbols, mean of either RN or RLW; open symbols, individual RN or RLW values; error bars, ±1 SD; n.s., non-significant; asterisk, significant difference (P<0.05). Sample size: cone photoresponse, S + ASP Natural = 4, S + ASP LW adaptation = 5, S + ASP + Co Natural = 4, S + ASP + Co LW adaptation = 5; cone output, S Natural = 5, S LW adaptation = 4, S + Co Natural = 4, S + Co LW adaptation = 5; optic nerve, S Natural = 5, S LW adaptation = 4, S + Co Natural = 5, S + Co LW adaptation = 5. See Methods for details of the choice of wavelengths used for the calculation of RN and RLW. Note that spectra missing sensitivity values at the wavelengths used for the calculation of RN and RLW (370 and 580 nm for cone photoresponse, and 370 and 640 nm for cone output and optic nerve) were omitted from analysis.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC3672170&req=5

pone-0066216-g006: Efficiency of color induction varies between the photoresponse of cones, output of cones, and optic nerve.(A) In the photoresponse of cones, the sensitivity ratio between UV and long wavelengths (580 nm/370 nm) under the Natural background (RN) did not differ significantly from that under the LW adaptation background (RLW), for both retina treated with saline (S + ASP) and retina treated with saline, aspartate and cobalt (S + ASP + Co). This suggests minimal efficiency of color induction in the photoresponse of cones, regardless of whether HC-cone feedback is inhibited or not. (B) In the output of cones and (C) optic nerve, the sensitivity ratio between UV and long wavelengths (640 nm/370 nm) under the Natural background was significantly smaller than under the LW adaptation background, for saline-treated retina (S) but not for retina treated with saline and cobalt (S + Co). This suggests relatively high efficiency of color induction in the output of cones and optic nerve. This efficiency, however, decreased with the application of cobalt and became insignificant. Note that the relationship between the sensitivity ratio under the Natural and LW adaptation conditions is in agreement with the estimation of the quantum catches of cone pigments. Filled symbols, mean of either RN or RLW; open symbols, individual RN or RLW values; error bars, ±1 SD; n.s., non-significant; asterisk, significant difference (P<0.05). Sample size: cone photoresponse, S + ASP Natural = 4, S + ASP LW adaptation = 5, S + ASP + Co Natural = 4, S + ASP + Co LW adaptation = 5; cone output, S Natural = 5, S LW adaptation = 4, S + Co Natural = 4, S + Co LW adaptation = 5; optic nerve, S Natural = 5, S LW adaptation = 4, S + Co Natural = 5, S + Co LW adaptation = 5. See Methods for details of the choice of wavelengths used for the calculation of RN and RLW. Note that spectra missing sensitivity values at the wavelengths used for the calculation of RN and RLW (370 and 580 nm for cone photoresponse, and 370 and 640 nm for cone output and optic nerve) were omitted from analysis.

Mentions: To complete our analysis of the variation in the efficiency of color induction across different retinal processing stages, and to substantiate further our findings regarding the effect of HC-cone feedback on color induction, we took a different approach. We calculated the ratio between long-wavelength and ultraviolet sensitivity, for the Natural (RN) and LW adaptation (RLW) backgrounds (see Methods for a detailed description of the calculation of sensitivity ratios). A non-significant difference between RN and RLW may suggest minimal color induction. In contrast, a significant difference between RN and RLW may suggest substantial color induction. See Table 1 for detailed statistics of the effect of background modulation on the ratio between long-wavelength and ultraviolet sensitivity, across retinal processing stages. For the photoresponse of cones, RN and RLW did not differ significantly, for both saline-treated retina and cobalt-treated retina (Figure 6A). This suggests minimal (or zero) efficiency of color induction in the photoresponse of cones, regardless of whether HC-cone feedback is inhibited or not. On the other hand, for the output of cones and optic nerve, RN was significantly smaller than RLW for saline-treated retina, but not for cobalt-treated retina (Figure 6B,C). This suggests relatively high efficiency of color induction in the output of cones and optic nerve. This efficiency, however, decreased with the application of cobalt and became insignificant; supporting our findings of the importance of HC-cone feedback in mediating color induction.


Feedback from horizontal cells to cones mediates color induction and may facilitate color constancy in rainbow trout.

Sabbah S, Zhu C, Hornsby MA, Kamermans M, Hawryshyn CW - PLoS ONE (2013)

Efficiency of color induction varies between the photoresponse of cones, output of cones, and optic nerve.(A) In the photoresponse of cones, the sensitivity ratio between UV and long wavelengths (580 nm/370 nm) under the Natural background (RN) did not differ significantly from that under the LW adaptation background (RLW), for both retina treated with saline (S + ASP) and retina treated with saline, aspartate and cobalt (S + ASP + Co). This suggests minimal efficiency of color induction in the photoresponse of cones, regardless of whether HC-cone feedback is inhibited or not. (B) In the output of cones and (C) optic nerve, the sensitivity ratio between UV and long wavelengths (640 nm/370 nm) under the Natural background was significantly smaller than under the LW adaptation background, for saline-treated retina (S) but not for retina treated with saline and cobalt (S + Co). This suggests relatively high efficiency of color induction in the output of cones and optic nerve. This efficiency, however, decreased with the application of cobalt and became insignificant. Note that the relationship between the sensitivity ratio under the Natural and LW adaptation conditions is in agreement with the estimation of the quantum catches of cone pigments. Filled symbols, mean of either RN or RLW; open symbols, individual RN or RLW values; error bars, ±1 SD; n.s., non-significant; asterisk, significant difference (P<0.05). Sample size: cone photoresponse, S + ASP Natural = 4, S + ASP LW adaptation = 5, S + ASP + Co Natural = 4, S + ASP + Co LW adaptation = 5; cone output, S Natural = 5, S LW adaptation = 4, S + Co Natural = 4, S + Co LW adaptation = 5; optic nerve, S Natural = 5, S LW adaptation = 4, S + Co Natural = 5, S + Co LW adaptation = 5. See Methods for details of the choice of wavelengths used for the calculation of RN and RLW. Note that spectra missing sensitivity values at the wavelengths used for the calculation of RN and RLW (370 and 580 nm for cone photoresponse, and 370 and 640 nm for cone output and optic nerve) were omitted from analysis.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3672170&req=5

pone-0066216-g006: Efficiency of color induction varies between the photoresponse of cones, output of cones, and optic nerve.(A) In the photoresponse of cones, the sensitivity ratio between UV and long wavelengths (580 nm/370 nm) under the Natural background (RN) did not differ significantly from that under the LW adaptation background (RLW), for both retina treated with saline (S + ASP) and retina treated with saline, aspartate and cobalt (S + ASP + Co). This suggests minimal efficiency of color induction in the photoresponse of cones, regardless of whether HC-cone feedback is inhibited or not. (B) In the output of cones and (C) optic nerve, the sensitivity ratio between UV and long wavelengths (640 nm/370 nm) under the Natural background was significantly smaller than under the LW adaptation background, for saline-treated retina (S) but not for retina treated with saline and cobalt (S + Co). This suggests relatively high efficiency of color induction in the output of cones and optic nerve. This efficiency, however, decreased with the application of cobalt and became insignificant. Note that the relationship between the sensitivity ratio under the Natural and LW adaptation conditions is in agreement with the estimation of the quantum catches of cone pigments. Filled symbols, mean of either RN or RLW; open symbols, individual RN or RLW values; error bars, ±1 SD; n.s., non-significant; asterisk, significant difference (P<0.05). Sample size: cone photoresponse, S + ASP Natural = 4, S + ASP LW adaptation = 5, S + ASP + Co Natural = 4, S + ASP + Co LW adaptation = 5; cone output, S Natural = 5, S LW adaptation = 4, S + Co Natural = 4, S + Co LW adaptation = 5; optic nerve, S Natural = 5, S LW adaptation = 4, S + Co Natural = 5, S + Co LW adaptation = 5. See Methods for details of the choice of wavelengths used for the calculation of RN and RLW. Note that spectra missing sensitivity values at the wavelengths used for the calculation of RN and RLW (370 and 580 nm for cone photoresponse, and 370 and 640 nm for cone output and optic nerve) were omitted from analysis.
Mentions: To complete our analysis of the variation in the efficiency of color induction across different retinal processing stages, and to substantiate further our findings regarding the effect of HC-cone feedback on color induction, we took a different approach. We calculated the ratio between long-wavelength and ultraviolet sensitivity, for the Natural (RN) and LW adaptation (RLW) backgrounds (see Methods for a detailed description of the calculation of sensitivity ratios). A non-significant difference between RN and RLW may suggest minimal color induction. In contrast, a significant difference between RN and RLW may suggest substantial color induction. See Table 1 for detailed statistics of the effect of background modulation on the ratio between long-wavelength and ultraviolet sensitivity, across retinal processing stages. For the photoresponse of cones, RN and RLW did not differ significantly, for both saline-treated retina and cobalt-treated retina (Figure 6A). This suggests minimal (or zero) efficiency of color induction in the photoresponse of cones, regardless of whether HC-cone feedback is inhibited or not. On the other hand, for the output of cones and optic nerve, RN was significantly smaller than RLW for saline-treated retina, but not for cobalt-treated retina (Figure 6B,C). This suggests relatively high efficiency of color induction in the output of cones and optic nerve. This efficiency, however, decreased with the application of cobalt and became insignificant; supporting our findings of the importance of HC-cone feedback in mediating color induction.

Bottom Line: Color vision is most beneficial when the visual system is color constant and can correct the excitations of photoreceptors for differences in environmental irradiance.We found that the efficiency of color induction in the cone output and optic nerve decreased significantly with the inhibition of HC-cone feedback.Therefore, our findings suggest not only that color induction originates as a result of HC-cone feedback, but also that this effect of HC-cone feedback is further amplified at downstream retinal elements, possibly through feedback mechanisms at the inner plexiform layer.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Queen's University, Kingston, Ontario, Canada. shai_sabbah@brown.edu

ABSTRACT
Color vision is most beneficial when the visual system is color constant and can correct the excitations of photoreceptors for differences in environmental irradiance. A phenomenon related to color constancy is color induction, where the color of an object shifts away from the color of its surroundings. These two phenomena depend on chromatic spatial integration, which was suggested to originate at the feedback synapse from horizontal cells (HC) to cones. However, the exact retinal site was never determined. Using the electroretinogram and compound action potential recordings, we estimated the spectral sensitivity of the photoresponse of cones, the output of cones, and the optic nerve in rainbow trout. Recordings were performed before and following pharmacological inhibition of HC-cone feedback, and were repeated under two colored backgrounds to estimate the efficiency of color induction. No color induction could be detected in the photoresponse of cones. However, the efficiency of color induction in the cone output and optic nerve was substantial, with the efficiency in the optic nerve being significantly higher than in the cone output. We found that the efficiency of color induction in the cone output and optic nerve decreased significantly with the inhibition of HC-cone feedback. Therefore, our findings suggest not only that color induction originates as a result of HC-cone feedback, but also that this effect of HC-cone feedback is further amplified at downstream retinal elements, possibly through feedback mechanisms at the inner plexiform layer. This study provides evidence for an important role of HC-cone feedback in mediating color induction, and therefore, likely also in mediating color constancy.

Show MeSH
Related in: MedlinePlus