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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.

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HC-cone feedback does not affect the efficiency of color induction in the photoresponse of cones.(A,B) Spectral sensitivity of the photoresponse of cones measured from retina treated with saline and aspartate (S + ASP), and from retina treated with saline, aspartate and cobalt (S + ASP + Co). A sensitivity peak in the ultraviolet region (ca. 370 nm) in the S+ASP-treated retina disappeared following the application of cobalt. Error bars, ±1 SEM. Sample size: S + ASP: Natural = 5, LW adaptation = 5; S + ASP + Co: Natural = 5, LW adaptation = 4. (C) The efficiency of color induction, as indicated by the root mean square error (RMSE) between the spectral sensitivity under the two backgrounds, did not vary significantly with the application of cobalt that inhibits HC-cone feedback (denoted n.s.; see text for statistics). Box: mean (dashed), median (solid), 25th and 75th percentiles; whiskers: 10th and 90th percentiles.
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pone-0066216-g003: HC-cone feedback does not affect the efficiency of color induction in the photoresponse of cones.(A,B) Spectral sensitivity of the photoresponse of cones measured from retina treated with saline and aspartate (S + ASP), and from retina treated with saline, aspartate and cobalt (S + ASP + Co). A sensitivity peak in the ultraviolet region (ca. 370 nm) in the S+ASP-treated retina disappeared following the application of cobalt. Error bars, ±1 SEM. Sample size: S + ASP: Natural = 5, LW adaptation = 5; S + ASP + Co: Natural = 5, LW adaptation = 4. (C) The efficiency of color induction, as indicated by the root mean square error (RMSE) between the spectral sensitivity under the two backgrounds, did not vary significantly with the application of cobalt that inhibits HC-cone feedback (denoted n.s.; see text for statistics). Box: mean (dashed), median (solid), 25th and 75th percentiles; whiskers: 10th and 90th percentiles.

Mentions: To study the effect of HC-cone feedback on the efficiency of color induction in the photoresponse of cones, spectral sensitivity of the photoresponse of cones was measured by ERG from retina treated with saline (and ASP) as well as from retina treated with saline and cobalt (and ASP) (Figure 3A,B). The efficiency of color induction was defined as the extent by which two sensitivity spectra, obtained under the two backgrounds, differed. We used the root mean square error (RMSE) between the two sensitivity spectra as an index for this difference. See Methods for detailed description of estimation of the efficiency of 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)

HC-cone feedback does not affect the efficiency of color induction in the photoresponse of cones.(A,B) Spectral sensitivity of the photoresponse of cones measured from retina treated with saline and aspartate (S + ASP), and from retina treated with saline, aspartate and cobalt (S + ASP + Co). A sensitivity peak in the ultraviolet region (ca. 370 nm) in the S+ASP-treated retina disappeared following the application of cobalt. Error bars, ±1 SEM. Sample size: S + ASP: Natural = 5, LW adaptation = 5; S + ASP + Co: Natural = 5, LW adaptation = 4. (C) The efficiency of color induction, as indicated by the root mean square error (RMSE) between the spectral sensitivity under the two backgrounds, did not vary significantly with the application of cobalt that inhibits HC-cone feedback (denoted n.s.; see text for statistics). Box: mean (dashed), median (solid), 25th and 75th percentiles; whiskers: 10th and 90th percentiles.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3672170&req=5

pone-0066216-g003: HC-cone feedback does not affect the efficiency of color induction in the photoresponse of cones.(A,B) Spectral sensitivity of the photoresponse of cones measured from retina treated with saline and aspartate (S + ASP), and from retina treated with saline, aspartate and cobalt (S + ASP + Co). A sensitivity peak in the ultraviolet region (ca. 370 nm) in the S+ASP-treated retina disappeared following the application of cobalt. Error bars, ±1 SEM. Sample size: S + ASP: Natural = 5, LW adaptation = 5; S + ASP + Co: Natural = 5, LW adaptation = 4. (C) The efficiency of color induction, as indicated by the root mean square error (RMSE) between the spectral sensitivity under the two backgrounds, did not vary significantly with the application of cobalt that inhibits HC-cone feedback (denoted n.s.; see text for statistics). Box: mean (dashed), median (solid), 25th and 75th percentiles; whiskers: 10th and 90th percentiles.
Mentions: To study the effect of HC-cone feedback on the efficiency of color induction in the photoresponse of cones, spectral sensitivity of the photoresponse of cones was measured by ERG from retina treated with saline (and ASP) as well as from retina treated with saline and cobalt (and ASP) (Figure 3A,B). The efficiency of color induction was defined as the extent by which two sensitivity spectra, obtained under the two backgrounds, differed. We used the root mean square error (RMSE) between the two sensitivity spectra as an index for this difference. See Methods for detailed description of estimation of the efficiency of 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