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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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Background illumination conditions, and absorbance spectra and quantum catch of cone pigments in rainbow trout.(A) Two background illumination conditions were used, a broad-spectrum ‘Natural’ background and a long wavelength (LW) adaptation background. The broad-spectrum background simulated the fish natural photic environment by reproducing the sideward irradiance measured at a depth of 3 m at Lake Cowichan, Vancouver Island, BC, Canada (root mean square error = 0.38 log photons cm−2 s−1; Pearson r = 0.94). The LW adaptation background was designed to dampen the sensitivity of the LWS cone mechanism. (B) Absorbance spectra of the cone pigment classes in rainbow trout. Based on the range of photoreceptor sensitivity, absorbance spectra were constructed while assuming visual pigments are of A1 chromophore. (C) The number of photons collected by the various cone pigment classes under the background conditions used, as estimated using a quantum catch model. (D) The ratio between the quantum catch (QC) of pigments under the LW adaptation and Natural backgrounds was highest for LWS, indicating that LWS is the pigment being adapted most extensively under the LW adaptation compared to the Natural background.
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pone-0066216-g002: Background illumination conditions, and absorbance spectra and quantum catch of cone pigments in rainbow trout.(A) Two background illumination conditions were used, a broad-spectrum ‘Natural’ background and a long wavelength (LW) adaptation background. The broad-spectrum background simulated the fish natural photic environment by reproducing the sideward irradiance measured at a depth of 3 m at Lake Cowichan, Vancouver Island, BC, Canada (root mean square error = 0.38 log photons cm−2 s−1; Pearson r = 0.94). The LW adaptation background was designed to dampen the sensitivity of the LWS cone mechanism. (B) Absorbance spectra of the cone pigment classes in rainbow trout. Based on the range of photoreceptor sensitivity, absorbance spectra were constructed while assuming visual pigments are of A1 chromophore. (C) The number of photons collected by the various cone pigment classes under the background conditions used, as estimated using a quantum catch model. (D) The ratio between the quantum catch (QC) of pigments under the LW adaptation and Natural backgrounds was highest for LWS, indicating that LWS is the pigment being adapted most extensively under the LW adaptation compared to the Natural background.

Mentions: Spectral sensitivity was measured under two different background illumination conditions. To evaluate the spectral sensitivity under natural photic conditions, measurements were conducted under a broad-spectrum background illumination that accurately reproduced the natural photic conditions encountered at the native environment of rainbow trout (‘Natural background’). Spectral sensitivity was also measured under background illumination that selectively adapted the LWS cones (‘long wavelength (LW)-adaptation background’). Figure 2 shows the spectral irradiance of the background conditions used, the absorbance spectra of cone pigments in rainbow trout, and the quantum catch for each cone pigment under both backgrounds.


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)

Background illumination conditions, and absorbance spectra and quantum catch of cone pigments in rainbow trout.(A) Two background illumination conditions were used, a broad-spectrum ‘Natural’ background and a long wavelength (LW) adaptation background. The broad-spectrum background simulated the fish natural photic environment by reproducing the sideward irradiance measured at a depth of 3 m at Lake Cowichan, Vancouver Island, BC, Canada (root mean square error = 0.38 log photons cm−2 s−1; Pearson r = 0.94). The LW adaptation background was designed to dampen the sensitivity of the LWS cone mechanism. (B) Absorbance spectra of the cone pigment classes in rainbow trout. Based on the range of photoreceptor sensitivity, absorbance spectra were constructed while assuming visual pigments are of A1 chromophore. (C) The number of photons collected by the various cone pigment classes under the background conditions used, as estimated using a quantum catch model. (D) The ratio between the quantum catch (QC) of pigments under the LW adaptation and Natural backgrounds was highest for LWS, indicating that LWS is the pigment being adapted most extensively under the LW adaptation compared to the Natural background.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3672170&req=5

pone-0066216-g002: Background illumination conditions, and absorbance spectra and quantum catch of cone pigments in rainbow trout.(A) Two background illumination conditions were used, a broad-spectrum ‘Natural’ background and a long wavelength (LW) adaptation background. The broad-spectrum background simulated the fish natural photic environment by reproducing the sideward irradiance measured at a depth of 3 m at Lake Cowichan, Vancouver Island, BC, Canada (root mean square error = 0.38 log photons cm−2 s−1; Pearson r = 0.94). The LW adaptation background was designed to dampen the sensitivity of the LWS cone mechanism. (B) Absorbance spectra of the cone pigment classes in rainbow trout. Based on the range of photoreceptor sensitivity, absorbance spectra were constructed while assuming visual pigments are of A1 chromophore. (C) The number of photons collected by the various cone pigment classes under the background conditions used, as estimated using a quantum catch model. (D) The ratio between the quantum catch (QC) of pigments under the LW adaptation and Natural backgrounds was highest for LWS, indicating that LWS is the pigment being adapted most extensively under the LW adaptation compared to the Natural background.
Mentions: Spectral sensitivity was measured under two different background illumination conditions. To evaluate the spectral sensitivity under natural photic conditions, measurements were conducted under a broad-spectrum background illumination that accurately reproduced the natural photic conditions encountered at the native environment of rainbow trout (‘Natural background’). Spectral sensitivity was also measured under background illumination that selectively adapted the LWS cones (‘long wavelength (LW)-adaptation background’). Figure 2 shows the spectral irradiance of the background conditions used, the absorbance spectra of cone pigments in rainbow trout, and the quantum catch for each cone pigment under both backgrounds.

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