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Distinct contributions of rod, cone, and melanopsin photoreceptors to encoding irradiance.

Lall GS, Revell VL, Momiji H, Al Enezi J, Altimus CM, Güler AD, Aguilar C, Cameron MA, Allender S, Hankins MW, Lucas RJ - Neuron (2010)

Bottom Line: These photoreceptors define circadian responses at very dim "scotopic" light levels but also at irradiances at which pattern vision relies heavily on cones.By contrast, cone input to irradiance responses dissipates following light adaptation to the extent that these receptors make a very limited contribution to circadian and pupillary light responses under these conditions.Our data provide new insight into retinal circuitry upstream of mRGCs and optimal stimuli for eliciting irradiance responses.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Life Sciences, AV Hill Building, University of Manchester, Manchester M13 9PT, UK.

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Cone Contributions to Defining Pupil Size(A) Sixty-second stimuli drove irradiance-dependent decreases in pupil size at both 500 and 650 nm in dark-adapted Opn1mwR mice (n = 4–12).(B) Wild-type mice also responded to both wavelengths, but were much less sensitive to 650 than 500 nm (n = 4–5).(C) Following correction of the 650 nm data from Opn1mwR mice to allow for the reduced sensitivity of cones to this wavelength versus 500 nm (irradiance of 650 nm stimuli × 0.13), the two irradiance response curves are superimposed at <1011 photons/cm2/s. F-test analysis reveals that sigmoidal curves fitted to these data sets differ (p < 0.01) in the best fit for their lower asymptote (nonoverlapping 95% confidence intervals), but not in other parameters.(D) There was no such convergence when irradiances were normalized according to the spectral sensitivity of rods or melanopsin.(E) As previously reported (Lucas et al., 2003), the pupillary responses of dark-adapted rd/rd cl mice elicited by 60 s 500 nm stimuli had a high threshold (n = 4–5).(F) A detailed examination of pupil size (n = 4) over the first 3 s of exposure (lights on at time = 0) to bright stimuli at 500 nm (2.2 × 1013 photons/cm2/s) and 650 nm (1.6 × 1014 photons/cm2/s) isoluminant for red cones revealed that, whereas the early rate of constriction was equivalent, responses at the two wavelengths diverged after ∼0.8 s. The response of wild-type mice to the longer wavelength was smaller and slower, confirming that the 650 nm response over these timescales relies on red cones. All data points show mean ± SEM pupil area normalized to prestimulus condition.
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fig2: Cone Contributions to Defining Pupil Size(A) Sixty-second stimuli drove irradiance-dependent decreases in pupil size at both 500 and 650 nm in dark-adapted Opn1mwR mice (n = 4–12).(B) Wild-type mice also responded to both wavelengths, but were much less sensitive to 650 than 500 nm (n = 4–5).(C) Following correction of the 650 nm data from Opn1mwR mice to allow for the reduced sensitivity of cones to this wavelength versus 500 nm (irradiance of 650 nm stimuli × 0.13), the two irradiance response curves are superimposed at <1011 photons/cm2/s. F-test analysis reveals that sigmoidal curves fitted to these data sets differ (p < 0.01) in the best fit for their lower asymptote (nonoverlapping 95% confidence intervals), but not in other parameters.(D) There was no such convergence when irradiances were normalized according to the spectral sensitivity of rods or melanopsin.(E) As previously reported (Lucas et al., 2003), the pupillary responses of dark-adapted rd/rd cl mice elicited by 60 s 500 nm stimuli had a high threshold (n = 4–5).(F) A detailed examination of pupil size (n = 4) over the first 3 s of exposure (lights on at time = 0) to bright stimuli at 500 nm (2.2 × 1013 photons/cm2/s) and 650 nm (1.6 × 1014 photons/cm2/s) isoluminant for red cones revealed that, whereas the early rate of constriction was equivalent, responses at the two wavelengths diverged after ∼0.8 s. The response of wild-type mice to the longer wavelength was smaller and slower, confirming that the 650 nm response over these timescales relies on red cones. All data points show mean ± SEM pupil area normalized to prestimulus condition.

Mentions: To confirm this finding and to provide a more detailed picture of cone contributions to defining pupil size, we next described full irradiance response relationships at 500 and 650 nm for the dark-adapted pupillary light reflex (PLR). In Opn1mwR mice there is a substantial divergence in relative sensitivity of melanopsin, rods, and red cones between these two wavelengths (Figure 1B). We found that irradiance response curves at 500 and 650 nm were remarkably similar for Opn1mwR, but not littermate wild-type, mice (Figures 2A and 2B). In fact, when corrected for the difference in red cone sensitivity at these two wavelengths (650 nm irradiance measures ×0.13), pupil responses became indistinguishable at irradiances <1011 photons/cm2/s in Opn1mwR mice (Figure 2C). By contrast, responses were highly divergent when correction factors based upon the relative sensitivity of either rods or melanopsin were applied (Figure 2D). This suggests that under these conditions red cones define the magnitude of pupil constriction in the range of ∼108–1011 photons/cm2/s. The lower limit of this range is ∼1 log unit below the reported threshold for cone-based vision in mice (Nathan et al., 2006), indicating that cone pathways presynaptic to mRGCs are at least as sensitive as those subserving pattern vision. The upper limit is probably defined by cone saturation, which similarly occurs around 3 log units above threshold for light steps in mice (Nikonov et al., 2006).


Distinct contributions of rod, cone, and melanopsin photoreceptors to encoding irradiance.

Lall GS, Revell VL, Momiji H, Al Enezi J, Altimus CM, Güler AD, Aguilar C, Cameron MA, Allender S, Hankins MW, Lucas RJ - Neuron (2010)

Cone Contributions to Defining Pupil Size(A) Sixty-second stimuli drove irradiance-dependent decreases in pupil size at both 500 and 650 nm in dark-adapted Opn1mwR mice (n = 4–12).(B) Wild-type mice also responded to both wavelengths, but were much less sensitive to 650 than 500 nm (n = 4–5).(C) Following correction of the 650 nm data from Opn1mwR mice to allow for the reduced sensitivity of cones to this wavelength versus 500 nm (irradiance of 650 nm stimuli × 0.13), the two irradiance response curves are superimposed at <1011 photons/cm2/s. F-test analysis reveals that sigmoidal curves fitted to these data sets differ (p < 0.01) in the best fit for their lower asymptote (nonoverlapping 95% confidence intervals), but not in other parameters.(D) There was no such convergence when irradiances were normalized according to the spectral sensitivity of rods or melanopsin.(E) As previously reported (Lucas et al., 2003), the pupillary responses of dark-adapted rd/rd cl mice elicited by 60 s 500 nm stimuli had a high threshold (n = 4–5).(F) A detailed examination of pupil size (n = 4) over the first 3 s of exposure (lights on at time = 0) to bright stimuli at 500 nm (2.2 × 1013 photons/cm2/s) and 650 nm (1.6 × 1014 photons/cm2/s) isoluminant for red cones revealed that, whereas the early rate of constriction was equivalent, responses at the two wavelengths diverged after ∼0.8 s. The response of wild-type mice to the longer wavelength was smaller and slower, confirming that the 650 nm response over these timescales relies on red cones. All data points show mean ± SEM pupil area normalized to prestimulus condition.
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fig2: Cone Contributions to Defining Pupil Size(A) Sixty-second stimuli drove irradiance-dependent decreases in pupil size at both 500 and 650 nm in dark-adapted Opn1mwR mice (n = 4–12).(B) Wild-type mice also responded to both wavelengths, but were much less sensitive to 650 than 500 nm (n = 4–5).(C) Following correction of the 650 nm data from Opn1mwR mice to allow for the reduced sensitivity of cones to this wavelength versus 500 nm (irradiance of 650 nm stimuli × 0.13), the two irradiance response curves are superimposed at <1011 photons/cm2/s. F-test analysis reveals that sigmoidal curves fitted to these data sets differ (p < 0.01) in the best fit for their lower asymptote (nonoverlapping 95% confidence intervals), but not in other parameters.(D) There was no such convergence when irradiances were normalized according to the spectral sensitivity of rods or melanopsin.(E) As previously reported (Lucas et al., 2003), the pupillary responses of dark-adapted rd/rd cl mice elicited by 60 s 500 nm stimuli had a high threshold (n = 4–5).(F) A detailed examination of pupil size (n = 4) over the first 3 s of exposure (lights on at time = 0) to bright stimuli at 500 nm (2.2 × 1013 photons/cm2/s) and 650 nm (1.6 × 1014 photons/cm2/s) isoluminant for red cones revealed that, whereas the early rate of constriction was equivalent, responses at the two wavelengths diverged after ∼0.8 s. The response of wild-type mice to the longer wavelength was smaller and slower, confirming that the 650 nm response over these timescales relies on red cones. All data points show mean ± SEM pupil area normalized to prestimulus condition.
Mentions: To confirm this finding and to provide a more detailed picture of cone contributions to defining pupil size, we next described full irradiance response relationships at 500 and 650 nm for the dark-adapted pupillary light reflex (PLR). In Opn1mwR mice there is a substantial divergence in relative sensitivity of melanopsin, rods, and red cones between these two wavelengths (Figure 1B). We found that irradiance response curves at 500 and 650 nm were remarkably similar for Opn1mwR, but not littermate wild-type, mice (Figures 2A and 2B). In fact, when corrected for the difference in red cone sensitivity at these two wavelengths (650 nm irradiance measures ×0.13), pupil responses became indistinguishable at irradiances <1011 photons/cm2/s in Opn1mwR mice (Figure 2C). By contrast, responses were highly divergent when correction factors based upon the relative sensitivity of either rods or melanopsin were applied (Figure 2D). This suggests that under these conditions red cones define the magnitude of pupil constriction in the range of ∼108–1011 photons/cm2/s. The lower limit of this range is ∼1 log unit below the reported threshold for cone-based vision in mice (Nathan et al., 2006), indicating that cone pathways presynaptic to mRGCs are at least as sensitive as those subserving pattern vision. The upper limit is probably defined by cone saturation, which similarly occurs around 3 log units above threshold for light steps in mice (Nikonov et al., 2006).

Bottom Line: These photoreceptors define circadian responses at very dim "scotopic" light levels but also at irradiances at which pattern vision relies heavily on cones.By contrast, cone input to irradiance responses dissipates following light adaptation to the extent that these receptors make a very limited contribution to circadian and pupillary light responses under these conditions.Our data provide new insight into retinal circuitry upstream of mRGCs and optimal stimuli for eliciting irradiance responses.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Life Sciences, AV Hill Building, University of Manchester, Manchester M13 9PT, UK.

Show MeSH
Related in: MedlinePlus