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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 Input to the PLR Is Reduced under Light-Adapted Conditions(A) Pre-exposure to 5 min 644 nm (1013 photons/cm2/s) substantially reduced pupillary responses (mean ± SEM; n = 6–7) to 10 s stimuli of equivalent or even higher irradiance (open circles) compared to those obtained following 1 hr of dark adaptation (closed circles).(B) Under more extensive adaptation (15 min 1.2 × 1015 photons/cm2/s; “Light”), pupil responses were completely absent throughout 30 s of exposure to a 650 nm test stimulus (2 × 1014 photons/cm2/s; hatched columns) capable of driving strong constriction under dark-adapted conditions (“Dark”). By contrast the response to an equivalent 500 nm (2 × 1013 photons/cm2/s; solid columns) test stimulus was unaffected. One-way ANOVA, p < 0.0001; selected post hoc tests with Tukey's correction shown, ∗∗∗p < 0.001; ns, p > 0.05.(C) The degree to which responses to the 30 s 650 nm test stimulus were inhibited was dependent upon the duration of prior light exposure (one-way ANOVA, p < 0.0001), although all exposures >15 s significantly impaired responses when compared with those of dark-adapted animals (Dunnett's post hoc comparisons, p < 0.01; n = 5–7).(D) Responsiveness to a 15 s 650 nm test stimulus (1.8 × 1014 photons/cm2/s) recovered over the course of 1 hr of dark adaptation (one-way ANOVA, p < 0.001; Dunnett's post hoc comparisons, p < 0.05, versus 0.1 min dark adaptation for times >1 min; n = 5–7).(E) Pre-exposure of rd/rd cl mice to 500 nm light (1.4 × 1014 photons/cm2/s) for either 5 or 60 min induced more classical light adaptation comprising a simple reduction in sensitivity to a subsequent 10 s 500 nm test pulse. All data points show mean ± SEM pupil area normalized to prestimulus condition.
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fig5: Cone Input to the PLR Is Reduced under Light-Adapted Conditions(A) Pre-exposure to 5 min 644 nm (1013 photons/cm2/s) substantially reduced pupillary responses (mean ± SEM; n = 6–7) to 10 s stimuli of equivalent or even higher irradiance (open circles) compared to those obtained following 1 hr of dark adaptation (closed circles).(B) Under more extensive adaptation (15 min 1.2 × 1015 photons/cm2/s; “Light”), pupil responses were completely absent throughout 30 s of exposure to a 650 nm test stimulus (2 × 1014 photons/cm2/s; hatched columns) capable of driving strong constriction under dark-adapted conditions (“Dark”). By contrast the response to an equivalent 500 nm (2 × 1013 photons/cm2/s; solid columns) test stimulus was unaffected. One-way ANOVA, p < 0.0001; selected post hoc tests with Tukey's correction shown, ∗∗∗p < 0.001; ns, p > 0.05.(C) The degree to which responses to the 30 s 650 nm test stimulus were inhibited was dependent upon the duration of prior light exposure (one-way ANOVA, p < 0.0001), although all exposures >15 s significantly impaired responses when compared with those of dark-adapted animals (Dunnett's post hoc comparisons, p < 0.01; n = 5–7).(D) Responsiveness to a 15 s 650 nm test stimulus (1.8 × 1014 photons/cm2/s) recovered over the course of 1 hr of dark adaptation (one-way ANOVA, p < 0.001; Dunnett's post hoc comparisons, p < 0.05, versus 0.1 min dark adaptation for times >1 min; n = 5–7).(E) Pre-exposure of rd/rd cl mice to 500 nm light (1.4 × 1014 photons/cm2/s) for either 5 or 60 min induced more classical light adaptation comprising a simple reduction in sensitivity to a subsequent 10 s 500 nm test pulse. All data points show mean ± SEM pupil area normalized to prestimulus condition.

Mentions: We first explored the effects of prior treatment with 644 nm on subsequent cone-dependent pupillary responses in Opn1mwR mice. We found that 5 min of exposure to 1013 photons/cm2/s of 644 nm light greatly reduced pupil responses to a subsequent 650 nm test stimulus of equivalent irradiance (Figure 5A). Higher test irradiances drove larger constrictions, but the response magnitude was always substantially smaller than that elicited by an equivalent stimulus under dark-adapted conditions (Figure 5A). More extensive light exposure (15 min 1.2 × 1015 photons/cm2/s 644 nm) rendered the pupil entirely refractory to irradiances (1014 photons/cm2/s 650 nm) that drove large constrictions when dark-adapted (Figure 5B). To trace the kinetics of this effect, we assessed responses to the 650 nm test stimulus after 15 s, 30 s, 1 min, and 15 min exposure to 644 nm at 1.2 × 1015 photons/cm2/s. A significant decrease in response amplitude was observed at all exposure times bar the shortest, but only after 15 min were the animals entirely refractory to the 650 nm test pulse (Figure 5C). We traced dark adaptation as defined by the recovery of responses to the test stimulus following exposure to 15 min of 1.2 × 1015 photons/cm2/s 644 nm. This was also slow, with full recovery taking up to 1 hr (Figure 5D). Importantly, this did not reflect a general decrease in pupillary responsiveness because constrictions to 500 nm test stimuli survived even the brightest 644 nm pretreatment (Figure 5B). These data suggest that prior light exposure over timescales ranging from tens of seconds to tens of minutes reduces the ability of cones to regulate pupil size.


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 Input to the PLR Is Reduced under Light-Adapted Conditions(A) Pre-exposure to 5 min 644 nm (1013 photons/cm2/s) substantially reduced pupillary responses (mean ± SEM; n = 6–7) to 10 s stimuli of equivalent or even higher irradiance (open circles) compared to those obtained following 1 hr of dark adaptation (closed circles).(B) Under more extensive adaptation (15 min 1.2 × 1015 photons/cm2/s; “Light”), pupil responses were completely absent throughout 30 s of exposure to a 650 nm test stimulus (2 × 1014 photons/cm2/s; hatched columns) capable of driving strong constriction under dark-adapted conditions (“Dark”). By contrast the response to an equivalent 500 nm (2 × 1013 photons/cm2/s; solid columns) test stimulus was unaffected. One-way ANOVA, p < 0.0001; selected post hoc tests with Tukey's correction shown, ∗∗∗p < 0.001; ns, p > 0.05.(C) The degree to which responses to the 30 s 650 nm test stimulus were inhibited was dependent upon the duration of prior light exposure (one-way ANOVA, p < 0.0001), although all exposures >15 s significantly impaired responses when compared with those of dark-adapted animals (Dunnett's post hoc comparisons, p < 0.01; n = 5–7).(D) Responsiveness to a 15 s 650 nm test stimulus (1.8 × 1014 photons/cm2/s) recovered over the course of 1 hr of dark adaptation (one-way ANOVA, p < 0.001; Dunnett's post hoc comparisons, p < 0.05, versus 0.1 min dark adaptation for times >1 min; n = 5–7).(E) Pre-exposure of rd/rd cl mice to 500 nm light (1.4 × 1014 photons/cm2/s) for either 5 or 60 min induced more classical light adaptation comprising a simple reduction in sensitivity to a subsequent 10 s 500 nm test pulse. All data points show mean ± SEM pupil area normalized to prestimulus condition.
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fig5: Cone Input to the PLR Is Reduced under Light-Adapted Conditions(A) Pre-exposure to 5 min 644 nm (1013 photons/cm2/s) substantially reduced pupillary responses (mean ± SEM; n = 6–7) to 10 s stimuli of equivalent or even higher irradiance (open circles) compared to those obtained following 1 hr of dark adaptation (closed circles).(B) Under more extensive adaptation (15 min 1.2 × 1015 photons/cm2/s; “Light”), pupil responses were completely absent throughout 30 s of exposure to a 650 nm test stimulus (2 × 1014 photons/cm2/s; hatched columns) capable of driving strong constriction under dark-adapted conditions (“Dark”). By contrast the response to an equivalent 500 nm (2 × 1013 photons/cm2/s; solid columns) test stimulus was unaffected. One-way ANOVA, p < 0.0001; selected post hoc tests with Tukey's correction shown, ∗∗∗p < 0.001; ns, p > 0.05.(C) The degree to which responses to the 30 s 650 nm test stimulus were inhibited was dependent upon the duration of prior light exposure (one-way ANOVA, p < 0.0001), although all exposures >15 s significantly impaired responses when compared with those of dark-adapted animals (Dunnett's post hoc comparisons, p < 0.01; n = 5–7).(D) Responsiveness to a 15 s 650 nm test stimulus (1.8 × 1014 photons/cm2/s) recovered over the course of 1 hr of dark adaptation (one-way ANOVA, p < 0.001; Dunnett's post hoc comparisons, p < 0.05, versus 0.1 min dark adaptation for times >1 min; n = 5–7).(E) Pre-exposure of rd/rd cl mice to 500 nm light (1.4 × 1014 photons/cm2/s) for either 5 or 60 min induced more classical light adaptation comprising a simple reduction in sensitivity to a subsequent 10 s 500 nm test pulse. All data points show mean ± SEM pupil area normalized to prestimulus condition.
Mentions: We first explored the effects of prior treatment with 644 nm on subsequent cone-dependent pupillary responses in Opn1mwR mice. We found that 5 min of exposure to 1013 photons/cm2/s of 644 nm light greatly reduced pupil responses to a subsequent 650 nm test stimulus of equivalent irradiance (Figure 5A). Higher test irradiances drove larger constrictions, but the response magnitude was always substantially smaller than that elicited by an equivalent stimulus under dark-adapted conditions (Figure 5A). More extensive light exposure (15 min 1.2 × 1015 photons/cm2/s 644 nm) rendered the pupil entirely refractory to irradiances (1014 photons/cm2/s 650 nm) that drove large constrictions when dark-adapted (Figure 5B). To trace the kinetics of this effect, we assessed responses to the 650 nm test stimulus after 15 s, 30 s, 1 min, and 15 min exposure to 644 nm at 1.2 × 1015 photons/cm2/s. A significant decrease in response amplitude was observed at all exposure times bar the shortest, but only after 15 min were the animals entirely refractory to the 650 nm test pulse (Figure 5C). We traced dark adaptation as defined by the recovery of responses to the test stimulus following exposure to 15 min of 1.2 × 1015 photons/cm2/s 644 nm. This was also slow, with full recovery taking up to 1 hr (Figure 5D). Importantly, this did not reflect a general decrease in pupillary responsiveness because constrictions to 500 nm test stimuli survived even the brightest 644 nm pretreatment (Figure 5B). These data suggest that prior light exposure over timescales ranging from tens of seconds to tens of minutes reduces the ability of cones to regulate pupil size.

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