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.2019 Dec 16;29(24):4260-4267.e4.
doi: 10.1016/j.cub.2019.10.028.

Cones Support Alignment to an Inconsistent World by Suppressing Mouse Circadian Responses to the Blue Colors Associated with Twilight

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Cones Support Alignment to an Inconsistent World by Suppressing Mouse Circadian Responses to the Blue Colors Associated with Twilight

Joshua W Mouland et al. Curr Biol..

Abstract

In humans, short-wavelength light evokes larger circadian responses than longer wavelengths [1-3]. This reflects the fact that melanopsin, a key contributor to circadian assessments of light intensity, most efficiently captures photons around 480 nm [4-8] and gives rise to the popular view that "blue" light exerts the strongest effects on the clock. However, in the natural world, there is often no direct correlation between perceived color (as reported by the cone-based visual system) and melanopsin excitation. Accordingly, although the mammalian clock does receive cone-based chromatic signals [9], the influence of color on circadian responses to light remains unclear. Here, we define the nature and functional significance of chromatic influences on the mouse circadian system. Using polychromatic lighting and mice with altered cone spectral sensitivity (Opn1mwR), we generate conditions that differ in color (i.e., ratio of L- to S-cone opsin activation) while providing identical melanopsin and rod activation. When biased toward S-opsin activation (appearing "blue"), these stimuli reliably produce weaker circadian behavioral responses than those favoring L-opsin ("yellow"). This influence of color (which is absent in animals lacking cone phototransduction; Cnga3-/-) aligns with natural changes in spectral composition over twilight, where decreasing solar angle is accompanied by a strong blue shift [9-11]. Accordingly, we find that naturalistic color changes support circadian alignment when environmental conditions render diurnal variations in light intensity weak/ambiguous sources of timing information. Our data thus establish how color contributes to circadian entrainment in mammals and provide important new insight to inform the design of lighting environments that benefit health.

Keywords: color opponency; daylight; metamer; non-image-forming; photoentrainment; photoreceptor; suprachiasmatic.

Copyright © 2019 The Author(s). Published by Elsevier Ltd.. All rights reserved.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1
Color Modulates Circadian Assessment of Light Levels (A) Schematic of experimental paradigm (left), spectral composition of L−S+(blue) and L+S−(yellow) stimuli (mid), and opsin sensitivity curves (right) for red-cone mice with corresponding quantification for stimuli at maximum intensity (ND0). See also Figure S1 for additional details of stimulus design. (B) Representative actogram for red-cone mouse under constant L−S+(blue) or L+S−(yellow) illumination at 0.01, 0.1, and 1× intensity level shown in (A) (ND2–ND0, respectively). (C) Circadian period for red-cone mice under L−S+(blue) versus L+S−(yellow) illumination at varying intensity (n = 7–8/intensity). Data analyzed by two-way repeated measures (RM) ANOVA with Sidak’s post-tests: intensity, F2, 20 = 39.4; p < 0.001; color, F1, 20 = 11.7; p = 0.003; intensity × color, F2, 20 = 3.8; p = 0.04. (D) Activity bout duration (α), expressed as a fraction of circadian period length, for red-cone mice as above. Two-way RM ANOVA: intensity, F2, 20 = 17.0; p < 0.001; color, F1, 20 = 2.98; p = 0.10; intensity × color, F2, 20 = 0.1; p = 0.92. (E) Same as (B) but for coneless mouse. (F) Same as (C) but for coneless mice. Two-way RM ANOVA: intensity, F2, 14 = 31.3; p < 0.001; color, F1, 14 = 0.1; p = 0.82; intensity × color, F2, 14 = 2.6; p = 0.11. (G) Same as (D) for coneless mice (n = 5–6) mice. Two-way RM ANOVA: intensity, F2, 14 = 9.1; p = 0.003; color, F1, 14 = 2.4; p = 0.14; intensity × color, F2, 14 = 0.9; p = 0.44. (H) Spectral composition of stimuli that modulated cone illuminance (μ(L,S)) without changing color or melanopsin/rod excitation. (I) Representative actograms for two red-cone mice exposed to constant L+S−(yellow), L−S+(blue), L−S−(dim), and L+S+(bright) stimuli at ND1. (J) Circadian period determined for red-cone mice (n = 14) under the conditions illustrated in (I). Data analyzed by one-way RM ANOVA with Dunnett’s post-tests: F3,39 = 3.869; p = 0.016.∗p < 0.05,∗∗p < 0.01, and∗∗∗p < 0.001; ns = p > 0.05.
Figure 2
Figure 2
Color Modulates Re-entrainment following Jet Lag (A) Representative actogram for red-cone mouse under 12:12LD cycles and subsequently exposed to 6-h delays and advances where the light phase was rendered in L−S+(blue) or L+S−(yellow) at 0.1× intensity levels shown in Figure 1A. (B) Mean ± SEM phase change (mid-point between activity onsets and offsets, normalized to pre-shift average for each mouse) for red-cone mice (n = 8) during L−S+(blue) and L+S−(yellow) shifts. Data analyzed by two-way RM ANOVA with Sidak’s post-tests are shown. Delays (top panel): time, F16,112 = 103.5; p < 0.0001; color, F1, 7 = 24.2; p = 0.002; color × time, F16, 112 = 2.3, p = 0.007. Advances (bottom panel): time, F16,112 = 99.3; p < 0.0001; color, F1, 7 = 2.45; p = 0.16; color × time, F16, 112 = 1.7; p = 0.049. (C) Same as (A) but for coneless mouse. (D) Same as (B) but for coneless mice. Two-way RM ANOVA is shown. Delays (top panel; n = 7): time, F16, 96 = 143.8; p < 0.0001; color, F1, 6 = 5.17; p = 0.06; color × time, F16, 96 = 1.60; p = 0.08. Advances (bottom panel; n = 8): time, F16, 112 = 133.2; p < 0.0001; color, F1, 7 = 0.05; p = 0.84; color × time, F16, 112 = 0.56; p = 0.91.∗p < 0.05,∗∗p < 0.01, and∗∗∗p < 0.001, respectively; ns = p > 0.05. See also Figure S2 for details of responses to acute pulses of L−S+(blue) and L+S−(yellow) stimuli.
Figure 3
Figure 3
Color Is Not an Independent Timing Cue for the Circadian Clock (A) Representative passive infrared (PIR)-derived actograms for two red-cone mice transferred from 12:12LD to aligned L+S−:L−S+ (yellow:blue) or L−S+:L+S− (blue:yellow) cycles (spectra provided in Figure S3A). (B) Period of activity rhythms under LD and L+S−:L−S+ (yellow:blue; top) or L−S+:L+S− (blue:yellow; bottom). Data (n = 6 in both cases) are compared against an expected period of 24 h (one-sample t tests) and between conditions (paired t tests), showing an increase in period, above 24 h, in both cases. (C) PIR-derived actograms for two red-cone mice transferred from 12:12LD to aligned cycles providing modest daily changes in illumination just for melanopsin and rods (mel/rod; Figure S3B) or with superimposed changes in color (col+mel; Figure S3C). Note, two mice retained partial entrainment under col+mel (shown in left panel and Figure S3D) although other animals free ran with a long circadian period (representative example in right panel). (D) Period of activity rhythms under LD and subsequent mel/rod (top) or col+mel cycles (bottom). Data (n = 6 in both cases) are analyzed with one-sample t tests and paired t tests as above.∗∗∗p < 0.001. Spectral power distributions for all stimuli are provided in Figure S3.
Figure 4
Figure 4
Daily Changes in Color Support Stable Entrainment in the Face of Weather-Related Variation in Light Intensity (A) Schematic of the light exposure paradigm that included naturalistic changes in color and intensity with superimposed stochastic variations to simulate clouds. Left and right panels, respectively, provide quantification of apparent color and concurrent changes in light intensity; see Figure S4 for additional details of stimuli. (B) Representative PIR-derived actograms for a red-cone mouse under the lighting schedule shown in (A). Symbols adjacent to the traces indicate 24-h epochs that were used for subsequent analysis. (C) Mean ± SEM normalized activity waveforms for red-cone mice (n = 12) under days providing natural changes in color and intensity or matched intensity-only days. (D) Same as (C) but for 24-h epochs of constant dim illumination following natural or intensity-only days. (E–H) Quantification of rhythm robustness and stability for red-cone mice (n = 12) under natural or intensity-only days (diurnal) and subsequent constant routine (circadian), analyzed throughout by paired t test; (E) interdaily stability (diurnal: p = 0.02; circadian p = 0.001); (F) percent activity occurring during the “day”/projected day (diurnal: p = 0.004; circadian p = 0.0002); (G) intradaily variability (diurnal: p = 0.26; circadian = 0.02); (H) mean day-day correlation in activity patterns (diurnal: 0.025; circadian: 0.005). See STAR Methods for further details of analysis procedures.∗p < 0.05,∗∗p < 0.01, and∗∗∗p < 0.001.
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