Integration of color and intensity increases time signal stability for the human circadian system when sunlight is obscured by clouds

Abstract

The mammalian circadian system encodes both absolute levels of light intensity and color to phase-lock (entrain) its rhythm to the 24-h solar cycle. The evolutionary benefits of circadian color-coding over intensity-coding per se are yet far from understood. A detailed characterization of sunlight is crucial in understanding how and why circadian photoreception integrates color and intensity information. To this end, we continuously measured 100 days of sunlight spectra over the course of a year. Our analyses suggest that circadian color-coding may have evolved to cope with cloud-induced variation in light intensity. We proceed to show how an integration of intensity and spectral composition reduces day-to-day variability in the synchronizing signal (Zeitgeber). As a consequence, entrained phase angle of the circadian clock will be more stable, which will be beneficial for the organism. The presented characterization of sunlight dynamics may become important in designing lighting solutions aimed at minimizing the detrimental effects of light at night in modern societies.

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

“…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, 10, 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.…”

“…An especially pertinent question, however, is whether the effects of color described here extend to other mammals, such as humans. The qualitative relationship between sun position and blue-yellow color should be retained for any mammal capable of color vision [12], and theoretical studies suggest that color could aid circadian entrainment in humans [11]. Existing evidence for color opponency in primate ipRGCs and melanopsin-dependent responses in man [37, 38, 39, 40] give further reasons to believe that the effects of color reported here could extend also to humans.…”

“…Accordingly, although we do not discount the idea that some animals use color to help entrainment under such conditions, it seems unlikely that this is the primary role of color input to the clock for most mammals. Instead, a more globally relevant potential benefit of using color is to compensate for stochastic fluctuations in the diurnal rhythm of light intensity, e.g., due to variations in cloud cover [11, 12].…”

“…Clouds can reduce ambient light levels by >10-fold, rendering the timing of sunrise/sunset ambiguous for a system that relies simply on light intensity. The twilight blue shift, however, is retained irrespective of clouds [9, 10, 11]. To test whether this color information buffers clock entrainment against weather-related changes in illumination, we designed an experimental paradigm to provide naturalistic cycles of color and/or light intensity that incorporated stochastic variations to simulate the impact of clouds (Figure 4A).…”

Reconciling Color Vision Models With Midget Ganglion Cell Receptive Fields

“…For example, the amount of illumination from blue sky light relative to direct sunlight changes throughout the day. As a result, the illuminant color can vary from blue to yellow (Foster, 2011; Pauers et al, 2012; Spitschan et al, 2016; Woelders et al, 2018). The ideal receptive fields for serving hue perception would be designed to help extract surface spectral reflectance independent of the illuminant.…”