Chromatic clocks: Color opponency in non-image-forming visual function

Abstract

During dusk and dawn, the ambient illumination undergoes drastic changes in irradiance (or intensity) and spectrum (or color). While the former is a well-studied factor in synchronizing behavior and physiology to the earth’s 24-h rotation, color sensitivity in the regulation of circadian rhythms has not been systematically studied. Drawing on the concept of color opponency, a well-known property of image-forming vision in many vertebrates (including humans), we consider how the spectral shifts during twilight are encoded by a color-opponent sensory system for non-image-forming (NIF) visual functions, including phase shifting and melatonin suppression. We review electrophysiological evidence for color sensitivity in the pineal/parietal organs of fish, amphibians and reptiles, color coding in neurons in the circadian pacemaker in mice as well as sporadic evidence for color sensitivity in NIF visual functions in birds and mammals. Together, these studies suggest that color opponency may be an important modulator of light-driven physiological and behavioral responses.

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

“…Therefore, the more erratic the light intensity profile is compared to solar angle-induced changes in light intensity, the more beneficial it may become to integrate parametric entrainment and circadian color-coding. Finally, as was discussed in the introduction, an additional hypothesis is that circadian color-coding may allow for common-mode noise rejection mechanisms 10 , such that the circadian system is buffered against behavior-induced changes in perceived intensity that are accompanied by changes in color (for example an animal moving in and out of vegetation shade).…”

“…Such noise is partially accounted for by integrating light intensities over time, resulting in low-pass filtering of the Zeitgeber signal 9 . Another possible strategy by which such changes may be accounted for is through common-node noise rejection 10 , by making use of another signal that normalizes for such changes, such as color (unlike intensity changes by burrow visits 8 , color and intensity may change in concert when moving in and out of vegetation shade, such that the perceived change in color may be used to correct for the perceived change in intensity). Importantly, not only behavior induces Zeitgeber noise, but also external factors such as cloud cover impact the perceived intensity of sunlight, which will be the main focus of the work presented here.…”

“…For example, during an overcast evening following clear-sky days, the delaying effect of light will be smaller than usual, which would cause an unwanted advance. It has therefore been proposed that circadian systems have evolved color-vision to obtain a more accurate indication of solar time 8 , 10 – 14 . This is plausible, as wavelength-dependent photon scattering in the atmosphere depends on solar angle, such that distinct changes in the color of the sky may be observed around dusk and dawn 15 .…”

Color opponency with a single kind of bistable opsin in the zebrafish pineal organ

“…In contrast to the two-opsin system involving parietopsin, the chromatic mechanism involving parapinopsin alone in the zebrafish pineal organ may not be suitable for detecting dawn and dusk. Light intensity at these times [e.g., irradiance of 0.1 W/m 2 or less ( 25 ), ∼3% brightness of the white light used in Fig. 4 ] is not sufficiently strong to form a photoequilibrium between the two states, which is essential for generating color opponency via this mechanism.…”

Direct effects of the light environment on daily neuroendocrine control

“…On the other hand, at least some ipRGCs (in both rodents and primates) exhibit evidence of opponent processing of signals that originate from different classes of cone photoreceptors (Dacey et al 2005, Stabio et al 2018. This mechanism (equivalent to that which supports our ability to discriminate blue/ yellow colours) thus renders those ipRGCs capable of detecting changes in the spectral composition ('colour') of light, such as those occurring during natural twilight (Walmsley et al 2015, Spitschan et al 2017.…”