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Bright daytime light enhances circadian amplitude in a diurnal mammal

Beatriz Baño-Otálora,Franck P. Martial,C. Harding,D. Bechtold,Annette E. Allen,T. Brown,M. D. Belle,R. Lucas

Published 2021 in Proceedings of the National Academy of Sciences of the United States of America

ABSTRACT

Significance Light is an important regulator of endogenous circadian clocks. Regular light–dark cycles set circadian phase to ensure synchrony with external time, while irregular or inappropriate light exposure can disrupt circadian rhythms. We ask here whether light can also impact another key parameter of circadian rhythms, their amplitude, under conditions of stable entrainment. Using a diurnal rodent species and carefully calibrated light stimuli, we show that increasing the intensity of daytime light enhances the reproducibility and robustness of behavioral and physiological rhythms and increases the amplitude of circadian rhythms in electrical activity in the central brain pacemaker. These findings reveal an impact of light on circadian amplitude and highlight the potential importance of daytime light exposure for circadian health. Mammalian circadian rhythms are orchestrated by a master pacemaker in the hypothalamic suprachiasmatic nuclei (SCN), which receives information about the 24 h light–dark cycle from the retina. The accepted function of this light signal is to reset circadian phase in order to ensure appropriate synchronization with the celestial day. Here, we ask whether light also impacts another key property of the circadian oscillation, its amplitude. To this end, we measured circadian rhythms in behavioral activity, body temperature, and SCN electrophysiological activity in the diurnal murid rodent Rhabdomys pumilio following stable entrainment to 12:12 light–dark cycles at four different daytime intensities (ranging from 18 to 1,900 lx melanopic equivalent daylight illuminance). R. pumilio showed strongly diurnal activity and body temperature rhythms in all conditions, but measures of rhythm robustness were positively correlated with daytime irradiance under both entrainment and subsequent free run. Whole-cell and extracellular recordings of electrophysiological activity in ex vivo SCN revealed substantial differences in electrophysiological activity between dim and bright light conditions. At lower daytime irradiance, daytime peaks in SCN spontaneous firing rate and membrane depolarization were substantially depressed, leading to an overall marked reduction in the amplitude of circadian rhythms in spontaneous activity. Our data reveal a previously unappreciated impact of daytime light intensity on SCN physiology and the amplitude of circadian rhythms and highlight the potential importance of daytime light exposure for circadian health.

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