Endogenous time of day-dependent modulation of brain activity and visual perception in humans

Earth’s rotation and the resulting day-night cycle of solar irradiance causes rhythmic changes in environmental conditions. The circadian system anticipates these predictable challenges and the brain integrates this information with homeostatic cues in order to time behavior accordingly. Humans highly depend on the visual system, which is most drastically affected by planetary rotation, with the most pronounced changes occurring during twilight. Yet, it is still unclear how visual perception and its underlying neural processes are modulated according to the time of day. We thus investigated human brain activity in constant dim light via the fMRI BOLD-signal during resting-state and a close-to-threshold visual detection task over 6 times of the day. BOLD-variability decreased endogenously at times of twilight in sensory cortices during resting-state and, even more, in the visual cortex during visual perception at these times. Furthermore, the visual cortex BOLD-variability reductions were associated with improved visual detection performance. In contrast, mean BOLD-activations related to visual perception were not significantly modulated by the time of day. In conclusion, these results imply that the visual cortex BOLD-variability reductions at times of twilight constitute a predictive mechanism facilitating visual perception to compensate for the degraded visual signal quality at these times. Individual chronotype and homeostatic sleep pressure explained part of the BOLD-variability modulation, suggesting a combined circadian and homeostatic regulation. Human activity usually extends into times of twilight, even in preindustrial societies. Therefore, anticipatory optimization of the visual system at twilight may have been crucial for survival and may still be relevant today whenever electric light is not available at these times. Moreover, the findings suggest that endogenous BOLD-variability reductions in sensory cortices constitute a novel general mechanism underlying enhanced close-to-threshold perception, further supporting the biological significance of BOLD-variability.