Acute and Phase-Shifting Effects of Ocular and Extraocular Light in Human Circadian Physiology

Abstract

Light can influence physiology and performance of humans in two distinct ways. It can acutely change the level of physiological and behavioral parameters, and it can induce a phase shift in the circadian oscillators underlying variations in these levels. Until recently, both effects were thought to require retinal light perception. This view was challenged by Campbell and Murphy, who showed significant phase shifts in core body temperature and melatonin using an extraocular stimulus. Their study employed popliteal skin illumination and exclusively considered phase-shifting effects. In this paper, the authors explore both acute effects and phase-shifting effects of ocular as well as extraocular light. Twelve healthy males participated in a within-subject design and received all of three light conditions--(1) dim ocular light/no light to the knee, (2) dim ocular light/bright extraocular light to the knee, and (3) bright ocular light/no light to the knee--on separate nights in random order. The protocol consisted of an adaptation night followed by a 26-h period of sustained wakefulness, during which a 4-h light pulse was presented at a time when maximal phase delays were expected. The authors found neither immediate nor phase-shifting effects of extraocular light exposure on melatonin, core body temperature (CBT), or sleepiness. Ocular bright-light exposure reduced the nocturnal circadian drop in CBT, suppressed melatonin, and reduced sleepiness significantly. In addition, the 4-h ocular light pulse delayed the CBT rhythm by -55 min compared to the drift of the CBT rhythm in dim light. The melatonin rhythm shifted by -113 min, which differed significantly from the drift in the melatonin rhythm in the dim-light condition (-26 min). The failure to find immediate or phase-shifting effects in response to extraocular light in a within-subjects design in which effects of ocular bright light are confirmed strengthens the doubts raised by other labs of the impact of extraocular light on the human circadian system.

Nasal versus Temporal Illumination of the Human Retina: Effects on Core Body Temperature, Melatonin, and Circadian Phase

“…These findings are in contrast with earlier results on full-retinal bright-light exposure (Badia et al, 1991;Cajochen et al, 2000;Rüger et al, 2003), in which a reduction of sleepiness and a reduction of the circadian drop of CBT were associated with the suppression of melatonin. On the basis of our current results, we have to conclude that 100 lux of nasal and temporal illumination of the human retina is strong enough to significantly suppress melatonin but not strong enough to influence CBT or subjective sleepiness significantly.…”

“…On the one hand, nasal illumination resulted in a delay of the melatonin rhythm by -78 min, which falls into the range of delays obtained by full-retinal exposure to bright light during the night (Kubota et al, 2002;Rüger et al, 2003). On the other hand, we found no phase shift of the CBT rhythm in the nasal condition.…”

“…They also contribute to the pupillary light reflex Lucas et al, 2001;Lucas et al, 2003) and play an important role in the suppression of melatonin by light (Lucas et al, 1999). Suppression of melatonin itself is associated with reduced nighttime sleepiness (Cajochen et al, 2000;Rüger et al, 2003) and elevation of body temperature (Badia et al, 1991;French et al, 1990;Rüger et al, 2003).…”

Effects of Artificial Dawn on Subjective Ratings of Sleep Inertia and Dim Light Melatonin Onset

“…The activating effects of light have been shown to be present both during the night and daytime, indicating that melatonin suppression may not necessarily be a prerequisit to assert the effect Campbell et al, 1995;Phipps-Nelson et al, 2003;Rüger et al, 2003Rüger et al, , 2006. We hypothesize that this is the most likely mechanism by which complaints are reduced.…”

“…Lack of morning light during winter days may also worsen sleepinertia complaints due to the absence of the phase-advancing stimulus of morning light (Beersma & Daan, 1993;Gordijn et al, 1999;Honma & Honma, 1988;Khalsa et al, 2003;Minors et al, 1991) and the lack of its acute alerting effect Campbell et al, 1995;Rüger et al, 2003Rüger et al, , 2006. Because of the impact that sleep inertia may have in our society when high performance and alertness are required in the early morning, diminishing complaints of sleep inertia is of great interest.…”