All organisms exhibit significant daily rhythms in a myriad of functions from molecular levels to the level of the whole organism. Significantly, most of these rhythms will persist under constant conditions, showing that they are driven by an internal circadian clock. In birds the circadian system is composed of several interacting sites, each of which may contain a circadian clock. These sites include the pineal organ, the suprachiasmatic nucleus (SCN) of the hypothalamus, and, in some species, the eyes. Light is the most powerful entraining stimulus for circadian rhythms and, in birds, light can affect the system via three different pathways: the eyes, the pineal, and extraretinal photoreceptors located in the deep brain. Circadian pacemakers in the pineal and in the eyes of some avian species communicate with the hypothalamic pacemakers via the rhythmic synthesis and release of the hormone melatonin. Often the hypothalamic pacemakers are unable to sustain persistent rhythmicity in constant conditions in the absence of periodic melatonin input from the pineal (or eyes). It has also been proposed that pineal pacemakers may be unable to sustain rhythmicity in constant conditions without periodic neural input from the SCN. Significant variation can occur among birds in the relative roles that the pineal, the SCN, and the eyes play within the circadian system; for example, in the house sparrow pacemakers in the pineal play the predominant role, in the pigeon circadian pacemakers in both the pineal and eyes play a significant role, and in Japanese quail ocular pacemakers play the predominant role.

Our previous studies showed that the eyes of Japanese quail contain a biological clock that drives a daily rhythm of melatonin synthesis. Furthermore, we hypothesized that these ocular clocks are pacemakers because eye removal abolishes freerunning rhythms in constant darkness (DD). If the eyes are indeed acting as pacemakers, we predicted that the two ocular pacemakers in an individual bird must remain in phase in DD and, furthermore, the two ocular pacemakers would rapidly regain coupling after being forced out of phase. These predictions were confirmed by demonstrating that 1) the ocular melatonin rhythms of the two eyes maintained phase for at least 57 days in DD and 2) after ocular pacemakers were forced out of phase by alternately patching the eyes in constant light, two components of body temperature were observed that fused into a consolidated rhythm after 5-6 days in DD, showing pacemaker recoupling. The ability to maintain phase in DD and rapidly recouple after out-of-phase entrainment demonstrates that the eyes are strongly coupled pacemakers that work in synchrony to drive circadian rhythmicity in Japanese quail.

Previous studies have shown that the circadian system of Japanese quail is composed of multiple photic inputs and multiple oscillators. Among these are extraretinal photoreceptors that mediate both circadian and photoperiodic responses and circadian pacemakers in the eyes that, via neural and hormonal outputs, help to maintain rhythmicity of central circadian clocks (presumably located in the suprachiasmatic area of the hypothalamus). Furthermore, a component of the central circadian system is influenced by reproductive hormones. Under certain conditions, the circadian system of female quail can be induced to split into two circadian components: one driven by ocular pacemakers and one driven by feedback from reproductive hormones. Importantly, ovulation is either inhibited or permitted as these two oscillators (or sets of oscillators) constantly change internal phase relationships with each other, suggesting an "internal coincidence" mechanism in the control of ovulation. The oviposition patterns of quail in light-dark (LD) cycles also support an internal coincidence mechanism. The authors tested the hypothesis that the ocular pacemakers are an important component of an internal coincidence mechanism controlling ovulation by examinig the effects of blinding by complete eye removal (EX), and the effects of eye-patching, on the body temperature and oviposition patterns of quail exposed to 24-h LD cycles. They also examined the effects of EX on quail exposed to continuous light (LL) and to continuous darkness (DD). Neither EX nor eye-patching affected the oviposition patterns of birds in LD. Furthermore, robust body temperature and oviposition rhythms continued in EX birds in LL, but body temperature became arrhythmic in DD with the cessation of ovulation. The results do not show a role for ocular pacemakers in the control of ovulation, but they do support the hypotheses that (1) entrainment of the central oscillators by extraretinally perceived light is sufficient to preserve a normal ovulatory pattern in LD in the absence of the ocular pacemakers, and (2) in LL, feedback of reproductive hormones onto the central oscillators is sufficient to organize the circadian system even in the absence of the ocular pacemakers. Whether or not the ocular pacemakers are normally involved in the control of ovulation is still an open question.

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