Ocular clocks are tightly coupled and act as pacemakers in the circadian system of Japanese quail

Abstract

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.

Dynamics of Three Coupled Van der Pol Oscillators With Application to Circadian Rhythms

“…Complete removal of the eyes causes loss of rhythmicity of body temperature in Japanese quail, a rhythm thought to be controlled by the SCN [10]. Thus the eyes appear to be essential to the sustainment of circadian rhythms in the SCN in this species.…”

“…Recent experiments [10] have strengthened the conclusion that the circadian rhythms present in the eyes are the central pacemakers for the entire circadian system in Their experiments showed that when Japanese quail are placed in constant darkness (representing an autonomous system with no external forcing), the level of melatonin in their two eyes are found to be in phase after a period of more than 40 days. Furthermore, experiments showed that this in-phase stability is robust and seems to hold for a wide range of initial conditions, even, e.g., if the two eyes are initially light-loaded to be out of phase.…”

“…In the pigeon, both pinealectomy and eye removal are necessary to abolish overt behavior rhythms. In the quail, eye removal alone causes arrhythmia in body temperature [10].…”

“…First, the pineal gland and the SCN have been conjectured to be joined together in a "neuroendocrine loop" [3] in which "a daily melatonin output from the pineal is required to maintain rhythmicity in the SCN, and a daily neural output from the SCN is required to maintain rhythmicity in the pineal." [10] This relationship between the pineal and SCN is mutually inhibitory -during night the pineal produces and secretes melatonin into the bloodstream which inhibits SCN activity and during the day the SCN inhibits the pineal through neural signals. From this model we can expect the pineal and SCN rhythms to be 180 degrees out-of-phase.…”

“…Most likely this is accomplished via both neural (the nature of which is still unknown) and hormonal outputs. Evidence suggesting a hormonal component includes the fact that severing the optic nerve only produces arrhythmia in approximately 25% of Japanese quail undergoing the procedure [10].…”