Properties of mutual coupling between the two circadian pacemakers in the eyes of the mollusc Bulla gouldiana.

We examined, in vitro, the effects of changing the free-running period (tau) of one oscillator on the phase relationship between the circadian rhythms of impulse activity in the optic nerves that are driven by the bilaterally paired ocular pacemakers in Bulla gouldiana. One eye of the coupled pair was treated either with lithium artificial seawater (to lengthen tau) or with low-chloride artificial seawater (to shorten tau). The results suggested that the coupling is relatively weak, since the majority (9 to 16) of eyes were unable to maintain a stable phase relationship when tau differences between the eyes were only about 1 hr. When stable phase differences were achieved, the tau of the coupled system was intermediate between the tau's of the individual oscillators, and the eye with the shorter intrinsic tau would invariably phase-lead the pair. Interestingly, in a few instances, pairs of eyes that had desynchronized by 9.5-10.5 hr resynchronized within a single cycle via a massive phase advance in the rhythm from the phase-lagging eye. The result suggests the existence of a novel phase-shifting mechanism that is part of the mutual coupling pathway. We found evidence that connection of the eye with the cerebral ganglion increases the tau of the ocular pacemaker, suggesting that efferent signals from the central nervous system influence tau. These signals may also modulate the phase-shifting response.