Transplantation of a circadian pacemaker in Drosophila

Abstract

A MAJOR question in the physiology of activity rhythms is the nature of the coupling between the pacemaker and the motor system. There is good evidence for humoral coupling in several species. In the sparrow, pineal organs from donor birds maintained in a light–dark cycle different from that of the host were transplanted into the anterior chamber of the eye of recipient birds made arrhythmic by pinealectomy. In this case the activity rhythm of the host was restored and its phase was determined by a diffusible humoral factor from the implanted pineal1. In the mollusc Aplysia humoral coupling between the circadian pacemaker and the output cells is thought to control locomotor activity, although electrical coupling has not been ruled out2. In insects, however, experiments involving cockroaches and silkmoths indicate that an intact electrical connection between the brain and thoracic ganglia is required for rhythmic activity. The pacemaker controlling the locomotor activity rhythm in the cockroach appears to reside in the optic lobes, and disruption of the electrical pathway between the optic lobes and thoracic ganglia results in arrhythmicity3–6. Initial transplant experiments with this insect indicated that activity could be hormonally controlled by the sub-oesophageal ganglion7. While these results have not been repeatable by other laboratories8–10, evidence from parabiosis experiments does suggest some humoral influence on the activity rhythm11. Surgical experiments using giant silkmoths have also demonstrated the need for an intact neural connection between brain and thorax for expression of the flight activity rhythm12. Thus, until now, there has been no unambiguous evidence for humoral control of activity rhythms in insects. Here we show that a short-period mutant brain can produce a short-period activity rhythm when implanted into the abdomen of a genetically arrhythmic host. In this instance, there were no functional neural connections between the implanted brain and the locomotor system of the recipient, so the action of the brain must be mediated by humoral influences.