Transient membrane shedding in Limulus photoreceptors: control mechanisms under natural lighting

Abstract

Photoreceptors of the Limulus lateral eye shed their light-sensitive membranes (rhabdoms) in a burst early each morning when the animal is maintained in natural lighting. This shedding burst produces a cloud of multivesicular bodies which coalesce and migrate away from the rhabdom. Within 24 hr, these gradually collapse to combination bodies and ultimately to lamellar bodies. Light initiates the burst of shedding. If animals are maintained in darkness beyond their normal dawn, the shedding burst is delayed until the first onset of light. We have not been able to produce a second burst of membrane shedding within one 24-hr period. Efferent optic nerve activity generated by a circadian clock in the brain primes the shedding burst. At least 3 hr of efferent activity in darkness must precede light onset to prime membrane shedding; however, the efferent fibers need not be active when the light-initiated burst occurs. Chronically blocking the efferent input to the retina abolishes the shedding burst. The burst of membrane shedding is robust and short-lived. Within 15 min of light onset the area of photosensitive membrane decreases by about 70%, and within an hour the rhabdom returns to essentially its preburst size. At other times in the diurnal light cycle, the size of the rhabdom undergoes significant variations which are not abolished by blocking the efferent input. Apparently the daily burst of shedding overlays a second cycle of membrane metabolism that is not controlled by efferent optic nerve activity.