Circadian rhythms in Limulus photoreceptors. I. Intracellular studies

The sensitivity of the lateral eye of the horseshoe crab, Limulus polyphemus, is modulated by efferent optic nerve impulses transmitted from a circadian clock located in the brain (Barlow, R. B., Jr., S. J. Bolanowski, and M. L. Brachman. 1977. Science. 197:86-89). At night, the efferent impulses invade the retinular, eccentric, and pigment cells of every ommatidium, inducing multiple anatomical and physiological changes that combine to increase retinal sensitivity as much as 100,000 times. We developed techniques for recording transmembrane potentials from a single cell in situ for several days to determine what circadian changes in retinal sensitivity originate in the primary phototransducing cell, the retinular cell. We found that the direct efferent input to the photoreceptor cell decreases its noise and increases its response. Noise is decreased by reducing the rate of spontaneous bumps by up to 100%. The response is increased by elevating photon catch (photons absorbed per flash) as much as 30 times, and increasing gain (response per absorbed photon) as much as 40%. The cellular mechanism for reducing the rate of spontaneous quantum bumps is not known. The mechanism for increasing gain appears to be the modulation of ionic conductances in the photoreceptor cell membrane. The mechanism for increasing photon catch is multiple changes in the anatomy of retinal cells. We combine these cellular events in a proposed scheme for the circadian rhythm in the intensity coding of single photoreceptors.