Dual controls for screening pigment movement in photoreceptors of the Limulus lateral eye: circadian efferent input and light.

The radial and longitudinal distribution of retinular screening pigment in the lateral eye of the horseshoe crab Limulus polyphemus was quantified under a variety of experimental conditions. Pigment position was characterized by the center and width of the radial distribution at four levels in the ommatidium. Under diurnal lighting, intact animals show movement of pigment granules from the periphery of the retinular cell at night towards the junction of the arhabdomeral and rhabdomeral segments of the retinular cell in the day. In constant darkness, intact animals exhibit the same circadian rhythm in pigment migration. Animals with bilaterally cut optic nerves do not receive circadian efferent input from the brain and show little pigment movement in diurnal lighting. In all of these cases, pigment was either aggregated in a band just peripheral to the rays of the rhabdom or dispersed to the periphery of the retinular cell. When dark-adapted animals are exposed to a sudden large light increment, pigment moves inward between the rays of the rhabdom. During the day, this inward response begins immediately and reverses as the ommatidial aperture begins to close. At night, the onset of the inward movement is delayed, but then occurs more rapidly than during the day. No significant longitudinal movement of photoreceptor screening pigment was detected under any of these experimental conditions. Two opposing mechanisms control the movement of screening pigment in these cells. Release of neurotransmitters from the circadian efferents causes outward movement; large increments of light cause inward movement. In the absence of sudden changes in light intensity, circadian efferent input, not cyclic lighting, appears to be the major determinant of screening pigment position. A sudden and large increment of light triggers the rapid inward movement which appears to be a protective mechanism optimized for daytime performance.