Mechanisms controlling the sensitivity of the Limulus lateral eye in natural lighting

Abstract

Electroretinograms were recorded from the horseshoe crab compound eye using a high-intensity light-emitting diode and a whole-eye seawater electrode. Recordings were made from both lateral eyes in natural daylight or in continuous darkness with the optic nerve intact or cut. Recordings from two eyes of the same animal in different conditions facilitated direct comparisons of the effects of diurnal lighting and circadian efferent activity on the daily patterns of sensitivity of the eye. Structural changes appear to account for about half of the total electroretinogram excursion. Circadian input begins about 45 min in advance of sunset and the nighttime sensitivity returns to the daytime values 20 min after sunrise. When the optic nerve is cut, the nighttime sensitivity shows exponential decay over the next 5 or 6 days, consistent with a light-triggered structural light adaptation process unopposed by efferent input. Our results suggest that two mechanisms mediate the increase in lateral eye sensitivity at night-physiological dark adaptation and circadian efferent input. Three mechanisms appear to be involved in mediating the decrease in lateral eye sensitivity during daylight-physiological light adaptation, a continuous structural light adaptation process, and a separate light-triggered, efferent-primed structural light adaptation process.

Opsin1-2, Gqα and arrestin levels at Limulus rhabdoms are controlled by diurnal light and a circadian clock

“…In both populations, structural changes must be underway before dark, indicating clock input to LEs of both groups begins before dark. In Woods Hole animals, clock input is estimated to begin approximately 45min before SS (Pieprzyk et al, 2003). During dawn, TRS in both populations begins at approximately SR. .…”

“…Light alone appears responsible for the daytime decrease in RhG q α levels; however, clock input at night is required to prime the rapid shedding of RhOps1-2 at first light, and this probably contributes to a rapid decrease in visual sensitivity in the morning (Pieprzyk et al, 2003). Furthermore, because clock input is required for maximum increases in RhOps1-2 and RhG q α levels in the dark, low photoreceptor sensitivity is maintained throughout the day, even in the dark.…”

“…The sensitivity of Limulus LEs increases dramatically at night (Barlow et al, 1977;Barlow, 1983), and behavioral studies indicate that these animals see at night with their LEs nearly as well as during the day (Powers et al, 1991). Half of this increase in sensitivity is driven by signals from a central circadian clock (Pieprzyk et al, 2003). At night, the central clock activates a bilateral population of neurons that project from the chelicerial ganglia in the brain to all of the eyes -LEs, median ocelli and rudimentary eyes -through their optic nerves (Fahrenbach, 1973;Fahrenbach, 1981;Barlow et al, 1977;Barlow et al, 1980;Calman and Battelle, 1991;Kass and Barlow, 1992).…”

Opsin co-expression in Limulus photoreceptors: differential regulation by light and a circadian clock

“…This clock-driven efferent input, referred to here as clock input, becomes active about 45min before sunset, remains active throughout the night and is inactive during the day (Barlow 1983;Pieprzyk et al, 2003). During the night, clock input has dramatic and diverse effects on LE structure, function and biochemistry (reviewed in Battelle, 2002) and, as mentioned above, is required to prime TRS that occurs at first light.…”

Evolution of arthropod visual systems: Development of the eyes and central visual pathways in the horseshoe crabLimulus polyphemusLinnaeus, 1758 (Chelicerata, Xiphosura)

“…Aspects that have been explored in the past include adult ommatidial morphology of the lateral eyes (review Fahrenbach, 1975), organization of the retinal projections into the brain as well as efferent projections Barlow, 1980, 1982;Batra and Chamberlain, 1985;, and distribution of the visual pathway neurotransmitters (reviewed in Battelle et al, 1999) octopamine (Evans et al, 1983), serotonin , FMRFamide and substance P (Chamberlain and Engbretson, 1982;Lewandoswski et al, 1989), histamine , and acetylcholine (Hornstein et al, 1994). Additionally, circadian modulation of the photoresponse (e.g., Battelle et al, 1998Battelle et al, , 2000Battelle et al, , 2001Sacunas et al, 2002;Waren and Chamberlain, 2002;Ankrom and Chamberlain, 2002;Dalal et al, 2003;Pieprzyk et al, 2003;Runyon et al, 2004;reviews, Barlow, 2001;Battelle, 2002), and both computational and behavioral aspects of vision (reviewed in Barlow et al, 2001) are active areas of current research.…”