Light-activation of Teleost Rod Photoreceptor Elongation

Abstract

Rod photoreceptors in the retinas of teleost fish undergo changes in cell length in response to changing ambient light intensities. In the dark rods shorten and in the light rods elongate. These movements are mediated by actin-dependent processes which occur in the ellipsoid and myoid of the inner segment. As an approach to examining the underlying intracellular signaling pathways that link light absorption to actin-dependent motility in the inner segment, we have investigated the quantitative aspects of the light stimulus required to activate elongation in isolated rod inner/outer segments (RIS-ROS) of the green sunfish (Lepomis cyanellus).The intensity thresholds and strength-duration characteristics of the light stimulus required to activate teleost rod elongation were found to differ from those reported to activate vertebrate rod membrane hyperpolarization. In response to brief pulses of light, RIS-ROS elongated in a graded manner, both as a function of increasing light pulse intensity and light pulse duration. Half maximal activation of light-induced RIS-ROS elongation was produced by a stimulus of roughly 6 × 1015 photons cm-2, which is calculated to bleach approximately 20% of the photopigment molecules in green sunfish rod outer segments. This degree of photopigment bleach is approximately 6-7 orders of magnitude greater than that required to elicit half maximal changes in membrane potential in other vertebrate rod preparations. Furthermore, the reciprocal relationship between light pulse intensity and duration in eliciting an equal elongation response held for relatively long light pulse durations. There was an approximately equal elongation response to light pulse durations of 15, 120, and 600 sec, that delivered roughly equal quanta. Over these light pulse durations, the temporal integration function is described by a single slope of -0·9 on log-log coordinates of stimulus intensity and duration. The integration time of the rod elongation response lasts for light pulse durations at least as long as 600 sec, which is approximately 3 orders of magnitude longer than that reported for rod membrane hyperpolarization. The high threshold and long integration time of the photoreceptive mechanisms mediating rod elongation indicate that the intracellular signals that regulate motility dramatically diverge from those regulating rod membrane hyperpolarization. A further implication of these results is that vertebrate rod photoreceptors possess different intensity thresholds and temporal processing mechanisms in the light-activation of distinct cell functions such as membrane hyperpolarization and cell elongation.