Origin and control of the dominant time constant of salamander cone photoreceptors

Abstract

Recovery of the light response in vertebrate photoreceptors requires the shutoff of both active intermediates in the phototransduction cascade: the visual pigment and the transducin–phosphodiesterase complex. Whichever intermediate quenches more slowly will dominate photoresponse recovery. In suction pipette recordings from isolated salamander ultraviolet- and blue-sensitive cones, response recovery was delayed, and the dominant time constant slowed when internal [Ca2+] was prevented from changing after a bright flash by exposure to 0Ca2+/0Na+ solution. Taken together with a similar prior observation in salamander red-sensitive cones, these observations indicate that the dominance of response recovery by a Ca2+-sensitive process is a general feature of amphibian cone phototransduction. Moreover, changes in the external pH also influenced the dominant time constant of red-sensitive cones even when changes in internal [Ca2+] were prevented. Because the cone photopigment is, uniquely, exposed to the external solution, this may represent a direct effect of protons on the equilibrium between its inactive Meta I and active Meta II forms, consistent with the notion that the process dominating recovery of the bright flash response represents quenching of the active Meta II form of the cone photopigment.