Adapting lights and lowered extracellular free calcium desensitize toad photoreceptors by differing mechanisms

Abstract

Extracellular recordings were made across the outer segment layer of isolated, superfused toad retinas. Under these recording conditions, the photovoltage reflects primarily the current flowing through the outer-segment membrane of red rods. In normal toad Ringer solution, a dim conditioning flash desensitized a test flash response. The desensitization reached a peak 1.8-2.0 s after the conditioning flash and then declined approximately as an exponential with time constant 6 s. Lowered extracellular calcium, [Ca2+]o, desensitized the photoresponse. It required approximately ten times more light to reach a half-maximal response for each ten-fold change in [Ca2+]o from 10(-6) to 10(-9) M. When [Ca2+]o was less than 10(-7) M, substitution of Li+ for Na+ as the predominant monovalent cation in the superfusate permitted responses to continue and a resensitization of up to approximately 1 log unit was observed. The effects of lowered [Ca2+]o on response kinetics were markedly different from the effects of background lights producing a comparable desensitization. Low [Ca2+]o increased absolute latency and time-to-peak of the flash response. Background lights decreased time-to-peak, leaving latency unchanged. The effects of background lights and lowered [Ca2+]o are not additive. Moderate backgrounds had little effect on the intensity/response function in low [Ca2+]o. Conditioning flashes facilitated the test flash response in 10(-7) M-[Ca2+]o superfusate. These results can be understood in terms of the Ca2+ hypothesis of transduction (Hagins & Yoshikami, 1974) if it is assumed that lowered [Ca2+]o exposes an endogenous Ca2+ buffer. The data also provide evidence for a role of Na+/Ca2+ exchange in regulating intracellular Ca2+ concentration in the toad photoreceptor. A quantitative model based on these assumptions is derived and compared with the experimental data.