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Biophysical Journal 38: 53-61 (1982)
© 1982 the Biophysical Society

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On the Origin and the Signal-Shaping Mechanism of the Fast Photosignal in the Vertebrate Retina

P. Hochstrate, M. Lindau and H. Rüppel

ABSTRACT

Fast photosignals (FPS) with R1 and R2 components were measured in retinas of cattle, rat, and frog within a temperature range of 0° to 60°C. Except for temperatures near 0°C the signal rise of the R1 component was determined by the duration of the exciting flash. The kinetics of the R2 component and the meta transition of rhodopsin in the cattle and rat retina were compared. For the analysis of the FPS it is presupposed that the signal is produced by light-induced charges on the outer segment envelope membrane that spread onto the whole plasma membrane of the photoreceptor cell. To a good approximation, this mechanism can be described by a model circuit with two distinct capacitors. In this model, the charging capacitance of the pigmented outer segment envelope membrane and the capacitance of the receptor's nonpigmented plasma membrane are connected via the extra- and intracellular electrolyte resistances. The active charging is explained by two independent processes, both with exponential rise (R1 and R2), that are due to charge displacements within the pigmented envelope membrane. The time constant {tau}2 of the R2 membrane charging process shows a strong temperature dependence that of the charge redistribution, {tau}r, a weak one. In frog and cattle retinas the active charging is much slower within a large temperature range than the passive charge redistribution. From the two-capacitor model it follows for {tau}r « {tau}2 that the rise of the R2 component is determined by {tau}r, whereas the decay is given by {tau}2. For the rat retina, however, {tau}2 approaches {tau}r at physiological temperatures and becomes <{tau}r above 45°C. In this temperature range where {tau}2 {approx} {tau}r, both processes affect rise and decay of the photosignal. The absolute values of {tau}r are in good accordance with the known electric parameters of the photoreceptors. At least in the cattle retina, the time constant {tau}2 is identical with that of the slow component of the meta II formation. The strong temperature dependence of the meta transition time gives rise to the marked decrease of the R2 amplitude with falling temperature. As the R1 rise could not be fully time resolved the signal analysis does not yield the time constant {tau}1 of the R1 generating process. It could be established, however, within the whole temperature range that the decay of the R1 component is determined by {tau}r. Using an extended model that allows for membrane leakage, we show that in normal ringer solution the membrane time constant does not influence the signal time-course and amplitude.




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M. L. Woodruff, J. Lem, and G. L. Fain
Early receptor current of wild-type and transducin knockout mice: photosensitivity and light-induced Ca2+ release
J. Physiol., June 15, 2004; 557(3): 821 - 828.
[Abstract] [Full Text] [PDF]


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