Kinetics of Recovery of the Dark-adapted Salamander Rod Photoresponse

The kinetics of the dark-adapted salamander rod photocurrent response to flashes producing from 10 to 105 photoisomerizations (Φ) were investigated in normal Ringer's solution, and in a choline solution that clamps calcium near its resting level. For saturating intensities ranging from ∼102 to 104 Φ, the recovery phases of the responses in choline were nearly invariant in form. Responses in Ringer's were similarly invariant for saturating intensities from ∼103 to 104 Φ. In both solutions, recoveries to flashes in these intensity ranges translated on the time axis a constant amount (τc) per e-fold increment in flash intensity, and exhibited exponentially decaying “tail phases” with time constant τc. The difference in recovery half-times for responses in choline and Ringer's to the same saturating flash was 5–7 s. Above ∼104 Φ, recoveries in both solutions were systematically slower, and translation invariance broke down. Theoretical analysis of the translation-invariant responses established that τc must represent the time constant of inactivation of the disc-associated cascade intermediate (R*, G*, or PDE*) having the longest lifetime, and that the cGMP hydrolysis and cGMP-channel activation reactions are such as to conserve this time constant. Theoretical analysis also demonstrated that the 5–7-s shift in recovery half-times between responses in Ringer's and in choline is largely (4–6 s) accounted for by the calcium-dependent activation of guanylyl cyclase, with the residual (1–2 s) likely caused by an effect of calcium on an intermediate with a nondominant time constant. Analytical expressions for the dim-flash response in calcium clamp and Ringer's are derived, and it is shown that the difference in the responses under the two conditions can be accounted for quantitatively by cyclase activation. Application of these expressions yields an estimate of the calcium buffering capacity of the rod at rest of ∼20, much lower than previous estimates.

[1]  V. Arshavsky,et al.  Onset of Feedback Reactions Underlying Vertebrate Rod Photoreceptor Light Adaptation , 1998, The Journal of general physiology.

[2]  C. Cowan,et al.  RGS9, a GTPase Accelerator for Phototransduction , 1998, Neuron.

[3]  N. P. Smith,et al.  The a-wave of the human electroretinogram recorded with a minimally invasive technique , 1997, Vision Research.

[4]  Denis A. Baylor,et al.  Prolonged photoresponses in transgenic mouse rods lacking arrestin , 1997, Nature.

[5]  E. Pugh,et al.  Photoreceptor Guanylate Cyclases: A Review , 1997, Bioscience reports.

[6]  L. Lagnado,et al.  G-protein deactivation is rate-limiting for shut-off of the phototransduction cascade , 1997, Nature.

[7]  H. R. Matthews,et al.  Actions of Ca2+ on an Early Stage in Phototransduction Revealed by the Dynamic Fall in Ca2+ Concentration during the Bright Flash Response , 1997, The Journal of general physiology.

[8]  T. Lamb,et al.  Kinetics of desensitization induced by saturating flashes in toad and salamander rods. , 1996, The Journal of physiology.

[9]  A. Cideciyan,et al.  An Alternative Phototransduction Model for Human Rod and Cone ERG a-waves: Normal Parameters and Variation with Age , 1996, Vision Research.

[10]  P. Detwiler,et al.  Ca2+ Dependence of Dark- and Light-Adapted Flash Responses in Rod Photoreceptors , 1996, Neuron.

[11]  Y. Koutalos,et al.  Regulation of sensitivity in vertebrate rod photoreceptors by calcium , 1996, Trends in Neurosciences.

[12]  E. Pugh,et al.  The kinetics of inactivation of the rod phototransduction cascade with constant Ca2+i , 1996, The Journal of general physiology.

[13]  H R Matthews,et al.  Static and dynamic actions of cytoplasmic Ca2+ in the adaptation of responses to saturating flashes in salamander rods. , 1996, The Journal of physiology.

[14]  Y. Koutalos,et al.  Characterization of guanylate cyclase activity in single retinal rod outer segments , 1995, The Journal of general physiology.

[15]  Y. Koutalos,et al.  The cGMP-phosphodiesterase and its contribution to sensitivity regulation in retinal rods , 1995, The Journal of general physiology.

[16]  G. Jones Light adaptation and the rising phase of the flash photocurrent of salamander retinal rods. , 1995, The Journal of physiology.

[17]  J B Hurley,et al.  Ca-dependent Interaction of Recoverin with Rhodopsin Kinase (*) , 1995, The Journal of Biological Chemistry.

[18]  P. Calvert,et al.  Inhibition of Rhodopsin Kinase by Recoverin , 1995, The Journal of Biological Chemistry.

[19]  H. Matthews Effects of lowered cytoplasmic calcium concentration and light on the responses of salamander rod photoreceptors. , 1995, The Journal of physiology.

[20]  J. Miller,et al.  Differences in calcium homeostasis between retinal rod and cone photoreceptors revealed by the effects of voltage on the cGMP-gated conductance in intact cells , 1994, The Journal of general physiology.

[21]  H. Hamm,et al.  Regulation of transducin GTPase activity in bovine rod outer segments. , 1994, The Journal of biological chemistry.

[22]  T. Wensel,et al.  Enhancement of rod outer segment GTPase accelerating protein activity by the inhibitory subunit of cGMP phosphodiesterase. , 1994, The Journal of biological chemistry.

[23]  D. Hood,et al.  Rod phototransduction in retinitis pigmentosa: estimation and interpretation of parameters derived from the rod a-wave. , 1994, Investigative ophthalmology & visual science.

[24]  E. Pugh,et al.  Rod outer segment structure influences the apparent kinetic parameters of cyclic GMP phosphodiesterase , 1994, The Journal of general physiology.

[25]  D. Baylor,et al.  Calcium controls light-triggered formation of catalytically active rhodopsin , 1994, Nature.

[26]  J. Jin,et al.  Modulation of transduction gain in light adaptation of retinal rods , 1994, Visual Neuroscience.

[27]  E N Pugh,et al.  Analysis of ERG a-wave amplification and kinetics in terms of the G-protein cascade of phototransduction. , 1994, Investigative ophthalmology & visual science.

[28]  J. L. Schnapf,et al.  Visual transduction in human rod photoreceptors. , 1993, The Journal of physiology.

[29]  Satoru Kawamura,et al.  Rhodopsin phosphorylation as a mechanism of cyclic GMP phosphodiesterase regulation by S-modulin , 1993, Nature.

[30]  T. Lamb,et al.  Amplification and kinetics of the activation steps in phototransduction. , 1993, Biochimica et biophysica acta.

[31]  Y. Hsu,et al.  Modulation of the cGMP-gated channel of rod photoreceptor cells by calmodulin , 1993, Nature.

[32]  P. Mcnaughton,et al.  Calcium homeostasis in the outer segments of retinal rods from the tiger salamander. , 1992, The Journal of physiology.

[33]  V. Arshavsky,et al.  Regulation of deactivation of photoreceptor G protein by its target enzyme and cGMP , 1992, Nature.

[34]  E N Pugh,et al.  A quantitative account of the activation steps involved in phototransduction in amphibian photoreceptors. , 1992, The Journal of physiology.

[35]  J. Jin,et al.  Light-dependent delay in the falling phase of the retinal rod photoresponse , 1992, Visual Neuroscience.

[36]  M. Gray-Keller,et al.  cGMP suppresses GTPase activity of a portion of transducin equimolar to phosphodiesterase in frog rod outer segments. Light-induced cGMP decreases as a putative feedback mechanism of the photoresponse. , 1991, The Journal of biological chemistry.

[37]  K. Yau,et al.  Calcium feedback and sensitivity regulation in primate rods , 1991, The Journal of general physiology.

[38]  M. Murakami,et al.  Regulation of cGMP levels by guanylate cyclase in truncated frog rod outer segments , 1989, The Journal of general physiology.

[39]  T. Lamb,et al.  Cytoplasmic calcium as the messenger for light adaptation in salamander rods. , 1989, The Journal of physiology.

[40]  A. Hodgkin,et al.  Control of light‐sensitive current in salamander rods. , 1988, The Journal of physiology.

[41]  W. Cobbs,et al.  Kinetics and components of the flash photocurrent of isolated retinal rods of the larval salamander, Ambystoma tigrinum. , 1987, The Journal of physiology.

[42]  H R Matthews,et al.  Role of calcium in regulating the cyclic GMP cascade of phototransduction in retinal rods. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[43]  Edward H. Adelson,et al.  Saturation and adaptation in the rod system , 1982, Vision Research.

[44]  Edward H. Adelson,et al.  The delayed rod afterimage , 1982, Vision Research.

[45]  Peter K. F. Kuhfittig,et al.  Introduction to the Laplace transform , 1978 .

[46]  A. Hodgkin,et al.  Reconstruction of the electrical responses of turtle cones to flashes and steps of light , 1974, The Journal of physiology.

[47]  J. Aczél,et al.  Lectures on Functional Equations and Their Applications , 1968 .

[48]  J. C. Jaeger An Introduction to the Laplace Transformation , 1946 .