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Kinetics of recovery of the dark-adapted salamander rod photoresponse.

Nikonov S, Engheta N, Pugh EN - J. Gen. Physiol. (1998)

Bottom Line: Theoretical analysis of the translation-invariant responses established that tauc 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.Application of these expressions yields an estimate of the calcium buffering capacity of the rod at rest of approximately 20, much lower than previous estimates.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA.

ABSTRACT
The kinetics of the dark-adapted salamander rod photocurrent response to flashes producing from 10 to 10(5) photoisomerizations (Phi) were investigated in normal Ringer's solution, and in a choline solution that clamps calcium near its resting level. For saturating intensities ranging from approximately 10(2) to 10(4) Phi, the recovery phases of the responses in choline were nearly invariant in form. Responses in Ringer's were similarly invariant for saturating intensities from approximately 10(3) to 10(4) Phi. In both solutions, recoveries to flashes in these intensity ranges translated on the time axis a constant amount (tauc) per e-fold increment in flash intensity, and exhibited exponentially decaying "tail phases" with time constant tauc. The difference in recovery half-times for responses in choline and Ringer's to the same saturating flash was 5-7 s. Above approximately 10(4) Phi, recoveries in both solutions were systematically slower, and translation invariance broke down. Theoretical analysis of the translation-invariant responses established that tauc 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 approximately 20, much lower than previous estimates.

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Responses of rods i and j to the lowest intensity flashes used to stimulate each rod in Ringer's and in choline, compared with theoretical traces. The noisy darker gray traces are the responses in Ringer's; the lighter gray traces are the responses in choline. The choline traces were scaled to correspond to the Ringer's traces during the activation phase; the responses so plotted are governed by the same amplification constant, A. (The choline traces are noisier in part because of the scaling, in part because the unscaled amplitudes were smaller, and in part because they represent averages of fewer traces.) The “calcium-clamp” responses of both rods were obtained in 0-Ca2+ choline (see Table II), and had slowly increasing baselines, as illustrated in Fig. 4, rod c. Correction for the baseline was made by computing F(t) = J(t)/Jdark(t), where Jdark(t) is the baseline current in the dark recorded after a jump into choline over a period equal to that of the response, and J(t) is the current trace recorded when the flash is delivered. For the two panels at left, the theory traces were computed as in Fig. 12 for fittings to the Ringer's responses, and by numerically solving Eqs. 5, 6, and 9 for fitting the responses in choline; the solutions to the latter equations were generated with the same method used to fit calcium-clamp responses by Lyubarsky et al. (1996). For the two panels at right, the analytical solutions for ΔcG(t) = cG(t) − cGdark were used (i, theorems 4 and 6). At the peak of the ΔcG(t) response, the values were not sufficiently small for the perturbation expansion of the Hill relation (Eq. A4.3) to be accurate. Thus, rather than use Eqs. 19 and 20 to generate the curves in this figure, the appropriate Hill relation was applied to cG(t)/cGdark. The Hill coefficient was nH = 2 for all theory traces; other parameter values are given in Table IV.
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Figure 13: Responses of rods i and j to the lowest intensity flashes used to stimulate each rod in Ringer's and in choline, compared with theoretical traces. The noisy darker gray traces are the responses in Ringer's; the lighter gray traces are the responses in choline. The choline traces were scaled to correspond to the Ringer's traces during the activation phase; the responses so plotted are governed by the same amplification constant, A. (The choline traces are noisier in part because of the scaling, in part because the unscaled amplitudes were smaller, and in part because they represent averages of fewer traces.) The “calcium-clamp” responses of both rods were obtained in 0-Ca2+ choline (see Table II), and had slowly increasing baselines, as illustrated in Fig. 4, rod c. Correction for the baseline was made by computing F(t) = J(t)/Jdark(t), where Jdark(t) is the baseline current in the dark recorded after a jump into choline over a period equal to that of the response, and J(t) is the current trace recorded when the flash is delivered. For the two panels at left, the theory traces were computed as in Fig. 12 for fittings to the Ringer's responses, and by numerically solving Eqs. 5, 6, and 9 for fitting the responses in choline; the solutions to the latter equations were generated with the same method used to fit calcium-clamp responses by Lyubarsky et al. (1996). For the two panels at right, the analytical solutions for ΔcG(t) = cG(t) − cGdark were used (i, theorems 4 and 6). At the peak of the ΔcG(t) response, the values were not sufficiently small for the perturbation expansion of the Hill relation (Eq. A4.3) to be accurate. Thus, rather than use Eqs. 19 and 20 to generate the curves in this figure, the appropriate Hill relation was applied to cG(t)/cGdark. The Hill coefficient was nH = 2 for all theory traces; other parameter values are given in Table IV.

Mentions: The parameters of Eqs. 19 and 20 have been identified in Tables I and III, respectively; g(s) is a second-order polynomial that arises in obtaining the perturbation solution of theorem 6 (see Eq. A6.8). Fig. 13 shows application of expressions closely relating Eqs. 19 and 20 to dim-flash responses of rods i and j.


Kinetics of recovery of the dark-adapted salamander rod photoresponse.

Nikonov S, Engheta N, Pugh EN - J. Gen. Physiol. (1998)

Responses of rods i and j to the lowest intensity flashes used to stimulate each rod in Ringer's and in choline, compared with theoretical traces. The noisy darker gray traces are the responses in Ringer's; the lighter gray traces are the responses in choline. The choline traces were scaled to correspond to the Ringer's traces during the activation phase; the responses so plotted are governed by the same amplification constant, A. (The choline traces are noisier in part because of the scaling, in part because the unscaled amplitudes were smaller, and in part because they represent averages of fewer traces.) The “calcium-clamp” responses of both rods were obtained in 0-Ca2+ choline (see Table II), and had slowly increasing baselines, as illustrated in Fig. 4, rod c. Correction for the baseline was made by computing F(t) = J(t)/Jdark(t), where Jdark(t) is the baseline current in the dark recorded after a jump into choline over a period equal to that of the response, and J(t) is the current trace recorded when the flash is delivered. For the two panels at left, the theory traces were computed as in Fig. 12 for fittings to the Ringer's responses, and by numerically solving Eqs. 5, 6, and 9 for fitting the responses in choline; the solutions to the latter equations were generated with the same method used to fit calcium-clamp responses by Lyubarsky et al. (1996). For the two panels at right, the analytical solutions for ΔcG(t) = cG(t) − cGdark were used (i, theorems 4 and 6). At the peak of the ΔcG(t) response, the values were not sufficiently small for the perturbation expansion of the Hill relation (Eq. A4.3) to be accurate. Thus, rather than use Eqs. 19 and 20 to generate the curves in this figure, the appropriate Hill relation was applied to cG(t)/cGdark. The Hill coefficient was nH = 2 for all theory traces; other parameter values are given in Table IV.
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Related In: Results  -  Collection

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Figure 13: Responses of rods i and j to the lowest intensity flashes used to stimulate each rod in Ringer's and in choline, compared with theoretical traces. The noisy darker gray traces are the responses in Ringer's; the lighter gray traces are the responses in choline. The choline traces were scaled to correspond to the Ringer's traces during the activation phase; the responses so plotted are governed by the same amplification constant, A. (The choline traces are noisier in part because of the scaling, in part because the unscaled amplitudes were smaller, and in part because they represent averages of fewer traces.) The “calcium-clamp” responses of both rods were obtained in 0-Ca2+ choline (see Table II), and had slowly increasing baselines, as illustrated in Fig. 4, rod c. Correction for the baseline was made by computing F(t) = J(t)/Jdark(t), where Jdark(t) is the baseline current in the dark recorded after a jump into choline over a period equal to that of the response, and J(t) is the current trace recorded when the flash is delivered. For the two panels at left, the theory traces were computed as in Fig. 12 for fittings to the Ringer's responses, and by numerically solving Eqs. 5, 6, and 9 for fitting the responses in choline; the solutions to the latter equations were generated with the same method used to fit calcium-clamp responses by Lyubarsky et al. (1996). For the two panels at right, the analytical solutions for ΔcG(t) = cG(t) − cGdark were used (i, theorems 4 and 6). At the peak of the ΔcG(t) response, the values were not sufficiently small for the perturbation expansion of the Hill relation (Eq. A4.3) to be accurate. Thus, rather than use Eqs. 19 and 20 to generate the curves in this figure, the appropriate Hill relation was applied to cG(t)/cGdark. The Hill coefficient was nH = 2 for all theory traces; other parameter values are given in Table IV.
Mentions: The parameters of Eqs. 19 and 20 have been identified in Tables I and III, respectively; g(s) is a second-order polynomial that arises in obtaining the perturbation solution of theorem 6 (see Eq. A6.8). Fig. 13 shows application of expressions closely relating Eqs. 19 and 20 to dim-flash responses of rods i and j.

Bottom Line: Theoretical analysis of the translation-invariant responses established that tauc 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.Application of these expressions yields an estimate of the calcium buffering capacity of the rod at rest of approximately 20, much lower than previous estimates.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA.

ABSTRACT
The kinetics of the dark-adapted salamander rod photocurrent response to flashes producing from 10 to 10(5) photoisomerizations (Phi) were investigated in normal Ringer's solution, and in a choline solution that clamps calcium near its resting level. For saturating intensities ranging from approximately 10(2) to 10(4) Phi, the recovery phases of the responses in choline were nearly invariant in form. Responses in Ringer's were similarly invariant for saturating intensities from approximately 10(3) to 10(4) Phi. In both solutions, recoveries to flashes in these intensity ranges translated on the time axis a constant amount (tauc) per e-fold increment in flash intensity, and exhibited exponentially decaying "tail phases" with time constant tauc. The difference in recovery half-times for responses in choline and Ringer's to the same saturating flash was 5-7 s. Above approximately 10(4) Phi, recoveries in both solutions were systematically slower, and translation invariance broke down. Theoretical analysis of the translation-invariant responses established that tauc 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 approximately 20, much lower than previous estimates.

Show MeSH
Related in: MedlinePlus