We investigated the kinetics and sensitivity of photocurrent responses of salamander rods, both in darkness and during adaptation to steady backgrounds producing 20–3,000 photoisomerizations per second, using suction pipet recordings. The most intense backgrounds suppressed 80% of the circulating dark current and decreased the flash sensitivity ∼30-fold. To investigate the underlying transduction mechanism, we expressed the responses as a fraction of the steady level of cGMP-activated current recorded in the background. The fractional responses to flashes of any fixed intensity began rising along a common trajectory, regardless of background intensity. We interpret these invariant initial trajectories to indicate that, at these background intensities, light adaptation does not alter the gain of any of the amplifying steps of phototransduction. For subsaturating flashes of fixed intensity, the fractional responses obtained on backgrounds of different intensity were found to “peel off” from their common initial trajectory in a background-dependent manner: the more intense the background, the earlier the time of peeling off. This behavior is consistent with a background-induced reduction in the effective lifetime of at least one of the three major integrating steps in phototransduction; i.e., an acceleration of one or more of the following: (1) the inactivation of activated rhodopsin (R*); (2) the inactivation of activated phosphodiesterase (E*, representing the complex Gα–PDE of phosphodiesterase with the transducin α-subunit); or (3) the hydrolysis of cGMP, with rate constant β. Our measurements show that, over the range of background intensities we used, β increased on average to ∼20 times its dark-adapted value; and our theoretical analysis indicates that this increase in β is the primary mechanism underlying the measured shortening of time-to-peak of the dim-flash response and the decrease in sensitivity of the fractional response.
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1 December 2000
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December 01 2000
The Role of Steady Phosphodiesterase Activity in the Kinetics and Sensitivity of the Light-Adapted Salamander Rod Photoresponse
S. Nikonov,
S. Nikonov
aDepartment of Ophthalmology and Institute of Neurological Sciences, University of Pennsylvania, Philadelphia, Pennsylvania 19104
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T.D. Lamb,
T.D. Lamb
bDepartment of Physiology, University of Cambridge, Cambridge, CB2 3EG, United Kingdom
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E.N. Pugh, Jr.
E.N. Pugh, Jr.
aDepartment of Ophthalmology and Institute of Neurological Sciences, University of Pennsylvania, Philadelphia, Pennsylvania 19104
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S. Nikonov
aDepartment of Ophthalmology and Institute of Neurological Sciences, University of Pennsylvania, Philadelphia, Pennsylvania 19104
T.D. Lamb
bDepartment of Physiology, University of Cambridge, Cambridge, CB2 3EG, United Kingdom
E.N. Pugh, Jr.
aDepartment of Ophthalmology and Institute of Neurological Sciences, University of Pennsylvania, Philadelphia, Pennsylvania 19104
Abbreviations used in this paper: IBMX, isobutyl methylxanthine; PDE, phosphodiesterase.
Received:
August 08 2000
Revision Requested:
September 13 2000
Accepted:
September 15 2000
Online ISSN: 1540-7748
Print ISSN: 0022-1295
© 2000 The Rockefeller University Press
2000
The Rockefeller University Press
J Gen Physiol (2000) 116 (6): 795–824.
Article history
Received:
August 08 2000
Revision Requested:
September 13 2000
Accepted:
September 15 2000
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Citation
S. Nikonov, T.D. Lamb, E.N. Pugh; The Role of Steady Phosphodiesterase Activity in the Kinetics and Sensitivity of the Light-Adapted Salamander Rod Photoresponse . J Gen Physiol 1 December 2000; 116 (6): 795–824. doi: https://doi.org/10.1085/jgp.116.6.795
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