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Origin and effect of phototransduction noise in primate cone photoreceptors.

Angueyra JM, Rieke F - Nat. Neurosci. (2013)

Bottom Line: This difference helps to explain why thresholds for rod- and cone-mediated signals have different dependencies on background light level.Third, past estimates of noise in mammalian cones are too high to explain behavioral sensitivity.Our measurements indicate a lower level of cone noise and therefore help to reconcile physiological and behavioral estimates of cone noise and sensitivity.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology and Biophysics, Howard Hughes Medical Institute, University of Washington, Seattle, Washington, USA.

ABSTRACT
Noise in the responses of cone photoreceptors sets a fundamental limit on visual sensitivity, yet the origin of noise in mammalian cones and its relation to behavioral sensitivity are poorly understood. Our work here on primate cones improves understanding of these issues in three ways. First, we found that cone noise was not dominated by spontaneous photopigment activation or by quantal fluctuations in photon absorption, but was instead dominated by other sources, namely channel noise and fluctuations in cyclic GMP. Second, adaptation in cones, unlike that in rods, affected signal and noise differently. This difference helps to explain why thresholds for rod- and cone-mediated signals have different dependencies on background light level. Third, past estimates of noise in mammalian cones are too high to explain behavioral sensitivity. Our measurements indicate a lower level of cone noise and therefore help to reconcile physiological and behavioral estimates of cone noise and sensitivity.

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High frequency noise arises from open/close transitions in the cGMP-gated channelsa. Channel noise was separated from sources causing fluctuations in [cGMP] by suppressing cGMP synthesis by omitting ATP and GTP from the internal solutions in a two-electrode recording. Different concentrations of the cGMP-channel agonist 8′Bromo-cyclic-GMP (8′Br-cGMP) were added to the second electrode.b. Changes in holding current before (black) and after (green) the introduction of a second electrode containing 27 μM 8′Br-cGMP. The filled black and green circles represent 500ms stretches of noise used to calculate the spectra in (c).c. Average noise power spectra for the cone in (B) before (black) and after (green) the introduction of a second electrode containing 27 μM 8′Br-cGMP. Insets show example noise traces in each condition corresponding to (1) and (2) in (b).d and e. Same as in (b) and (c) for an 8′Br-cGMP concentration of 100 μM.f. Average (± SEM) ratio of power spectra before and after introduction of 8′Br-cGMP. The color scale corresponds to the concentration of 8′Br-cGMP (18 μM: n = 10; 27 μM: n = 4; 100 μM: n = 3; 200 μM: n = 2). Changes in noise below 10Hz are unreliable due to slow drift in the measured current and are displayed as open circles. The increase at high frequencies (100 Hz–600Hz) is significant across all concentrations.
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Figure 3: High frequency noise arises from open/close transitions in the cGMP-gated channelsa. Channel noise was separated from sources causing fluctuations in [cGMP] by suppressing cGMP synthesis by omitting ATP and GTP from the internal solutions in a two-electrode recording. Different concentrations of the cGMP-channel agonist 8′Bromo-cyclic-GMP (8′Br-cGMP) were added to the second electrode.b. Changes in holding current before (black) and after (green) the introduction of a second electrode containing 27 μM 8′Br-cGMP. The filled black and green circles represent 500ms stretches of noise used to calculate the spectra in (c).c. Average noise power spectra for the cone in (B) before (black) and after (green) the introduction of a second electrode containing 27 μM 8′Br-cGMP. Insets show example noise traces in each condition corresponding to (1) and (2) in (b).d and e. Same as in (b) and (c) for an 8′Br-cGMP concentration of 100 μM.f. Average (± SEM) ratio of power spectra before and after introduction of 8′Br-cGMP. The color scale corresponds to the concentration of 8′Br-cGMP (18 μM: n = 10; 27 μM: n = 4; 100 μM: n = 3; 200 μM: n = 2). Changes in noise below 10Hz are unreliable due to slow drift in the measured current and are displayed as open circles. The increase at high frequencies (100 Hz–600Hz) is significant across all concentrations.

Mentions: The two-electrode experiments described in this section, isolated noise produced by cGMP-gated channels. Changes in cGMP were again suppressed by omitting ATP and GTP from the internal solution, and cGMP channels were activated with 8′Br-cGMP, a potent agonist of the cGMP-gated channels (Fig. 3a). Because 8′Br-cGMP is also poorly hydrolyzed by PDE, it suppresses activity within the PDE arm of the phototransduction cascade. Introduction of 8′Br-cGMP through the second electrode would ideally occur only after the internal cGMP has been depleted, but this process can take up to 5 min (Fig. 2g), and long recordings with two electrodes are technically difficult. Instead, we relied on shorter experiments in which we compared different concentrations of 8′Br-cGMP with the case where 8′Br-cGMP is absent (Fig. 2j).


Origin and effect of phototransduction noise in primate cone photoreceptors.

Angueyra JM, Rieke F - Nat. Neurosci. (2013)

High frequency noise arises from open/close transitions in the cGMP-gated channelsa. Channel noise was separated from sources causing fluctuations in [cGMP] by suppressing cGMP synthesis by omitting ATP and GTP from the internal solutions in a two-electrode recording. Different concentrations of the cGMP-channel agonist 8′Bromo-cyclic-GMP (8′Br-cGMP) were added to the second electrode.b. Changes in holding current before (black) and after (green) the introduction of a second electrode containing 27 μM 8′Br-cGMP. The filled black and green circles represent 500ms stretches of noise used to calculate the spectra in (c).c. Average noise power spectra for the cone in (B) before (black) and after (green) the introduction of a second electrode containing 27 μM 8′Br-cGMP. Insets show example noise traces in each condition corresponding to (1) and (2) in (b).d and e. Same as in (b) and (c) for an 8′Br-cGMP concentration of 100 μM.f. Average (± SEM) ratio of power spectra before and after introduction of 8′Br-cGMP. The color scale corresponds to the concentration of 8′Br-cGMP (18 μM: n = 10; 27 μM: n = 4; 100 μM: n = 3; 200 μM: n = 2). Changes in noise below 10Hz are unreliable due to slow drift in the measured current and are displayed as open circles. The increase at high frequencies (100 Hz–600Hz) is significant across all concentrations.
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Related In: Results  -  Collection

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Figure 3: High frequency noise arises from open/close transitions in the cGMP-gated channelsa. Channel noise was separated from sources causing fluctuations in [cGMP] by suppressing cGMP synthesis by omitting ATP and GTP from the internal solutions in a two-electrode recording. Different concentrations of the cGMP-channel agonist 8′Bromo-cyclic-GMP (8′Br-cGMP) were added to the second electrode.b. Changes in holding current before (black) and after (green) the introduction of a second electrode containing 27 μM 8′Br-cGMP. The filled black and green circles represent 500ms stretches of noise used to calculate the spectra in (c).c. Average noise power spectra for the cone in (B) before (black) and after (green) the introduction of a second electrode containing 27 μM 8′Br-cGMP. Insets show example noise traces in each condition corresponding to (1) and (2) in (b).d and e. Same as in (b) and (c) for an 8′Br-cGMP concentration of 100 μM.f. Average (± SEM) ratio of power spectra before and after introduction of 8′Br-cGMP. The color scale corresponds to the concentration of 8′Br-cGMP (18 μM: n = 10; 27 μM: n = 4; 100 μM: n = 3; 200 μM: n = 2). Changes in noise below 10Hz are unreliable due to slow drift in the measured current and are displayed as open circles. The increase at high frequencies (100 Hz–600Hz) is significant across all concentrations.
Mentions: The two-electrode experiments described in this section, isolated noise produced by cGMP-gated channels. Changes in cGMP were again suppressed by omitting ATP and GTP from the internal solution, and cGMP channels were activated with 8′Br-cGMP, a potent agonist of the cGMP-gated channels (Fig. 3a). Because 8′Br-cGMP is also poorly hydrolyzed by PDE, it suppresses activity within the PDE arm of the phototransduction cascade. Introduction of 8′Br-cGMP through the second electrode would ideally occur only after the internal cGMP has been depleted, but this process can take up to 5 min (Fig. 2g), and long recordings with two electrodes are technically difficult. Instead, we relied on shorter experiments in which we compared different concentrations of 8′Br-cGMP with the case where 8′Br-cGMP is absent (Fig. 2j).

Bottom Line: This difference helps to explain why thresholds for rod- and cone-mediated signals have different dependencies on background light level.Third, past estimates of noise in mammalian cones are too high to explain behavioral sensitivity.Our measurements indicate a lower level of cone noise and therefore help to reconcile physiological and behavioral estimates of cone noise and sensitivity.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology and Biophysics, Howard Hughes Medical Institute, University of Washington, Seattle, Washington, USA.

ABSTRACT
Noise in the responses of cone photoreceptors sets a fundamental limit on visual sensitivity, yet the origin of noise in mammalian cones and its relation to behavioral sensitivity are poorly understood. Our work here on primate cones improves understanding of these issues in three ways. First, we found that cone noise was not dominated by spontaneous photopigment activation or by quantal fluctuations in photon absorption, but was instead dominated by other sources, namely channel noise and fluctuations in cyclic GMP. Second, adaptation in cones, unlike that in rods, affected signal and noise differently. This difference helps to explain why thresholds for rod- and cone-mediated signals have different dependencies on background light level. Third, past estimates of noise in mammalian cones are too high to explain behavioral sensitivity. Our measurements indicate a lower level of cone noise and therefore help to reconcile physiological and behavioral estimates of cone noise and sensitivity.

Show MeSH
Related in: MedlinePlus