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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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Related in: MedlinePlus

Two-electrode recordings allow pharmacological manipulation of cone phototransductiona. Phototransduction cascade. Light-activated Opsin activates transducin (Gt), which then activates phosphodiesterase (PDE). Active PDE reduces the cyclic-GMP (cGMP) concentration, closing membrane channels. Cyclic-GMP is restored by guanylate cyclase (GC).b. Changes in holding current before (black) and after (gray) introduction of a second electrode; both electrodes contained control internal solution. Filled black and gray circles represent 500 ms stretches of noise used to calculate the spectra in (d).c. Light responses and noise before (black) and after (gray) introduction of the second electrode (time points noted in (b)). Upper left shows expanded examples of noise used to calculate the power spectra in (d).d. Power spectra before (black circles) and after (gray circles) the introduction of the second electrode.e. Average (± SEM, n=16) ratio between power spectra calculated before and after introduction of the second electrode.f. Omission of both ATP and GTP from the internal solution shuts down the phototransduction cascade, causing cGMP-gated channels to close.g. Changes in holding current during a two-electrode recording in which both electrodes contained a solution lacking ATP and GTP. Filled black and purple circles represent 500 ms stretches of noise used to calculate the spectra in (i).h. Examples of light responses and noise recorded before (black) and after (purple) the introduction of a second electrode (time points noted in (g)).i. Power spectra before (black) and after (purple) the introduction of the second electrode.j. Average (± SEM, n=6) ratio of power spectra before and after the introduction of the second electrode. Conditions as in (g).
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Figure 2: Two-electrode recordings allow pharmacological manipulation of cone phototransductiona. Phototransduction cascade. Light-activated Opsin activates transducin (Gt), which then activates phosphodiesterase (PDE). Active PDE reduces the cyclic-GMP (cGMP) concentration, closing membrane channels. Cyclic-GMP is restored by guanylate cyclase (GC).b. Changes in holding current before (black) and after (gray) introduction of a second electrode; both electrodes contained control internal solution. Filled black and gray circles represent 500 ms stretches of noise used to calculate the spectra in (d).c. Light responses and noise before (black) and after (gray) introduction of the second electrode (time points noted in (b)). Upper left shows expanded examples of noise used to calculate the power spectra in (d).d. Power spectra before (black circles) and after (gray circles) the introduction of the second electrode.e. Average (± SEM, n=16) ratio between power spectra calculated before and after introduction of the second electrode.f. Omission of both ATP and GTP from the internal solution shuts down the phototransduction cascade, causing cGMP-gated channels to close.g. Changes in holding current during a two-electrode recording in which both electrodes contained a solution lacking ATP and GTP. Filled black and purple circles represent 500 ms stretches of noise used to calculate the spectra in (i).h. Examples of light responses and noise recorded before (black) and after (purple) the introduction of a second electrode (time points noted in (g)).i. Power spectra before (black) and after (purple) the introduction of the second electrode.j. Average (± SEM, n=6) ratio of power spectra before and after the introduction of the second electrode. Conditions as in (g).

Mentions: Because the two-electrode technique has not been used previously in cones, we started by checking for artifactual changes in noise. We first used a normal internal solution in both electrodes, keeping the phototransduction cascade as intact as possible (Fig. 2a). Rupturing the membrane occluding the tip of the second electrode did not significantly change the holding current (Fig. 2b) or the kinetics or amplitude of the light response (Fig. 2c); some alterations in noise were apparent (Fig. 2c,d). We summarized the results across cells by computing the ratio, at each temporal frequency, of the noise spectra before and after rupturing the membrane at the tip of the second electrode (Fig. 2e); only pharmacological manipulations that produced changes in this ratio larger than the control case were deemed significant.


Origin and effect of phototransduction noise in primate cone photoreceptors.

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

Two-electrode recordings allow pharmacological manipulation of cone phototransductiona. Phototransduction cascade. Light-activated Opsin activates transducin (Gt), which then activates phosphodiesterase (PDE). Active PDE reduces the cyclic-GMP (cGMP) concentration, closing membrane channels. Cyclic-GMP is restored by guanylate cyclase (GC).b. Changes in holding current before (black) and after (gray) introduction of a second electrode; both electrodes contained control internal solution. Filled black and gray circles represent 500 ms stretches of noise used to calculate the spectra in (d).c. Light responses and noise before (black) and after (gray) introduction of the second electrode (time points noted in (b)). Upper left shows expanded examples of noise used to calculate the power spectra in (d).d. Power spectra before (black circles) and after (gray circles) the introduction of the second electrode.e. Average (± SEM, n=16) ratio between power spectra calculated before and after introduction of the second electrode.f. Omission of both ATP and GTP from the internal solution shuts down the phototransduction cascade, causing cGMP-gated channels to close.g. Changes in holding current during a two-electrode recording in which both electrodes contained a solution lacking ATP and GTP. Filled black and purple circles represent 500 ms stretches of noise used to calculate the spectra in (i).h. Examples of light responses and noise recorded before (black) and after (purple) the introduction of a second electrode (time points noted in (g)).i. Power spectra before (black) and after (purple) the introduction of the second electrode.j. Average (± SEM, n=6) ratio of power spectra before and after the introduction of the second electrode. Conditions as in (g).
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Figure 2: Two-electrode recordings allow pharmacological manipulation of cone phototransductiona. Phototransduction cascade. Light-activated Opsin activates transducin (Gt), which then activates phosphodiesterase (PDE). Active PDE reduces the cyclic-GMP (cGMP) concentration, closing membrane channels. Cyclic-GMP is restored by guanylate cyclase (GC).b. Changes in holding current before (black) and after (gray) introduction of a second electrode; both electrodes contained control internal solution. Filled black and gray circles represent 500 ms stretches of noise used to calculate the spectra in (d).c. Light responses and noise before (black) and after (gray) introduction of the second electrode (time points noted in (b)). Upper left shows expanded examples of noise used to calculate the power spectra in (d).d. Power spectra before (black circles) and after (gray circles) the introduction of the second electrode.e. Average (± SEM, n=16) ratio between power spectra calculated before and after introduction of the second electrode.f. Omission of both ATP and GTP from the internal solution shuts down the phototransduction cascade, causing cGMP-gated channels to close.g. Changes in holding current during a two-electrode recording in which both electrodes contained a solution lacking ATP and GTP. Filled black and purple circles represent 500 ms stretches of noise used to calculate the spectra in (i).h. Examples of light responses and noise recorded before (black) and after (purple) the introduction of a second electrode (time points noted in (g)).i. Power spectra before (black) and after (purple) the introduction of the second electrode.j. Average (± SEM, n=6) ratio of power spectra before and after the introduction of the second electrode. Conditions as in (g).
Mentions: Because the two-electrode technique has not been used previously in cones, we started by checking for artifactual changes in noise. We first used a normal internal solution in both electrodes, keeping the phototransduction cascade as intact as possible (Fig. 2a). Rupturing the membrane occluding the tip of the second electrode did not significantly change the holding current (Fig. 2b) or the kinetics or amplitude of the light response (Fig. 2c); some alterations in noise were apparent (Fig. 2c,d). We summarized the results across cells by computing the ratio, at each temporal frequency, of the noise spectra before and after rupturing the membrane at the tip of the second electrode (Fig. 2e); only pharmacological manipulations that produced changes in this ratio larger than the control case were deemed significant.

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