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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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An additional noise source with power in the low to mid frequency range causes fluctuations in cGMPa. The membrane-permeable and fast acting PDE inhibitor IBMX increases the cGMP concentration and therefore the number of open channels and inhibits any noise source upstream of (and including) PDE.b. Changes in holding current in the absence (black) and presence (gray) of IBMX. The filled black and gray circles represent 500 ms stretches of noise used to calculate the spectra in (c). Recordings were performed in complete darkness to avoid extrinsic noise.c. Corresponding power spectra in the absence (black circles) and presence (gray circles) of IBMX. Insets show example noise traces in each condition corresponding to (1) and (2) in (b). Changes in noise below 10Hz (open circles) are unreliable due to slow drift in the measured current.d. Average (± SEM) ratio of power spectra in the presence and in the absence of IBMX (n = 10) showing a decrease in noise in the 10 to 50 Hz range and an increase in noise at high frequencies (100 to 600Hz)e. Average (± SEM) ratio of power spectra before and after puffing a vehicle solution lacking IBMX (n=4). The increase in noise at the high frequencies (100–600Hz) and the decrease at low frequencies (10–30 Hz) seen with IBMX were significantly different than the changes with vehicle.
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Figure 4: An additional noise source with power in the low to mid frequency range causes fluctuations in cGMPa. The membrane-permeable and fast acting PDE inhibitor IBMX increases the cGMP concentration and therefore the number of open channels and inhibits any noise source upstream of (and including) PDE.b. Changes in holding current in the absence (black) and presence (gray) of IBMX. The filled black and gray circles represent 500 ms stretches of noise used to calculate the spectra in (c). Recordings were performed in complete darkness to avoid extrinsic noise.c. Corresponding power spectra in the absence (black circles) and presence (gray circles) of IBMX. Insets show example noise traces in each condition corresponding to (1) and (2) in (b). Changes in noise below 10Hz (open circles) are unreliable due to slow drift in the measured current.d. Average (± SEM) ratio of power spectra in the presence and in the absence of IBMX (n = 10) showing a decrease in noise in the 10 to 50 Hz range and an increase in noise at high frequencies (100 to 600Hz)e. Average (± SEM) ratio of power spectra before and after puffing a vehicle solution lacking IBMX (n=4). The increase in noise at the high frequencies (100–600Hz) and the decrease at low frequencies (10–30 Hz) seen with IBMX were significantly different than the changes with vehicle.

Mentions: The experiments described above indicate that channel fluctuations produce noise extending from low to high temporal frequencies. To test for other sources of low- to mid-frequency noise, we puffed the membrane-permeable PDE inhibitor IBMX onto the outer segments of voltage-clamped cones. IBMX has two effects: (1) it decreases baseline hydrolysis of cGMP, leading to an increase in [cGMP] and opening of cGMP-gated channels; and, (2) it decreases the fluctuations in [cGMP] produced by dark activation of any of the transduction components upstream of (and including) PDE (Fig. 4a). We performed recordings in darkness to avoid extrinsic noise and again focused on frequencies above 10 Hz to avoid artifacts induced by current drift.


Origin and effect of phototransduction noise in primate cone photoreceptors.

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

An additional noise source with power in the low to mid frequency range causes fluctuations in cGMPa. The membrane-permeable and fast acting PDE inhibitor IBMX increases the cGMP concentration and therefore the number of open channels and inhibits any noise source upstream of (and including) PDE.b. Changes in holding current in the absence (black) and presence (gray) of IBMX. The filled black and gray circles represent 500 ms stretches of noise used to calculate the spectra in (c). Recordings were performed in complete darkness to avoid extrinsic noise.c. Corresponding power spectra in the absence (black circles) and presence (gray circles) of IBMX. Insets show example noise traces in each condition corresponding to (1) and (2) in (b). Changes in noise below 10Hz (open circles) are unreliable due to slow drift in the measured current.d. Average (± SEM) ratio of power spectra in the presence and in the absence of IBMX (n = 10) showing a decrease in noise in the 10 to 50 Hz range and an increase in noise at high frequencies (100 to 600Hz)e. Average (± SEM) ratio of power spectra before and after puffing a vehicle solution lacking IBMX (n=4). The increase in noise at the high frequencies (100–600Hz) and the decrease at low frequencies (10–30 Hz) seen with IBMX were significantly different than the changes with vehicle.
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Related In: Results  -  Collection

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Figure 4: An additional noise source with power in the low to mid frequency range causes fluctuations in cGMPa. The membrane-permeable and fast acting PDE inhibitor IBMX increases the cGMP concentration and therefore the number of open channels and inhibits any noise source upstream of (and including) PDE.b. Changes in holding current in the absence (black) and presence (gray) of IBMX. The filled black and gray circles represent 500 ms stretches of noise used to calculate the spectra in (c). Recordings were performed in complete darkness to avoid extrinsic noise.c. Corresponding power spectra in the absence (black circles) and presence (gray circles) of IBMX. Insets show example noise traces in each condition corresponding to (1) and (2) in (b). Changes in noise below 10Hz (open circles) are unreliable due to slow drift in the measured current.d. Average (± SEM) ratio of power spectra in the presence and in the absence of IBMX (n = 10) showing a decrease in noise in the 10 to 50 Hz range and an increase in noise at high frequencies (100 to 600Hz)e. Average (± SEM) ratio of power spectra before and after puffing a vehicle solution lacking IBMX (n=4). The increase in noise at the high frequencies (100–600Hz) and the decrease at low frequencies (10–30 Hz) seen with IBMX were significantly different than the changes with vehicle.
Mentions: The experiments described above indicate that channel fluctuations produce noise extending from low to high temporal frequencies. To test for other sources of low- to mid-frequency noise, we puffed the membrane-permeable PDE inhibitor IBMX onto the outer segments of voltage-clamped cones. IBMX has two effects: (1) it decreases baseline hydrolysis of cGMP, leading to an increase in [cGMP] and opening of cGMP-gated channels; and, (2) it decreases the fluctuations in [cGMP] produced by dark activation of any of the transduction components upstream of (and including) PDE (Fig. 4a). We performed recordings in darkness to avoid extrinsic noise and again focused on frequencies above 10 Hz to avoid artifacts induced by current drift.

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