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Visual coding in locust photoreceptors.

Faivre O, Juusola M - PLoS ONE (2008)

Bottom Line: We found that brightening or warming increase and accelerate voltage responses, but reduce noise, enabling photoreceptors to encode more information.Furthermore, the Q(10)s of bump duration and latency distribution depended on light intensity.Altogether, this study suggests that biochemical constraints imposed upon signaling change continuously as locust photoreceptors adapt to environmental light and temperature conditions.

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology, University of Cambridge, Cambridge, United Kingdom.

ABSTRACT
Information capture by photoreceptors ultimately limits the quality of visual processing in the brain. Using conventional sharp microelectrodes, we studied how locust photoreceptors encode random (white-noise, WN) and naturalistic (1/f stimuli, NS) light patterns in vivo and how this coding changes with mean illumination and ambient temperature. We also examined the role of their plasma membrane in shaping voltage responses. We found that brightening or warming increase and accelerate voltage responses, but reduce noise, enabling photoreceptors to encode more information. For WN stimuli, this was accompanied by broadening of the linear frequency range. On the contrary, with NS the signaling took place within a constant bandwidth, possibly revealing a 'preference' for inputs with 1/f statistics. The faster signaling was caused by acceleration of the elementary phototransduction current--leading to bumps--and their distribution. The membrane linearly translated phototransduction currents into voltage responses without limiting the throughput of these messages. As the bumps reflected fast changes in membrane resistance, the data suggest that their shape is predominantly driven by fast changes in the light-gated conductance. On the other hand, the slower bump latency distribution is likely to represent slower enzymatic intracellular reactions. Furthermore, the Q(10)s of bump duration and latency distribution depended on light intensity. Altogether, this study suggests that biochemical constraints imposed upon signaling change continuously as locust photoreceptors adapt to environmental light and temperature conditions.

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Voltage responses to a WN light stimulus: analysis of the coding properties of the photoreceptor.Analysis of the coding properties of the photoreceptor, based on the SNR(f) (Fig. 1C, right). A, The total signal power increases ∼40 times from BG-4 to BG0. The variance calculated in the time domain, σS2, (not shown) is virtually identical, verifying the calculations. B, The total noise power is reduced ∼2 times from BG-4 to BG0. Here again it is identical to the noise variance calculated in the time domain, σN2, (not shown). C, Information in the frequency domain is calculated from SNR(f) at each frequency as log2[SNR(f)+1]. All the information resides in a frequency range below 100 Hz. This information is integrated to give the information transfer rate (Shannon's formula), D, which increases ∼11 times from BG-4 to BG0. The ratio of the signal and noise variances, SNRt (not shown) scales well with the information transfer rate. This highlights that the information transfer rate is a measure of the number of the ‘coding states’ used by the cell during a second. These states are the different voltage levels confined within the used voltage range (which is ∼ signal as σS2>>σN2) and separated one from another by the ‘resolution’ of the system (noise). From information transfer rate estimates we define three relevant backgrounds: BG-3, named as ‘dim’ (∼100 bits/s); BG-2 as ‘mid’ (∼200 bits/s) and BG0 as ‘bright’ (∼300 bit.s−1). E, Linear coherence, γlin, is calculated from SNR(f). At dim BGs the stimulus is itself noisy (attributable to the photon shot-noise), and so is the cell's behavior. At bright BGs the cell's response (assuming linearity, see Materials and Methods) is remarkably noise-free (γlin>99% at BG0) up to ∼30 Hz.
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pone-0002173-g002: Voltage responses to a WN light stimulus: analysis of the coding properties of the photoreceptor.Analysis of the coding properties of the photoreceptor, based on the SNR(f) (Fig. 1C, right). A, The total signal power increases ∼40 times from BG-4 to BG0. The variance calculated in the time domain, σS2, (not shown) is virtually identical, verifying the calculations. B, The total noise power is reduced ∼2 times from BG-4 to BG0. Here again it is identical to the noise variance calculated in the time domain, σN2, (not shown). C, Information in the frequency domain is calculated from SNR(f) at each frequency as log2[SNR(f)+1]. All the information resides in a frequency range below 100 Hz. This information is integrated to give the information transfer rate (Shannon's formula), D, which increases ∼11 times from BG-4 to BG0. The ratio of the signal and noise variances, SNRt (not shown) scales well with the information transfer rate. This highlights that the information transfer rate is a measure of the number of the ‘coding states’ used by the cell during a second. These states are the different voltage levels confined within the used voltage range (which is ∼ signal as σS2>>σN2) and separated one from another by the ‘resolution’ of the system (noise). From information transfer rate estimates we define three relevant backgrounds: BG-3, named as ‘dim’ (∼100 bits/s); BG-2 as ‘mid’ (∼200 bits/s) and BG0 as ‘bright’ (∼300 bit.s−1). E, Linear coherence, γlin, is calculated from SNR(f). At dim BGs the stimulus is itself noisy (attributable to the photon shot-noise), and so is the cell's behavior. At bright BGs the cell's response (assuming linearity, see Materials and Methods) is remarkably noise-free (γlin>99% at BG0) up to ∼30 Hz.

Mentions: Membrane potentials of green-sensitive R1–R6 photoreceptor cells [29], [30] were recorded with a switched-clamp amplifier SEC-10L (NPI Electronic) operating in the compensated current-clamp mode. A successful photoreceptor penetration was seen as a 60–80 mV drop in the electrode potential followed by vigorous responses to dim pulses. Before the experiments, the cells were allowed to dark-adapt and seal properly. Only data from photoreceptors with saturating impulse responses ≥40 mV and dark resting potential ≤−60 mV were used in the analysis. In this article, we exhibit our findings using two exemplary photoreceptors. Similar results were obtained from other photoreceptors (n = 15) that endured long-lasting recordings. These data are presented in the Supporting Information. A first photoreceptor is used throughout Materials and Methods to illustrate the way data was analyzed (Figs. 1 to 3) at a constant temperature (19°C). The second one is used throughout the article (Figs. 4 to 12). Because of its exceptional stability, we were able to use this cell in many separate experiments and so to explore how light adaptation occurs over a vast range of background intensities and temperatures (from 17 to 23°C). For these experiments we used both white-noise (WN) and naturalistic stimulation (NS), and were able to further investigate how the membrane properties of the cell varied at each experimental condition. Additionally, we made recordings from many other photoreceptors (>30 of outstanding quality) over a smaller range of experimental conditions. These recordings were consistent with the general framework presented here. Because we believe that intrinsic functional variability between photoreceptors could be an important feature of locust vision (see Discussion), we do not show averaged quantities. Data from these cells is shown as Q10 values in Table 1 and detailed further in Table S1.


Visual coding in locust photoreceptors.

Faivre O, Juusola M - PLoS ONE (2008)

Voltage responses to a WN light stimulus: analysis of the coding properties of the photoreceptor.Analysis of the coding properties of the photoreceptor, based on the SNR(f) (Fig. 1C, right). A, The total signal power increases ∼40 times from BG-4 to BG0. The variance calculated in the time domain, σS2, (not shown) is virtually identical, verifying the calculations. B, The total noise power is reduced ∼2 times from BG-4 to BG0. Here again it is identical to the noise variance calculated in the time domain, σN2, (not shown). C, Information in the frequency domain is calculated from SNR(f) at each frequency as log2[SNR(f)+1]. All the information resides in a frequency range below 100 Hz. This information is integrated to give the information transfer rate (Shannon's formula), D, which increases ∼11 times from BG-4 to BG0. The ratio of the signal and noise variances, SNRt (not shown) scales well with the information transfer rate. This highlights that the information transfer rate is a measure of the number of the ‘coding states’ used by the cell during a second. These states are the different voltage levels confined within the used voltage range (which is ∼ signal as σS2>>σN2) and separated one from another by the ‘resolution’ of the system (noise). From information transfer rate estimates we define three relevant backgrounds: BG-3, named as ‘dim’ (∼100 bits/s); BG-2 as ‘mid’ (∼200 bits/s) and BG0 as ‘bright’ (∼300 bit.s−1). E, Linear coherence, γlin, is calculated from SNR(f). At dim BGs the stimulus is itself noisy (attributable to the photon shot-noise), and so is the cell's behavior. At bright BGs the cell's response (assuming linearity, see Materials and Methods) is remarkably noise-free (γlin>99% at BG0) up to ∼30 Hz.
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pone-0002173-g002: Voltage responses to a WN light stimulus: analysis of the coding properties of the photoreceptor.Analysis of the coding properties of the photoreceptor, based on the SNR(f) (Fig. 1C, right). A, The total signal power increases ∼40 times from BG-4 to BG0. The variance calculated in the time domain, σS2, (not shown) is virtually identical, verifying the calculations. B, The total noise power is reduced ∼2 times from BG-4 to BG0. Here again it is identical to the noise variance calculated in the time domain, σN2, (not shown). C, Information in the frequency domain is calculated from SNR(f) at each frequency as log2[SNR(f)+1]. All the information resides in a frequency range below 100 Hz. This information is integrated to give the information transfer rate (Shannon's formula), D, which increases ∼11 times from BG-4 to BG0. The ratio of the signal and noise variances, SNRt (not shown) scales well with the information transfer rate. This highlights that the information transfer rate is a measure of the number of the ‘coding states’ used by the cell during a second. These states are the different voltage levels confined within the used voltage range (which is ∼ signal as σS2>>σN2) and separated one from another by the ‘resolution’ of the system (noise). From information transfer rate estimates we define three relevant backgrounds: BG-3, named as ‘dim’ (∼100 bits/s); BG-2 as ‘mid’ (∼200 bits/s) and BG0 as ‘bright’ (∼300 bit.s−1). E, Linear coherence, γlin, is calculated from SNR(f). At dim BGs the stimulus is itself noisy (attributable to the photon shot-noise), and so is the cell's behavior. At bright BGs the cell's response (assuming linearity, see Materials and Methods) is remarkably noise-free (γlin>99% at BG0) up to ∼30 Hz.
Mentions: Membrane potentials of green-sensitive R1–R6 photoreceptor cells [29], [30] were recorded with a switched-clamp amplifier SEC-10L (NPI Electronic) operating in the compensated current-clamp mode. A successful photoreceptor penetration was seen as a 60–80 mV drop in the electrode potential followed by vigorous responses to dim pulses. Before the experiments, the cells were allowed to dark-adapt and seal properly. Only data from photoreceptors with saturating impulse responses ≥40 mV and dark resting potential ≤−60 mV were used in the analysis. In this article, we exhibit our findings using two exemplary photoreceptors. Similar results were obtained from other photoreceptors (n = 15) that endured long-lasting recordings. These data are presented in the Supporting Information. A first photoreceptor is used throughout Materials and Methods to illustrate the way data was analyzed (Figs. 1 to 3) at a constant temperature (19°C). The second one is used throughout the article (Figs. 4 to 12). Because of its exceptional stability, we were able to use this cell in many separate experiments and so to explore how light adaptation occurs over a vast range of background intensities and temperatures (from 17 to 23°C). For these experiments we used both white-noise (WN) and naturalistic stimulation (NS), and were able to further investigate how the membrane properties of the cell varied at each experimental condition. Additionally, we made recordings from many other photoreceptors (>30 of outstanding quality) over a smaller range of experimental conditions. These recordings were consistent with the general framework presented here. Because we believe that intrinsic functional variability between photoreceptors could be an important feature of locust vision (see Discussion), we do not show averaged quantities. Data from these cells is shown as Q10 values in Table 1 and detailed further in Table S1.

Bottom Line: We found that brightening or warming increase and accelerate voltage responses, but reduce noise, enabling photoreceptors to encode more information.Furthermore, the Q(10)s of bump duration and latency distribution depended on light intensity.Altogether, this study suggests that biochemical constraints imposed upon signaling change continuously as locust photoreceptors adapt to environmental light and temperature conditions.

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology, University of Cambridge, Cambridge, United Kingdom.

ABSTRACT
Information capture by photoreceptors ultimately limits the quality of visual processing in the brain. Using conventional sharp microelectrodes, we studied how locust photoreceptors encode random (white-noise, WN) and naturalistic (1/f stimuli, NS) light patterns in vivo and how this coding changes with mean illumination and ambient temperature. We also examined the role of their plasma membrane in shaping voltage responses. We found that brightening or warming increase and accelerate voltage responses, but reduce noise, enabling photoreceptors to encode more information. For WN stimuli, this was accompanied by broadening of the linear frequency range. On the contrary, with NS the signaling took place within a constant bandwidth, possibly revealing a 'preference' for inputs with 1/f statistics. The faster signaling was caused by acceleration of the elementary phototransduction current--leading to bumps--and their distribution. The membrane linearly translated phototransduction currents into voltage responses without limiting the throughput of these messages. As the bumps reflected fast changes in membrane resistance, the data suggest that their shape is predominantly driven by fast changes in the light-gated conductance. On the other hand, the slower bump latency distribution is likely to represent slower enzymatic intracellular reactions. Furthermore, the Q(10)s of bump duration and latency distribution depended on light intensity. Altogether, this study suggests that biochemical constraints imposed upon signaling change continuously as locust photoreceptors adapt to environmental light and temperature conditions.

Show MeSH
Related in: MedlinePlus