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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 transfer properties of the photoreceptor.Analysis of the transfer properties of the photoreceptor, based on the cross-spectrum between the stimulus and the signal (Fig. 1C, left). A, Gain is the norm of the frequency response (see Materials and Methods). It displays the range and extent of stimulus frequencies the cell amplify linearly. B, Areas (integrals) under gain curves at different BGs, and D, corresponding 3 dB cut-off frequencies. The amplification increases with the light BGs whereas the cut-off frequency remains virtually unchanged. C, Phase of the frequency response and the minimum phase, calculated from the gain curves, exhibits a phase-lag. E, Impulse response K1 is calculated from the frequency response function (real parts seen as gain, A, and phase, C). It approximates the linear filtering properties of the system. Brightening increases its area, scaling closely with the gain power (not shown), and reduces its onset-delay, F, as well as its time-to-peak (the delay between onset and peak is virtually constant ∼20 ms). The dead-times estimated from the phase-shift observed in C (not shown) and from the impulse response (F) behave very similarly, vindicating the analysis. G, Noise-free coherence, γNF, indicates the frequency range where a photoreceptor, if operating linearly, would reproduce exactly the same response at each stimulus presentation. γNF departs from unity at certain frequencies, reflecting selective nonlinearities, which enhance particular features of the stimulus. The bandwidths of the coherences, H, are defined as the frequency beyond which γ<0.5. The bandwidths increase with brightening BGs, reflecting the photoreceptor's ability to follow the stimulus on a shorter time-scale (γlin). This increased precision takes place in a frequency range where the photoreceptor encodes linearly the WN stimulus (γNF>γlin at each BG).
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pone-0002173-g003: Voltage responses to a WN light stimulus: analysis of the transfer properties of the photoreceptor.Analysis of the transfer properties of the photoreceptor, based on the cross-spectrum between the stimulus and the signal (Fig. 1C, left). A, Gain is the norm of the frequency response (see Materials and Methods). It displays the range and extent of stimulus frequencies the cell amplify linearly. B, Areas (integrals) under gain curves at different BGs, and D, corresponding 3 dB cut-off frequencies. The amplification increases with the light BGs whereas the cut-off frequency remains virtually unchanged. C, Phase of the frequency response and the minimum phase, calculated from the gain curves, exhibits a phase-lag. E, Impulse response K1 is calculated from the frequency response function (real parts seen as gain, A, and phase, C). It approximates the linear filtering properties of the system. Brightening increases its area, scaling closely with the gain power (not shown), and reduces its onset-delay, F, as well as its time-to-peak (the delay between onset and peak is virtually constant ∼20 ms). The dead-times estimated from the phase-shift observed in C (not shown) and from the impulse response (F) behave very similarly, vindicating the analysis. G, Noise-free coherence, γNF, indicates the frequency range where a photoreceptor, if operating linearly, would reproduce exactly the same response at each stimulus presentation. γNF departs from unity at certain frequencies, reflecting selective nonlinearities, which enhance particular features of the stimulus. The bandwidths of the coherences, H, are defined as the frequency beyond which γ<0.5. The bandwidths increase with brightening BGs, reflecting the photoreceptor's ability to follow the stimulus on a shorter time-scale (γlin). This increased precision takes place in a frequency range where the photoreceptor encodes linearly the WN stimulus (γNF>γlin at each BG).

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 transfer properties of the photoreceptor.Analysis of the transfer properties of the photoreceptor, based on the cross-spectrum between the stimulus and the signal (Fig. 1C, left). A, Gain is the norm of the frequency response (see Materials and Methods). It displays the range and extent of stimulus frequencies the cell amplify linearly. B, Areas (integrals) under gain curves at different BGs, and D, corresponding 3 dB cut-off frequencies. The amplification increases with the light BGs whereas the cut-off frequency remains virtually unchanged. C, Phase of the frequency response and the minimum phase, calculated from the gain curves, exhibits a phase-lag. E, Impulse response K1 is calculated from the frequency response function (real parts seen as gain, A, and phase, C). It approximates the linear filtering properties of the system. Brightening increases its area, scaling closely with the gain power (not shown), and reduces its onset-delay, F, as well as its time-to-peak (the delay between onset and peak is virtually constant ∼20 ms). The dead-times estimated from the phase-shift observed in C (not shown) and from the impulse response (F) behave very similarly, vindicating the analysis. G, Noise-free coherence, γNF, indicates the frequency range where a photoreceptor, if operating linearly, would reproduce exactly the same response at each stimulus presentation. γNF departs from unity at certain frequencies, reflecting selective nonlinearities, which enhance particular features of the stimulus. The bandwidths of the coherences, H, are defined as the frequency beyond which γ<0.5. The bandwidths increase with brightening BGs, reflecting the photoreceptor's ability to follow the stimulus on a shorter time-scale (γlin). This increased precision takes place in a frequency range where the photoreceptor encodes linearly the WN stimulus (γNF>γlin at each BG).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2367440&req=5

pone-0002173-g003: Voltage responses to a WN light stimulus: analysis of the transfer properties of the photoreceptor.Analysis of the transfer properties of the photoreceptor, based on the cross-spectrum between the stimulus and the signal (Fig. 1C, left). A, Gain is the norm of the frequency response (see Materials and Methods). It displays the range and extent of stimulus frequencies the cell amplify linearly. B, Areas (integrals) under gain curves at different BGs, and D, corresponding 3 dB cut-off frequencies. The amplification increases with the light BGs whereas the cut-off frequency remains virtually unchanged. C, Phase of the frequency response and the minimum phase, calculated from the gain curves, exhibits a phase-lag. E, Impulse response K1 is calculated from the frequency response function (real parts seen as gain, A, and phase, C). It approximates the linear filtering properties of the system. Brightening increases its area, scaling closely with the gain power (not shown), and reduces its onset-delay, F, as well as its time-to-peak (the delay between onset and peak is virtually constant ∼20 ms). The dead-times estimated from the phase-shift observed in C (not shown) and from the impulse response (F) behave very similarly, vindicating the analysis. G, Noise-free coherence, γNF, indicates the frequency range where a photoreceptor, if operating linearly, would reproduce exactly the same response at each stimulus presentation. γNF departs from unity at certain frequencies, reflecting selective nonlinearities, which enhance particular features of the stimulus. The bandwidths of the coherences, H, are defined as the frequency beyond which γ<0.5. The bandwidths increase with brightening BGs, reflecting the photoreceptor's ability to follow the stimulus on a shorter time-scale (γlin). This increased precision takes place in a frequency range where the photoreceptor encodes linearly the WN stimulus (γNF>γlin at each BG).
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