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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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Membrane properties deduced from the current steps experiment.Voltage responses to the injected current steps were used to investigate the transmission properties of the photoreceptor membrane (Fig. S1). A, Membrane time-constant, τ, is greatly reduced from the dark-adapted state by dim light adaptation, but it reduces only slightly further with brightening BGs; i.e. the membrane ‘switches’ from a dark to a light-adapted state. B, Membrane resistance, R, displays a complex behavior in the light BG–temperature plane that correlates with the duration of the bumps, estimated from the noise power spectra (Fig. 6D). C, Mean membrane potential MMP shows that the light-induced depolarization increases by ∼15 mV from dark to bright BG, yet it is virtually temperature insensitive.
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pone-0002173-g010: Membrane properties deduced from the current steps experiment.Voltage responses to the injected current steps were used to investigate the transmission properties of the photoreceptor membrane (Fig. S1). A, Membrane time-constant, τ, is greatly reduced from the dark-adapted state by dim light adaptation, but it reduces only slightly further with brightening BGs; i.e. the membrane ‘switches’ from a dark to a light-adapted state. B, Membrane resistance, R, displays a complex behavior in the light BG–temperature plane that correlates with the duration of the bumps, estimated from the noise power spectra (Fig. 6D). C, Mean membrane potential MMP shows that the light-induced depolarization increases by ∼15 mV from dark to bright BG, yet it is virtually temperature insensitive.

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)

Membrane properties deduced from the current steps experiment.Voltage responses to the injected current steps were used to investigate the transmission properties of the photoreceptor membrane (Fig. S1). A, Membrane time-constant, τ, is greatly reduced from the dark-adapted state by dim light adaptation, but it reduces only slightly further with brightening BGs; i.e. the membrane ‘switches’ from a dark to a light-adapted state. B, Membrane resistance, R, displays a complex behavior in the light BG–temperature plane that correlates with the duration of the bumps, estimated from the noise power spectra (Fig. 6D). C, Mean membrane potential MMP shows that the light-induced depolarization increases by ∼15 mV from dark to bright BG, yet it is virtually temperature insensitive.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2367440&req=5

pone-0002173-g010: Membrane properties deduced from the current steps experiment.Voltage responses to the injected current steps were used to investigate the transmission properties of the photoreceptor membrane (Fig. S1). A, Membrane time-constant, τ, is greatly reduced from the dark-adapted state by dim light adaptation, but it reduces only slightly further with brightening BGs; i.e. the membrane ‘switches’ from a dark to a light-adapted state. B, Membrane resistance, R, displays a complex behavior in the light BG–temperature plane that correlates with the duration of the bumps, estimated from the noise power spectra (Fig. 6D). C, Mean membrane potential MMP shows that the light-induced depolarization increases by ∼15 mV from dark to bright BG, yet it is virtually temperature insensitive.
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