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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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Related in: MedlinePlus

The photoreceptors enhance transient features of the stimulus and flatten the probability density of the transmitted frequencies.The reliability of temporal patterns in the photoreceptor responses is analyzed by comparing the average response, A (i.e. signal), to the time-dependent variability of the voltage responses, B (i.e. noise SD), evoked by a NS sequence. The probability distributions of these functions are shown in right. Noise SD is non-uniform across the stimulation pattern, calculated for every time-point across the voltage traces to the last 90 presentations of the NS light pattern (the first 10 showing an adapting trend), at the bright BG at 19°C. At every time-point (left) the spread of voltage values of the responses follows an individual distribution, varying from skewed to Gaussian; however, their overall probability distribution approximates a Gaussian (right). The changes in noise SD are then compared to the SNR, C, estimated by calculating the signal SD and the noise SD over 5 consecutive time points (using a 10-point window gives similar results). Notice that the amplitude of the rate of change in the signal, i.e. the absolute value of its time derivative (red trace), behaves similarly as the SNR, indicating that the locust photoreceptors encode most efficiently fast voltage changes. D, By ignoring their temporal order, 1000 values for (noise SD and signal) and (noise SD and rate of change of signal) are displayed as functions of voltage and rate of voltage change, respectively. The noise SD depends mostly on the rate of voltage change (linear fit slope = 0.08 ms, R = 0.26) and little on the instantaneous voltage value (linear fit slope = 0, R = −0.08). Notice that the noise SD does not only depend on the absolute value but also on the sign of the derivative. This could imply that there is an asymmetrical step in the phototransduction cascade, possibly arising from a process that involves 2 different time-constant for the transition between 2 different states (e.g. phosphorylated/non-phosphorylated). Such asymmetry would naturally occur if the 2 transitions involved 2 different enzymes. Alternatively, fast membrane dynamics or synaptic feedbacks could enhance depolarizing and hyperpolarizing response patterns asymmetrically. E, The normalized power spectra of the NS stimulus (ordinate units c2 Hz−1) and of one stretch of the photoreceptor response (as in Fig. 8, at bright BG, ordinate units mV2 Hz−1) illustrates how the cell enhances selected stimulus frequencies, whitening its output and increasing the entropy of transmitted signals.
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pone-0002173-g012: The photoreceptors enhance transient features of the stimulus and flatten the probability density of the transmitted frequencies.The reliability of temporal patterns in the photoreceptor responses is analyzed by comparing the average response, A (i.e. signal), to the time-dependent variability of the voltage responses, B (i.e. noise SD), evoked by a NS sequence. The probability distributions of these functions are shown in right. Noise SD is non-uniform across the stimulation pattern, calculated for every time-point across the voltage traces to the last 90 presentations of the NS light pattern (the first 10 showing an adapting trend), at the bright BG at 19°C. At every time-point (left) the spread of voltage values of the responses follows an individual distribution, varying from skewed to Gaussian; however, their overall probability distribution approximates a Gaussian (right). The changes in noise SD are then compared to the SNR, C, estimated by calculating the signal SD and the noise SD over 5 consecutive time points (using a 10-point window gives similar results). Notice that the amplitude of the rate of change in the signal, i.e. the absolute value of its time derivative (red trace), behaves similarly as the SNR, indicating that the locust photoreceptors encode most efficiently fast voltage changes. D, By ignoring their temporal order, 1000 values for (noise SD and signal) and (noise SD and rate of change of signal) are displayed as functions of voltage and rate of voltage change, respectively. The noise SD depends mostly on the rate of voltage change (linear fit slope = 0.08 ms, R = 0.26) and little on the instantaneous voltage value (linear fit slope = 0, R = −0.08). Notice that the noise SD does not only depend on the absolute value but also on the sign of the derivative. This could imply that there is an asymmetrical step in the phototransduction cascade, possibly arising from a process that involves 2 different time-constant for the transition between 2 different states (e.g. phosphorylated/non-phosphorylated). Such asymmetry would naturally occur if the 2 transitions involved 2 different enzymes. Alternatively, fast membrane dynamics or synaptic feedbacks could enhance depolarizing and hyperpolarizing response patterns asymmetrically. E, The normalized power spectra of the NS stimulus (ordinate units c2 Hz−1) and of one stretch of the photoreceptor response (as in Fig. 8, at bright BG, ordinate units mV2 Hz−1) illustrates how the cell enhances selected stimulus frequencies, whitening its output and increasing the entropy of transmitted signals.

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)

The photoreceptors enhance transient features of the stimulus and flatten the probability density of the transmitted frequencies.The reliability of temporal patterns in the photoreceptor responses is analyzed by comparing the average response, A (i.e. signal), to the time-dependent variability of the voltage responses, B (i.e. noise SD), evoked by a NS sequence. The probability distributions of these functions are shown in right. Noise SD is non-uniform across the stimulation pattern, calculated for every time-point across the voltage traces to the last 90 presentations of the NS light pattern (the first 10 showing an adapting trend), at the bright BG at 19°C. At every time-point (left) the spread of voltage values of the responses follows an individual distribution, varying from skewed to Gaussian; however, their overall probability distribution approximates a Gaussian (right). The changes in noise SD are then compared to the SNR, C, estimated by calculating the signal SD and the noise SD over 5 consecutive time points (using a 10-point window gives similar results). Notice that the amplitude of the rate of change in the signal, i.e. the absolute value of its time derivative (red trace), behaves similarly as the SNR, indicating that the locust photoreceptors encode most efficiently fast voltage changes. D, By ignoring their temporal order, 1000 values for (noise SD and signal) and (noise SD and rate of change of signal) are displayed as functions of voltage and rate of voltage change, respectively. The noise SD depends mostly on the rate of voltage change (linear fit slope = 0.08 ms, R = 0.26) and little on the instantaneous voltage value (linear fit slope = 0, R = −0.08). Notice that the noise SD does not only depend on the absolute value but also on the sign of the derivative. This could imply that there is an asymmetrical step in the phototransduction cascade, possibly arising from a process that involves 2 different time-constant for the transition between 2 different states (e.g. phosphorylated/non-phosphorylated). Such asymmetry would naturally occur if the 2 transitions involved 2 different enzymes. Alternatively, fast membrane dynamics or synaptic feedbacks could enhance depolarizing and hyperpolarizing response patterns asymmetrically. E, The normalized power spectra of the NS stimulus (ordinate units c2 Hz−1) and of one stretch of the photoreceptor response (as in Fig. 8, at bright BG, ordinate units mV2 Hz−1) illustrates how the cell enhances selected stimulus frequencies, whitening its output and increasing the entropy of transmitted signals.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2367440&req=5

pone-0002173-g012: The photoreceptors enhance transient features of the stimulus and flatten the probability density of the transmitted frequencies.The reliability of temporal patterns in the photoreceptor responses is analyzed by comparing the average response, A (i.e. signal), to the time-dependent variability of the voltage responses, B (i.e. noise SD), evoked by a NS sequence. The probability distributions of these functions are shown in right. Noise SD is non-uniform across the stimulation pattern, calculated for every time-point across the voltage traces to the last 90 presentations of the NS light pattern (the first 10 showing an adapting trend), at the bright BG at 19°C. At every time-point (left) the spread of voltage values of the responses follows an individual distribution, varying from skewed to Gaussian; however, their overall probability distribution approximates a Gaussian (right). The changes in noise SD are then compared to the SNR, C, estimated by calculating the signal SD and the noise SD over 5 consecutive time points (using a 10-point window gives similar results). Notice that the amplitude of the rate of change in the signal, i.e. the absolute value of its time derivative (red trace), behaves similarly as the SNR, indicating that the locust photoreceptors encode most efficiently fast voltage changes. D, By ignoring their temporal order, 1000 values for (noise SD and signal) and (noise SD and rate of change of signal) are displayed as functions of voltage and rate of voltage change, respectively. The noise SD depends mostly on the rate of voltage change (linear fit slope = 0.08 ms, R = 0.26) and little on the instantaneous voltage value (linear fit slope = 0, R = −0.08). Notice that the noise SD does not only depend on the absolute value but also on the sign of the derivative. This could imply that there is an asymmetrical step in the phototransduction cascade, possibly arising from a process that involves 2 different time-constant for the transition between 2 different states (e.g. phosphorylated/non-phosphorylated). Such asymmetry would naturally occur if the 2 transitions involved 2 different enzymes. Alternatively, fast membrane dynamics or synaptic feedbacks could enhance depolarizing and hyperpolarizing response patterns asymmetrically. E, The normalized power spectra of the NS stimulus (ordinate units c2 Hz−1) and of one stretch of the photoreceptor response (as in Fig. 8, at bright BG, ordinate units mV2 Hz−1) illustrates how the cell enhances selected stimulus frequencies, whitening its output and increasing the entropy of transmitted signals.
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