Limits...
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.

Show MeSH
Voltage responses to a NS light pattern at 19°C.A, In separate experiments, a NS light pattern is repeatedly presented to a photoreceptor as dim and bright intensity variations. B, The superimposed traces show the corresponding voltage responses to the 20th stimulus presentations. For the bright NS the cell dedicates a larger voltage range for encoding the stimulus. C, Averaging over the 100 individual traces gives the corresponding signals, normalized to exhibit the differences in their timing. With the dim NS the voltage output of the photoreceptor follows the light input with a delay greater than the one with the bright NS by ∼1 ms. Nevertheless, the voltage responses can follow the same stimulus pattern, suggesting that the photoreceptor is utilizing the same frequency range at different BGs. This is confirmed by the analysis of the responses power spectra at different points during the repeated stimulation (3rd and 30th traces), D. Whilst the amplification is higher for bright NS, as was already apparent in A, the range of frequencies encoded is virtually the same. This is quantified by calculating the 3 dB cut-off frequency, f3 dB, which equals to 14 Hz in all cases. Comparing the spectra of the responses to the 3rd (left) and 30th (right) stimulation shows no additional adaptive trend, suggesting that the system adapts rapidly (after the 1st stimulation) to a relatively invariable coding state (see Text S1 and Fig. S2). The signal power spectra (not shown) look very similar to the power spectra of the responses, as expected from the high signal-to-noise ratio (Fig. 9).
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC2367440&req=5

pone-0002173-g008: Voltage responses to a NS light pattern at 19°C.A, In separate experiments, a NS light pattern is repeatedly presented to a photoreceptor as dim and bright intensity variations. B, The superimposed traces show the corresponding voltage responses to the 20th stimulus presentations. For the bright NS the cell dedicates a larger voltage range for encoding the stimulus. C, Averaging over the 100 individual traces gives the corresponding signals, normalized to exhibit the differences in their timing. With the dim NS the voltage output of the photoreceptor follows the light input with a delay greater than the one with the bright NS by ∼1 ms. Nevertheless, the voltage responses can follow the same stimulus pattern, suggesting that the photoreceptor is utilizing the same frequency range at different BGs. This is confirmed by the analysis of the responses power spectra at different points during the repeated stimulation (3rd and 30th traces), D. Whilst the amplification is higher for bright NS, as was already apparent in A, the range of frequencies encoded is virtually the same. This is quantified by calculating the 3 dB cut-off frequency, f3 dB, which equals to 14 Hz in all cases. Comparing the spectra of the responses to the 3rd (left) and 30th (right) stimulation shows no additional adaptive trend, suggesting that the system adapts rapidly (after the 1st stimulation) to a relatively invariable coding state (see Text S1 and Fig. S2). The signal power spectra (not shown) look very similar to the power spectra of the responses, as expected from the high signal-to-noise ratio (Fig. 9).

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 NS light pattern at 19°C.A, In separate experiments, a NS light pattern is repeatedly presented to a photoreceptor as dim and bright intensity variations. B, The superimposed traces show the corresponding voltage responses to the 20th stimulus presentations. For the bright NS the cell dedicates a larger voltage range for encoding the stimulus. C, Averaging over the 100 individual traces gives the corresponding signals, normalized to exhibit the differences in their timing. With the dim NS the voltage output of the photoreceptor follows the light input with a delay greater than the one with the bright NS by ∼1 ms. Nevertheless, the voltage responses can follow the same stimulus pattern, suggesting that the photoreceptor is utilizing the same frequency range at different BGs. This is confirmed by the analysis of the responses power spectra at different points during the repeated stimulation (3rd and 30th traces), D. Whilst the amplification is higher for bright NS, as was already apparent in A, the range of frequencies encoded is virtually the same. This is quantified by calculating the 3 dB cut-off frequency, f3 dB, which equals to 14 Hz in all cases. Comparing the spectra of the responses to the 3rd (left) and 30th (right) stimulation shows no additional adaptive trend, suggesting that the system adapts rapidly (after the 1st stimulation) to a relatively invariable coding state (see Text S1 and Fig. S2). The signal power spectra (not shown) look very similar to the power spectra of the responses, as expected from the high signal-to-noise ratio (Fig. 9).
© Copyright Policy
Related In: Results  -  Collection

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

pone-0002173-g008: Voltage responses to a NS light pattern at 19°C.A, In separate experiments, a NS light pattern is repeatedly presented to a photoreceptor as dim and bright intensity variations. B, The superimposed traces show the corresponding voltage responses to the 20th stimulus presentations. For the bright NS the cell dedicates a larger voltage range for encoding the stimulus. C, Averaging over the 100 individual traces gives the corresponding signals, normalized to exhibit the differences in their timing. With the dim NS the voltage output of the photoreceptor follows the light input with a delay greater than the one with the bright NS by ∼1 ms. Nevertheless, the voltage responses can follow the same stimulus pattern, suggesting that the photoreceptor is utilizing the same frequency range at different BGs. This is confirmed by the analysis of the responses power spectra at different points during the repeated stimulation (3rd and 30th traces), D. Whilst the amplification is higher for bright NS, as was already apparent in A, the range of frequencies encoded is virtually the same. This is quantified by calculating the 3 dB cut-off frequency, f3 dB, which equals to 14 Hz in all cases. Comparing the spectra of the responses to the 3rd (left) and 30th (right) stimulation shows no additional adaptive trend, suggesting that the system adapts rapidly (after the 1st stimulation) to a relatively invariable coding state (see Text S1 and Fig. S2). The signal power spectra (not shown) look very similar to the power spectra of the responses, as expected from the high signal-to-noise ratio (Fig. 9).
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