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Cellular elements for seeing in the dark: voltage-dependent conductances in cockroach photoreceptors.

Salmela I, Immonen EV, Frolov R, Krause S, Krause Y, Vähäsöyrinki M, Weckström M - BMC Neurosci (2012)

Bottom Line: Two voltage-dependent potassium conductances were found in the photoreceptors: a delayed rectifier type (KDR) and a fast transient inactivating type (KA).However, larger KA conductances were found in smaller and rapidly adapting photoreceptors, where KA could have a functional role.In general, the varying deployment of stereotypical K+ conductances in insect photoreceptors highlights their functional flexibility in neural coding.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Physics, University of Oulu, Oulu, Finland.

ABSTRACT

Background: The importance of voltage-dependent conductances in sensory information processing is well-established in insect photoreceptors. Here we present the characterization of electrical properties in photoreceptors of the cockroach (Periplaneta americana), a nocturnal insect with a visual system adapted for dim light.

Results: Whole-cell patch-clamped photoreceptors had high capacitances and input resistances, indicating large photosensitive rhabdomeres suitable for efficient photon capture and amplification of small photocurrents at low light levels. Two voltage-dependent potassium conductances were found in the photoreceptors: a delayed rectifier type (KDR) and a fast transient inactivating type (KA). Activation of KDR occurred during physiological voltage responses induced by light stimulation, whereas KA was nearly fully inactivated already at the dark resting potential. In addition, hyperpolarization of photoreceptors activated a small-amplitude inward-rectifying (IR) current mediated at least partially by chloride. Computer simulations showed that KDR shapes light responses by opposing the light-induced depolarization and speeding up the membrane time constant, whereas KA and IR have a negligible role in the majority of cells. However, larger KA conductances were found in smaller and rapidly adapting photoreceptors, where KA could have a functional role.

Conclusions: The relative expression of KA and KDR in cockroach photoreceptors was opposite to the previously hypothesized framework for dark-active insects, necessitating further comparative work on the conductances. In general, the varying deployment of stereotypical K+ conductances in insect photoreceptors highlights their functional flexibility in neural coding.

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Effect of varying the maximum conductances of the KDR and KA in the simulations. A) Light responses were simulated with 10% (top trace), 100% (gray trace), 200% and 1000% (lowest traces) of the experimentally determined mean KDR maximum conductance. B) Modifying the maximal KA conductance had no effect on the simulated light response. The responses were simulated with 0%, 100%, 200% and 1000% KA conductances relative to the standard simulation value of 60 nS. Due to minimal differences in the responses the traces overlap.
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Figure 10: Effect of varying the maximum conductances of the KDR and KA in the simulations. A) Light responses were simulated with 10% (top trace), 100% (gray trace), 200% and 1000% (lowest traces) of the experimentally determined mean KDR maximum conductance. B) Modifying the maximal KA conductance had no effect on the simulated light response. The responses were simulated with 0%, 100%, 200% and 1000% KA conductances relative to the standard simulation value of 60 nS. Due to minimal differences in the responses the traces overlap.

Mentions: To determine the roles of KDR and KA during light responses, a Hodgkin-Huxley type model of a cockroach photoreceptor was implemented following similar approach as previously described in Drosophila[3]. The model was based on the experimentally determined light-induced conductance (Figure 1D), the voltage- and time-dependent properties of KA and KDR (Figure 4), and the values of the resting potential, the capacitance and the input resistance. Simulated voltage clamps (Appendix, Figure 8) and light responses to a 10 s naturalistic contrast stimulus (Figure 9A, c.f. Figure 1D) behaved similarly to the experiments, and thus the various currents underlying the voltage responses could be estimated with the model. During the simulated light responses KDR activated strongly, producing currents up to 1 nA (Figure 9B). Conversely, KA currents during the light responses were small and the maximal KA current during the initial voltage transient was only ca. 40 pA (Figure 9C). The strong inactivation at physiological voltages kept KA currents very small throughout the simulations. As a test of the significance of the KDR, its partial removal from the model down to 10% of the mean experimentally determined conductance values increased the depolarization level of the light responses (Figure 10A). Conversely, increasing the KDR conductance up to 10-fold decreased the amplitude and speeded up the voltage response (Figure 10A). Varying the KA maximum conductance from zero to ten-fold from the experimentally determined value had no visible effect on the simulated voltage responses (Figure 10B). Similarly, no effect was found when other steady-state KA parameters were varied within their minimum/maximum experimental ranges, i.e. V50 of activation (-43 to -40 mV) and inactivation (-88 to -84 mV) and the slopes of activation (6.2 to 10.5 mV) and inactivation (-14.3 to -8.5 mV). The possible influence of the dark resting potential on these results was checked by running simulations using resting potentials ranging from -80 to -50 mV. With more hyperpolarized resting potentials the initial KA transients became larger but soon after the onset of the light stimulation the KA quickly inactivated to very low levels, similar to the standard simulation conditions. The overlap between the KA steady-state activation and inactivation (Figure 4D) indicated that the channel is partially activated already at dark resting potential at ca. -60 mV, although the conductance is small (ca. 0.08 nS). Since the graded voltage changes were slow compared to the kinetics of KA, inactivation always dominated and KA thus remained mostly inactivated after the initial transient.


Cellular elements for seeing in the dark: voltage-dependent conductances in cockroach photoreceptors.

Salmela I, Immonen EV, Frolov R, Krause S, Krause Y, Vähäsöyrinki M, Weckström M - BMC Neurosci (2012)

Effect of varying the maximum conductances of the KDR and KA in the simulations. A) Light responses were simulated with 10% (top trace), 100% (gray trace), 200% and 1000% (lowest traces) of the experimentally determined mean KDR maximum conductance. B) Modifying the maximal KA conductance had no effect on the simulated light response. The responses were simulated with 0%, 100%, 200% and 1000% KA conductances relative to the standard simulation value of 60 nS. Due to minimal differences in the responses the traces overlap.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3472236&req=5

Figure 10: Effect of varying the maximum conductances of the KDR and KA in the simulations. A) Light responses were simulated with 10% (top trace), 100% (gray trace), 200% and 1000% (lowest traces) of the experimentally determined mean KDR maximum conductance. B) Modifying the maximal KA conductance had no effect on the simulated light response. The responses were simulated with 0%, 100%, 200% and 1000% KA conductances relative to the standard simulation value of 60 nS. Due to minimal differences in the responses the traces overlap.
Mentions: To determine the roles of KDR and KA during light responses, a Hodgkin-Huxley type model of a cockroach photoreceptor was implemented following similar approach as previously described in Drosophila[3]. The model was based on the experimentally determined light-induced conductance (Figure 1D), the voltage- and time-dependent properties of KA and KDR (Figure 4), and the values of the resting potential, the capacitance and the input resistance. Simulated voltage clamps (Appendix, Figure 8) and light responses to a 10 s naturalistic contrast stimulus (Figure 9A, c.f. Figure 1D) behaved similarly to the experiments, and thus the various currents underlying the voltage responses could be estimated with the model. During the simulated light responses KDR activated strongly, producing currents up to 1 nA (Figure 9B). Conversely, KA currents during the light responses were small and the maximal KA current during the initial voltage transient was only ca. 40 pA (Figure 9C). The strong inactivation at physiological voltages kept KA currents very small throughout the simulations. As a test of the significance of the KDR, its partial removal from the model down to 10% of the mean experimentally determined conductance values increased the depolarization level of the light responses (Figure 10A). Conversely, increasing the KDR conductance up to 10-fold decreased the amplitude and speeded up the voltage response (Figure 10A). Varying the KA maximum conductance from zero to ten-fold from the experimentally determined value had no visible effect on the simulated voltage responses (Figure 10B). Similarly, no effect was found when other steady-state KA parameters were varied within their minimum/maximum experimental ranges, i.e. V50 of activation (-43 to -40 mV) and inactivation (-88 to -84 mV) and the slopes of activation (6.2 to 10.5 mV) and inactivation (-14.3 to -8.5 mV). The possible influence of the dark resting potential on these results was checked by running simulations using resting potentials ranging from -80 to -50 mV. With more hyperpolarized resting potentials the initial KA transients became larger but soon after the onset of the light stimulation the KA quickly inactivated to very low levels, similar to the standard simulation conditions. The overlap between the KA steady-state activation and inactivation (Figure 4D) indicated that the channel is partially activated already at dark resting potential at ca. -60 mV, although the conductance is small (ca. 0.08 nS). Since the graded voltage changes were slow compared to the kinetics of KA, inactivation always dominated and KA thus remained mostly inactivated after the initial transient.

Bottom Line: Two voltage-dependent potassium conductances were found in the photoreceptors: a delayed rectifier type (KDR) and a fast transient inactivating type (KA).However, larger KA conductances were found in smaller and rapidly adapting photoreceptors, where KA could have a functional role.In general, the varying deployment of stereotypical K+ conductances in insect photoreceptors highlights their functional flexibility in neural coding.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Physics, University of Oulu, Oulu, Finland.

ABSTRACT

Background: The importance of voltage-dependent conductances in sensory information processing is well-established in insect photoreceptors. Here we present the characterization of electrical properties in photoreceptors of the cockroach (Periplaneta americana), a nocturnal insect with a visual system adapted for dim light.

Results: Whole-cell patch-clamped photoreceptors had high capacitances and input resistances, indicating large photosensitive rhabdomeres suitable for efficient photon capture and amplification of small photocurrents at low light levels. Two voltage-dependent potassium conductances were found in the photoreceptors: a delayed rectifier type (KDR) and a fast transient inactivating type (KA). Activation of KDR occurred during physiological voltage responses induced by light stimulation, whereas KA was nearly fully inactivated already at the dark resting potential. In addition, hyperpolarization of photoreceptors activated a small-amplitude inward-rectifying (IR) current mediated at least partially by chloride. Computer simulations showed that KDR shapes light responses by opposing the light-induced depolarization and speeding up the membrane time constant, whereas KA and IR have a negligible role in the majority of cells. However, larger KA conductances were found in smaller and rapidly adapting photoreceptors, where KA could have a functional role.

Conclusions: The relative expression of KA and KDR in cockroach photoreceptors was opposite to the previously hypothesized framework for dark-active insects, necessitating further comparative work on the conductances. In general, the varying deployment of stereotypical K+ conductances in insect photoreceptors highlights their functional flexibility in neural coding.

Show MeSH
Related in: MedlinePlus