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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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Reversal potential of the sustained current followed the Nernst slope for potassium. The reversal potential was measured from tail currents with varying external K+ concentrations (inset), resulting in Erev = -68 mV under the standard 5 mM concentration (n = 17 (5 mM), 6 (15 and 50 mM) or 5 (25 mM), data are mean ± SD). The fitted Nernst slope (solid line) was 52 mV/mM and the theoretical Nernst slope (dashed line) for potassium was 58 mV/mM. Theoretical Erev with 5 mM [K+]out was -84 mV.
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Figure 3: Reversal potential of the sustained current followed the Nernst slope for potassium. The reversal potential was measured from tail currents with varying external K+ concentrations (inset), resulting in Erev = -68 mV under the standard 5 mM concentration (n = 17 (5 mM), 6 (15 and 50 mM) or 5 (25 mM), data are mean ± SD). The fitted Nernst slope (solid line) was 52 mV/mM and the theoretical Nernst slope (dashed line) for potassium was 58 mV/mM. Theoretical Erev with 5 mM [K+]out was -84 mV.

Mentions: The sustained current’s identity and selectivity was examined with tail currents recorded under different external potassium concentrations (Figure 3). The fitted Nernst slope was 52 ± 4 mV/mM (mean ± SE), close to the theoretical value of 58 mV/mM for potassium with the solutions used. Under standard K+ concentrations ([K]in/K]out = 5 mM/140 mM) the reversal potential of the current was -68 ± 5 mV (mean ± SD, n = 17). Theoretical Nernst potential for potassium was -84 mV, implying that the measured conductance was not entirely potassium-specific under multi-ionic conditions. The reversal potential was similar for chloride-containing and chloride-free solutions (see Methods for a description of solutions). Because of the overlap with the sustained current, the transient current’s reversal potential could not be measured reliably but was assumed to be the same as for the non-inactivating current, i.e. -68 mV, based on the close resemblance of both to K+ currents in insects [33]. The similarity of the voltage-dependent behaviour of the currents to previous findings in insects (Figure 2D-F) and the Nernst slope of the sustained current’s reversal potential (following K+ concentration and thus indicating a mainly K+ permeant channels; Figure 3) indicate that the currents are generated by voltage-dependent potassium (Kv) channels. Based on their similarities to delayed-rectifier and A-type Kv currents, the non-inactivating sustained current will be referred as KDR and the inactivating transient current as KA in the following.


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)

Reversal potential of the sustained current followed the Nernst slope for potassium. The reversal potential was measured from tail currents with varying external K+ concentrations (inset), resulting in Erev = -68 mV under the standard 5 mM concentration (n = 17 (5 mM), 6 (15 and 50 mM) or 5 (25 mM), data are mean ± SD). The fitted Nernst slope (solid line) was 52 mV/mM and the theoretical Nernst slope (dashed line) for potassium was 58 mV/mM. Theoretical Erev with 5 mM [K+]out was -84 mV.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: Reversal potential of the sustained current followed the Nernst slope for potassium. The reversal potential was measured from tail currents with varying external K+ concentrations (inset), resulting in Erev = -68 mV under the standard 5 mM concentration (n = 17 (5 mM), 6 (15 and 50 mM) or 5 (25 mM), data are mean ± SD). The fitted Nernst slope (solid line) was 52 mV/mM and the theoretical Nernst slope (dashed line) for potassium was 58 mV/mM. Theoretical Erev with 5 mM [K+]out was -84 mV.
Mentions: The sustained current’s identity and selectivity was examined with tail currents recorded under different external potassium concentrations (Figure 3). The fitted Nernst slope was 52 ± 4 mV/mM (mean ± SE), close to the theoretical value of 58 mV/mM for potassium with the solutions used. Under standard K+ concentrations ([K]in/K]out = 5 mM/140 mM) the reversal potential of the current was -68 ± 5 mV (mean ± SD, n = 17). Theoretical Nernst potential for potassium was -84 mV, implying that the measured conductance was not entirely potassium-specific under multi-ionic conditions. The reversal potential was similar for chloride-containing and chloride-free solutions (see Methods for a description of solutions). Because of the overlap with the sustained current, the transient current’s reversal potential could not be measured reliably but was assumed to be the same as for the non-inactivating current, i.e. -68 mV, based on the close resemblance of both to K+ currents in insects [33]. The similarity of the voltage-dependent behaviour of the currents to previous findings in insects (Figure 2D-F) and the Nernst slope of the sustained current’s reversal potential (following K+ concentration and thus indicating a mainly K+ permeant channels; Figure 3) indicate that the currents are generated by voltage-dependent potassium (Kv) channels. Based on their similarities to delayed-rectifier and A-type Kv currents, the non-inactivating sustained current will be referred as KDR and the inactivating transient current as KA in the following.

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