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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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Pharmacological properties of the Kv currents. Kv currents were elicited with a positive command potential, given after a negative inactivation-removal prepulse. Black traces are controls; gray traces are currents recorded after drug application. A) 1 mM 4-AP suppressed the transient KA component. B) 50 mM TEA blocked KDR partially. C) 1 mM quinidine blocked both KDR and KA. D) Concentration dependence of the quinidine block for the KDR (mean ± SD, n = 3 to 5). The fitted curve is a logistical function 1/(1 + ([quin]/IC50)p), with half-inhibition concentration IC50 = 32 ± 3 μM and Hill slope p = 0.97 ± 0.08 (mean ± SE).
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Figure 6: Pharmacological properties of the Kv currents. Kv currents were elicited with a positive command potential, given after a negative inactivation-removal prepulse. Black traces are controls; gray traces are currents recorded after drug application. A) 1 mM 4-AP suppressed the transient KA component. B) 50 mM TEA blocked KDR partially. C) 1 mM quinidine blocked both KDR and KA. D) Concentration dependence of the quinidine block for the KDR (mean ± SD, n = 3 to 5). The fitted curve is a logistical function 1/(1 + ([quin]/IC50)p), with half-inhibition concentration IC50 = 32 ± 3 μM and Hill slope p = 0.97 ± 0.08 (mean ± SE).

Mentions: Pharmacological properties of Kv currents were tested with a number of Kv channel blockers in whole-cell voltage clamp (Figure 6A-D). 4-aminopyridine (4-AP) typically blocks A-type Kv currents at high micro- to millimolar concentrations [34]. Application of 1 mM 4-AP in the extracellular solution inhibited the transient KA current, but had no effect on the KDR current (Figure 6A). Tetraethylammonium (TEA), a common blocker of delayed rectifier Kv currents, inhibited the non-inactivating KDR only partially at a high concentration of 50 mM (Figure 6B). Quinidine, a non-specific blocker of various Kv currents in insect neurons [15,34], inhibited the transient KA current at 1 mM extracellular concentration (Figure 6C) and the slow-activating KDR (Figure 6D) with half-maximum inhibitory concentration of IC50 = 32 ± 3 μM and Hill coefficient of 0.97 ± 0.08 (mean ± SE). Although quinidine inhibited the KDR current well, it had other effects, possibly mediated by interference with the light-gated channels or their activation; thus using it during light responses produced inconclusive results and was not investigated further. Application of 100 nM α-dendrotoxin, a potent blocker of Shaker A-type Kv channels [35], did not block KA or KDR (data not shown).


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)

Pharmacological properties of the Kv currents. Kv currents were elicited with a positive command potential, given after a negative inactivation-removal prepulse. Black traces are controls; gray traces are currents recorded after drug application. A) 1 mM 4-AP suppressed the transient KA component. B) 50 mM TEA blocked KDR partially. C) 1 mM quinidine blocked both KDR and KA. D) Concentration dependence of the quinidine block for the KDR (mean ± SD, n = 3 to 5). The fitted curve is a logistical function 1/(1 + ([quin]/IC50)p), with half-inhibition concentration IC50 = 32 ± 3 μM and Hill slope p = 0.97 ± 0.08 (mean ± SE).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 6: Pharmacological properties of the Kv currents. Kv currents were elicited with a positive command potential, given after a negative inactivation-removal prepulse. Black traces are controls; gray traces are currents recorded after drug application. A) 1 mM 4-AP suppressed the transient KA component. B) 50 mM TEA blocked KDR partially. C) 1 mM quinidine blocked both KDR and KA. D) Concentration dependence of the quinidine block for the KDR (mean ± SD, n = 3 to 5). The fitted curve is a logistical function 1/(1 + ([quin]/IC50)p), with half-inhibition concentration IC50 = 32 ± 3 μM and Hill slope p = 0.97 ± 0.08 (mean ± SE).
Mentions: Pharmacological properties of Kv currents were tested with a number of Kv channel blockers in whole-cell voltage clamp (Figure 6A-D). 4-aminopyridine (4-AP) typically blocks A-type Kv currents at high micro- to millimolar concentrations [34]. Application of 1 mM 4-AP in the extracellular solution inhibited the transient KA current, but had no effect on the KDR current (Figure 6A). Tetraethylammonium (TEA), a common blocker of delayed rectifier Kv currents, inhibited the non-inactivating KDR only partially at a high concentration of 50 mM (Figure 6B). Quinidine, a non-specific blocker of various Kv currents in insect neurons [15,34], inhibited the transient KA current at 1 mM extracellular concentration (Figure 6C) and the slow-activating KDR (Figure 6D) with half-maximum inhibitory concentration of IC50 = 32 ± 3 μM and Hill coefficient of 0.97 ± 0.08 (mean ± SE). Although quinidine inhibited the KDR current well, it had other effects, possibly mediated by interference with the light-gated channels or their activation; thus using it during light responses produced inconclusive results and was not investigated further. Application of 100 nM α-dendrotoxin, a potent blocker of Shaker A-type Kv channels [35], did not block KA or KDR (data not shown).

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