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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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Voltage-dependent properties of the Kv currents. A) Steady state activation and inactivation properties of the Kv currents (all data are mean ± SD). Black squares represent activation of the sustained KDR current (n = 6); gray symbols represent transient KA current’s activation (circles, n = 5) and inactivation (triangles, n = 4). The curves are the corresponding Boltzmann fits: KDR activation is a 1st order Boltzmann with V50 = -31 mV and slope = 12 mV. KA activation is a 2nd order Boltzmann with V50 = -43 mV and slope = 8.4 mV. KA inactivation is a 1st order Boltzmann with V50 = -85 mV and slope = -11 mV. B) Activation time constants of KDR (black squares, n = 8 to 14) and KA (gray circles, n = 5). KDR activation time constant was fitted with a bell-function τKDR = 1/(4·exp(-43*V) + 156·exp(43*V)) s, where V is voltage in volts. KA activation time constant was nearly voltage-independent and was thus set to constant 1.5 ms for the simulations. C) Time constant of the KA inactivation (n = 3 to 7). Bell function is τKA = 1/(341 ·exp(44·V) +0.211·exp(-44·V)) s, where V is voltage in volts. Inset: the inactivation recovery protocol used for voltages below -80 mV.
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Figure 4: Voltage-dependent properties of the Kv currents. A) Steady state activation and inactivation properties of the Kv currents (all data are mean ± SD). Black squares represent activation of the sustained KDR current (n = 6); gray symbols represent transient KA current’s activation (circles, n = 5) and inactivation (triangles, n = 4). The curves are the corresponding Boltzmann fits: KDR activation is a 1st order Boltzmann with V50 = -31 mV and slope = 12 mV. KA activation is a 2nd order Boltzmann with V50 = -43 mV and slope = 8.4 mV. KA inactivation is a 1st order Boltzmann with V50 = -85 mV and slope = -11 mV. B) Activation time constants of KDR (black squares, n = 8 to 14) and KA (gray circles, n = 5). KDR activation time constant was fitted with a bell-function τKDR = 1/(4·exp(-43*V) + 156·exp(43*V)) s, where V is voltage in volts. KA activation time constant was nearly voltage-independent and was thus set to constant 1.5 ms for the simulations. C) Time constant of the KA inactivation (n = 3 to 7). Bell function is τKA = 1/(341 ·exp(44·V) +0.211·exp(-44·V)) s, where V is voltage in volts. Inset: the inactivation recovery protocol used for voltages below -80 mV.

Mentions: KDR was isolated by giving voltage pulses from -47 to +23 mV in 10 mV steps after a -57 mV prepulse that inactivated the KA conductance (Figure 2E). Conductances were calculated from the steady-state currents and fitted with first order Boltzmann function g(V) = gmax/(1 + exp((V50 - V)/slope)), corresponding to 1st order kinetics for the activation. The resulting half-activation voltage (V50) was -31 ± 9 mV with slope factor of 12.0 ± 2.0 mV, and the maximum conductance (gmax) was 78 ± 22 nS (mean ± SD, n = 6), ranging between 40 and 90 nS. A normalized KDR activation profile is shown in Figure 4A (black squares and curve). Activation and deactivation kinetics were determined from single-exponential fits to activating currents or deactivating tail currents. At physiologically relevant voltages from -70 to -10 mV, KDR activation time constants fell between 20 and 11 ms (Figure 4B black squares).


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)

Voltage-dependent properties of the Kv currents. A) Steady state activation and inactivation properties of the Kv currents (all data are mean ± SD). Black squares represent activation of the sustained KDR current (n = 6); gray symbols represent transient KA current’s activation (circles, n = 5) and inactivation (triangles, n = 4). The curves are the corresponding Boltzmann fits: KDR activation is a 1st order Boltzmann with V50 = -31 mV and slope = 12 mV. KA activation is a 2nd order Boltzmann with V50 = -43 mV and slope = 8.4 mV. KA inactivation is a 1st order Boltzmann with V50 = -85 mV and slope = -11 mV. B) Activation time constants of KDR (black squares, n = 8 to 14) and KA (gray circles, n = 5). KDR activation time constant was fitted with a bell-function τKDR = 1/(4·exp(-43*V) + 156·exp(43*V)) s, where V is voltage in volts. KA activation time constant was nearly voltage-independent and was thus set to constant 1.5 ms for the simulations. C) Time constant of the KA inactivation (n = 3 to 7). Bell function is τKA = 1/(341 ·exp(44·V) +0.211·exp(-44·V)) s, where V is voltage in volts. Inset: the inactivation recovery protocol used for voltages below -80 mV.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
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Figure 4: Voltage-dependent properties of the Kv currents. A) Steady state activation and inactivation properties of the Kv currents (all data are mean ± SD). Black squares represent activation of the sustained KDR current (n = 6); gray symbols represent transient KA current’s activation (circles, n = 5) and inactivation (triangles, n = 4). The curves are the corresponding Boltzmann fits: KDR activation is a 1st order Boltzmann with V50 = -31 mV and slope = 12 mV. KA activation is a 2nd order Boltzmann with V50 = -43 mV and slope = 8.4 mV. KA inactivation is a 1st order Boltzmann with V50 = -85 mV and slope = -11 mV. B) Activation time constants of KDR (black squares, n = 8 to 14) and KA (gray circles, n = 5). KDR activation time constant was fitted with a bell-function τKDR = 1/(4·exp(-43*V) + 156·exp(43*V)) s, where V is voltage in volts. KA activation time constant was nearly voltage-independent and was thus set to constant 1.5 ms for the simulations. C) Time constant of the KA inactivation (n = 3 to 7). Bell function is τKA = 1/(341 ·exp(44·V) +0.211·exp(-44·V)) s, where V is voltage in volts. Inset: the inactivation recovery protocol used for voltages below -80 mV.
Mentions: KDR was isolated by giving voltage pulses from -47 to +23 mV in 10 mV steps after a -57 mV prepulse that inactivated the KA conductance (Figure 2E). Conductances were calculated from the steady-state currents and fitted with first order Boltzmann function g(V) = gmax/(1 + exp((V50 - V)/slope)), corresponding to 1st order kinetics for the activation. The resulting half-activation voltage (V50) was -31 ± 9 mV with slope factor of 12.0 ± 2.0 mV, and the maximum conductance (gmax) was 78 ± 22 nS (mean ± SD, n = 6), ranging between 40 and 90 nS. A normalized KDR activation profile is shown in Figure 4A (black squares and curve). Activation and deactivation kinetics were determined from single-exponential fits to activating currents or deactivating tail currents. At physiologically relevant voltages from -70 to -10 mV, KDR activation time constants fell between 20 and 11 ms (Figure 4B black squares).

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