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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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Hyperpolarization-activated inward rectifying (IR) current. A) Hyperpolarizing voltage clamps from -74 mV to -124 mV elicited a small-amplitude IR current that activated slowly and showed no inactivation. The sharp transients at the end of the clamp currents are capacitive transients. B) The IR current was insensitive to changes in the external potassium concentration, ruling out potassium as the current carrier. Black circles with [K]o = 5 mM, white squares [K]o = 20 mM (mean ± SEM, n = 4). C) Replacing the NaCl in the bath with Na-gluconate reduced the IR current, indicating that the IR current is carried at least partly by chloride. Black circles are controls with NaCl, white squares are substitution experiments with Na-gluconate (mean ± SEM, n = 4).
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Figure 7: Hyperpolarization-activated inward rectifying (IR) current. A) Hyperpolarizing voltage clamps from -74 mV to -124 mV elicited a small-amplitude IR current that activated slowly and showed no inactivation. The sharp transients at the end of the clamp currents are capacitive transients. B) The IR current was insensitive to changes in the external potassium concentration, ruling out potassium as the current carrier. Black circles with [K]o = 5 mM, white squares [K]o = 20 mM (mean ± SEM, n = 4). C) Replacing the NaCl in the bath with Na-gluconate reduced the IR current, indicating that the IR current is carried at least partly by chloride. Black circles are controls with NaCl, white squares are substitution experiments with Na-gluconate (mean ± SEM, n = 4).

Mentions: In the Cl-containing bath solution the current clamp recordings exhibited an inwardly-rectifying response to negative current injections (Figure 1E). In the whole-cell voltage-clamp experiments under similar ionic conditions, hyperpolarization of the photoreceptors activated a small inward current (IR, Figure 7A). Increasing the extracellular K+ concentration from 5 mM to 20 mM had no effect on the IR current (Figure 7B), indicating that it is neither carried nor modulated by potassium. Substituting the extracellular NaCl with Na-gluconate reduced the IR current amplitude (Figure 7C). The voltage-dependence of the current and the Na-gluconate effect were similar to the CLC-2 channels [36], suggesting chloride as the main current carrier. Because the activation of this current took place in a negative voltage regime compared to the dark resting potential, it was not investigated further here.


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)

Hyperpolarization-activated inward rectifying (IR) current. A) Hyperpolarizing voltage clamps from -74 mV to -124 mV elicited a small-amplitude IR current that activated slowly and showed no inactivation. The sharp transients at the end of the clamp currents are capacitive transients. B) The IR current was insensitive to changes in the external potassium concentration, ruling out potassium as the current carrier. Black circles with [K]o = 5 mM, white squares [K]o = 20 mM (mean ± SEM, n = 4). C) Replacing the NaCl in the bath with Na-gluconate reduced the IR current, indicating that the IR current is carried at least partly by chloride. Black circles are controls with NaCl, white squares are substitution experiments with Na-gluconate (mean ± SEM, n = 4).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 7: Hyperpolarization-activated inward rectifying (IR) current. A) Hyperpolarizing voltage clamps from -74 mV to -124 mV elicited a small-amplitude IR current that activated slowly and showed no inactivation. The sharp transients at the end of the clamp currents are capacitive transients. B) The IR current was insensitive to changes in the external potassium concentration, ruling out potassium as the current carrier. Black circles with [K]o = 5 mM, white squares [K]o = 20 mM (mean ± SEM, n = 4). C) Replacing the NaCl in the bath with Na-gluconate reduced the IR current, indicating that the IR current is carried at least partly by chloride. Black circles are controls with NaCl, white squares are substitution experiments with Na-gluconate (mean ± SEM, n = 4).
Mentions: In the Cl-containing bath solution the current clamp recordings exhibited an inwardly-rectifying response to negative current injections (Figure 1E). In the whole-cell voltage-clamp experiments under similar ionic conditions, hyperpolarization of the photoreceptors activated a small inward current (IR, Figure 7A). Increasing the extracellular K+ concentration from 5 mM to 20 mM had no effect on the IR current (Figure 7B), indicating that it is neither carried nor modulated by potassium. Substituting the extracellular NaCl with Na-gluconate reduced the IR current amplitude (Figure 7C). The voltage-dependence of the current and the Na-gluconate effect were similar to the CLC-2 channels [36], suggesting chloride as the main current carrier. Because the activation of this current took place in a negative voltage regime compared to the dark resting potential, it was not investigated further here.

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