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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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Small cells have large KA conductances and small depolarization in response to light. A) KA and B) KDR conductances versus the whole-cell capacitances (n = 23). Conductances were calculated from the currents elicited by a voltage jump to -4 mV from -104 mV C) The light-induced steady-state depolarization was smaller in cells with lower whole-cell capacitances.
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Figure 5: Small cells have large KA conductances and small depolarization in response to light. A) KA and B) KDR conductances versus the whole-cell capacitances (n = 23). Conductances were calculated from the currents elicited by a voltage jump to -4 mV from -104 mV C) The light-induced steady-state depolarization was smaller in cells with lower whole-cell capacitances.

Mentions: To test if the measured capacitances were linked to other photoreceptor properties, we looked at Kv conductances and voltage light responses recorded in the same cells. Kv currents were elicited by a -4 mV voltage step given after a hyperpolarizing inactivation removal pulse. KDR steady-state and KA peak conductances were then calculated from the currents after series resistance correction. Larger KA conductances were found in small cells, whereas no KA conductance could be observed in large cells (Figure 5A). However, the capacitive transient arising from the whole-cell capacitance and access resistance might partly conceal the transient KA current in the cells with large capacitance. KDR conductances were found in all cells, and conductance values showed a positive trend with increasing capacitance (Figure 5B), and KDR conductance density was 0.14 ± 0.06 nS/pF (mean ± SD, n = 23). Voltage responses to a saturating 10 s long light pulse were recorded from the same photoreceptors. The depolarization at the end of the response was taken as a measure of light-induced voltage change that is the result of the interplay between the depolarizing light-induced current and the hyperpolarizing Kv currents that are activated by the depolarization. Light-induced steady-state depolarization was smaller in cells with lower than those with higher capacitances (Figure 5C) and the relationship between the depolarization whole-cell capacitance resembled the variability of light responses as reported by Heimonen et al. (2006). This suggests that the variability reported earlier is related to cell size, possibly due to fewer or more numerous microvilli in the smaller or larger rhabdomeres and, consequently,a smaller or larger amount of transducing channels.


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)

Small cells have large KA conductances and small depolarization in response to light. A) KA and B) KDR conductances versus the whole-cell capacitances (n = 23). Conductances were calculated from the currents elicited by a voltage jump to -4 mV from -104 mV C) The light-induced steady-state depolarization was smaller in cells with lower whole-cell capacitances.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 5: Small cells have large KA conductances and small depolarization in response to light. A) KA and B) KDR conductances versus the whole-cell capacitances (n = 23). Conductances were calculated from the currents elicited by a voltage jump to -4 mV from -104 mV C) The light-induced steady-state depolarization was smaller in cells with lower whole-cell capacitances.
Mentions: To test if the measured capacitances were linked to other photoreceptor properties, we looked at Kv conductances and voltage light responses recorded in the same cells. Kv currents were elicited by a -4 mV voltage step given after a hyperpolarizing inactivation removal pulse. KDR steady-state and KA peak conductances were then calculated from the currents after series resistance correction. Larger KA conductances were found in small cells, whereas no KA conductance could be observed in large cells (Figure 5A). However, the capacitive transient arising from the whole-cell capacitance and access resistance might partly conceal the transient KA current in the cells with large capacitance. KDR conductances were found in all cells, and conductance values showed a positive trend with increasing capacitance (Figure 5B), and KDR conductance density was 0.14 ± 0.06 nS/pF (mean ± SD, n = 23). Voltage responses to a saturating 10 s long light pulse were recorded from the same photoreceptors. The depolarization at the end of the response was taken as a measure of light-induced voltage change that is the result of the interplay between the depolarizing light-induced current and the hyperpolarizing Kv currents that are activated by the depolarization. Light-induced steady-state depolarization was smaller in cells with lower than those with higher capacitances (Figure 5C) and the relationship between the depolarization whole-cell capacitance resembled the variability of light responses as reported by Heimonen et al. (2006). This suggests that the variability reported earlier is related to cell size, possibly due to fewer or more numerous microvilli in the smaller or larger rhabdomeres and, consequently,a smaller or larger amount of transducing channels.

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