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Cellular elements for seeing in the dark: voltage-dependent conductances in cockroach photoreceptors

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 syst...

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Autores principales: Salmela, Iikka, Immonen, Esa-Ville, Frolov, Roman, Krause, Stephan, Krause, Yani, Vähäsöyrinki, Mikko, Weckström, Matti
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3472236/
https://www.ncbi.nlm.nih.gov/pubmed/22867024
http://dx.doi.org/10.1186/1471-2202-13-93
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author Salmela, Iikka
Immonen, Esa-Ville
Frolov, Roman
Krause, Stephan
Krause, Yani
Vähäsöyrinki, Mikko
Weckström, Matti
author_facet Salmela, Iikka
Immonen, Esa-Ville
Frolov, Roman
Krause, Stephan
Krause, Yani
Vähäsöyrinki, Mikko
Weckström, Matti
author_sort Salmela, Iikka
collection PubMed
description 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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spelling pubmed-34722362012-10-23 Cellular elements for seeing in the dark: voltage-dependent conductances in cockroach photoreceptors Salmela, Iikka Immonen, Esa-Ville Frolov, Roman Krause, Stephan Krause, Yani Vähäsöyrinki, Mikko Weckström, Matti BMC Neurosci Research Article 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. BioMed Central 2012-08-06 /pmc/articles/PMC3472236/ /pubmed/22867024 http://dx.doi.org/10.1186/1471-2202-13-93 Text en Copyright ©2012 Salmela et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Salmela, Iikka
Immonen, Esa-Ville
Frolov, Roman
Krause, Stephan
Krause, Yani
Vähäsöyrinki, Mikko
Weckström, Matti
Cellular elements for seeing in the dark: voltage-dependent conductances in cockroach photoreceptors
title Cellular elements for seeing in the dark: voltage-dependent conductances in cockroach photoreceptors
title_full Cellular elements for seeing in the dark: voltage-dependent conductances in cockroach photoreceptors
title_fullStr Cellular elements for seeing in the dark: voltage-dependent conductances in cockroach photoreceptors
title_full_unstemmed Cellular elements for seeing in the dark: voltage-dependent conductances in cockroach photoreceptors
title_short Cellular elements for seeing in the dark: voltage-dependent conductances in cockroach photoreceptors
title_sort cellular elements for seeing in the dark: voltage-dependent conductances in cockroach photoreceptors
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3472236/
https://www.ncbi.nlm.nih.gov/pubmed/22867024
http://dx.doi.org/10.1186/1471-2202-13-93
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