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

Salmela, I.; Immonen, Esa-Ville LU ; Frolov, R.; Krause, S.; Krause, Y.; Vahasoyrinki, M. and Weckstrom, M. (2012) In BMC Neuroscience 13. p.93-93
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... (More)
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. (Less)
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organization
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Contribution to journal
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published
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keywords
Photoreceptor Cells, Photic Stimulation, Patch-Clamp Techniques, Biological, Models, Membrane Potentials/drug effects/*physiology, Light, In Vitro Techniques, Electric Stimulation, Computer Simulation, Cockroaches, Animals, Biophysical Phenomena/drug effects/*physiology, Invertebrate/*physiology, Potassium/metabolism, Potassium Channel Blockers/pharmacology, Potassium Channels/drug effects/*physiology, Tetraethylammonium/pharmacology
in
BMC Neuroscience
volume
13
pages
93 - 93
publisher
BioMed Central
external identifiers
  • Scopus:84864502309
ISSN
1471-2202
DOI
10.1186/1471-2202-13-93
language
English
LU publication?
yes
id
8c427004-ad30-4493-98a5-898510029992 (old id 5431803)
alternative location
http://www.ncbi.nlm.nih.gov/pubmed/22867024
date added to LUP
2015-06-16 15:07:14
date last changed
2016-10-13 04:26:29
@misc{8c427004-ad30-4493-98a5-898510029992,
  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.},
  author       = {Salmela, I. and Immonen, Esa-Ville and Frolov, R. and Krause, S. and Krause, Y. and Vahasoyrinki, M. and Weckstrom, M.},
  issn         = {1471-2202},
  keyword      = {Photoreceptor Cells,Photic Stimulation,Patch-Clamp Techniques,Biological,Models,Membrane Potentials/drug effects/*physiology,Light,In Vitro Techniques,Electric Stimulation,Computer Simulation,Cockroaches,Animals,Biophysical Phenomena/drug effects/*physiology,Invertebrate/*physiology,Potassium/metabolism,Potassium Channel Blockers/pharmacology,Potassium Channels/drug effects/*physiology,Tetraethylammonium/pharmacology},
  language     = {eng},
  pages        = {93--93},
  publisher    = {ARRAY(0xa774180)},
  series       = {BMC Neuroscience},
  title        = {Cellular elements for seeing in the dark: voltage-dependent conductances in cockroach photoreceptors},
  url          = {http://dx.doi.org/10.1186/1471-2202-13-93},
  volume       = {13},
  year         = {2012},
}