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Visual ecology and potassium conductances of insect photoreceptors.

Frolov, Roman; Immonen, Esa-Ville LU and Weckström, Matti (2016) In Journal of Neurophysiology 115(4). p.2147-2157
Abstract
Voltage-activated potassium channels (Kv channels) in the microvillar photoreceptors of arthropods are responsible for repolarization and regulation of photoreceptor signaling bandwidth. On the basis of analyzing Kv channels in dipteran flies, it was suggested that diurnal, rapidly flying insects predominantly express sustained K+ conductances, whereas crepuscular and nocturnally active animals exhibit strongly inactivating Kv conductances. The latter was suggested to function for minimizing cellular energy consumption. In this study we further explore the evolutionary adaptations of the photoreceptor channelome to visual ecology and behavior by comparing K+ conductances in 15 phylogenetically diverse insects, using patch-clamp recordings... (More)
Voltage-activated potassium channels (Kv channels) in the microvillar photoreceptors of arthropods are responsible for repolarization and regulation of photoreceptor signaling bandwidth. On the basis of analyzing Kv channels in dipteran flies, it was suggested that diurnal, rapidly flying insects predominantly express sustained K+ conductances, whereas crepuscular and nocturnally active animals exhibit strongly inactivating Kv conductances. The latter was suggested to function for minimizing cellular energy consumption. In this study we further explore the evolutionary adaptations of the photoreceptor channelome to visual ecology and behavior by comparing K+ conductances in 15 phylogenetically diverse insects, using patch-clamp recordings from dissociated ommatidia. We show that rapid diurnal flyers such as the blowfly (Calliphora vicina) and the honeybee (Apis mellifera) express relatively large noninactivating Kv conductances, conforming to the earlier hypothesis in Diptera. Nocturnal and/or slow-moving species do not in general exhibit stronger Kv conductance inactivation in the physiological membrane voltage range, but the photoreceptors in species that are known to rely more on vision behaviorally had higher densities of sustained Kv conductances than photoreceptors of less visually guided species. No statistically significant trends related to visual performance could be identified for the rapidly inactivating Kv conductances. Counterintuitively, strong negative correlations were observed between photoreceptor capacitance and specific membrane conductance for both sustained and inactivating fractions of Kv conductance, suggesting insignificant evolutionary pressure to offset negative effects of high capacitance on membrane filtering with increased conductance. (Less)
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author
publishing date
type
Contribution to journal
publication status
published
subject
keywords
insect photoreceptor, potassium channels, compund eye, visual ecology
in
Journal of Neurophysiology
volume
115
issue
4
pages
2147 - 2157
publisher
American Physiological Society
external identifiers
  • Scopus:84984646187
ISSN
1522-1598
DOI
10.1152/jn.00795.2015
language
English
LU publication?
no
id
1b02e879-41a5-4cd0-99a2-8efc8c0a4125
date added to LUP
2016-07-04 10:50:47
date last changed
2017-01-01 08:29:48
@article{1b02e879-41a5-4cd0-99a2-8efc8c0a4125,
  abstract     = {Voltage-activated potassium channels (Kv channels) in the microvillar photoreceptors of arthropods are responsible for repolarization and regulation of photoreceptor signaling bandwidth. On the basis of analyzing Kv channels in dipteran flies, it was suggested that diurnal, rapidly flying insects predominantly express sustained K+ conductances, whereas crepuscular and nocturnally active animals exhibit strongly inactivating Kv conductances. The latter was suggested to function for minimizing cellular energy consumption. In this study we further explore the evolutionary adaptations of the photoreceptor channelome to visual ecology and behavior by comparing K+ conductances in 15 phylogenetically diverse insects, using patch-clamp recordings from dissociated ommatidia. We show that rapid diurnal flyers such as the blowfly (Calliphora vicina) and the honeybee (Apis mellifera) express relatively large noninactivating Kv conductances, conforming to the earlier hypothesis in Diptera. Nocturnal and/or slow-moving species do not in general exhibit stronger Kv conductance inactivation in the physiological membrane voltage range, but the photoreceptors in species that are known to rely more on vision behaviorally had higher densities of sustained Kv conductances than photoreceptors of less visually guided species. No statistically significant trends related to visual performance could be identified for the rapidly inactivating Kv conductances. Counterintuitively, strong negative correlations were observed between photoreceptor capacitance and specific membrane conductance for both sustained and inactivating fractions of Kv conductance, suggesting insignificant evolutionary pressure to offset negative effects of high capacitance on membrane filtering with increased conductance.},
  author       = {Frolov, Roman and Immonen, Esa-Ville and Weckström, Matti},
  issn         = {1522-1598},
  keyword      = {insect photoreceptor,potassium channels,compund eye,visual ecology},
  language     = {eng},
  month        = {04},
  number       = {4},
  pages        = {2147--2157},
  publisher    = {American Physiological Society},
  series       = {Journal of Neurophysiology},
  title        = {Visual ecology and potassium conductances of insect photoreceptors.},
  url          = {http://dx.doi.org/10.1152/jn.00795.2015},
  volume       = {115},
  year         = {2016},
}