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Distinct roles of light-activated channels TRP and TRPL in photoreceptors of periplaneta americana

Saari, Paulus; French, Andrew S.; Torkkeli, Päivi H.; Liu, Hongxia; Immonen, Esa Ville LU and Frolov, Roman V. (2017) In Journal of General Physiology 149(4). p.455-464
Abstract

Electrophysiological studies in Drosophila melanogaster and Periplaneta americana have found that the receptor current in their microvillar photoreceptors is generated by two light-activated cationic channels, TRP (transient receptor potential) and TRPL (TRP-like), each having distinct properties. However, the relative contribution of the two channel types to sensory information coding by photoreceptors remains unclear. We recently showed that, in contrast to the diurnal Drosophila in which TRP is the principal phototransduction channel, photoreceptors of the nocturnal P americana strongly depend on TRPL. Here, we perform a functional analysis, using patch-clamp and intracellular recordings, of P americana photoreceptors after RNA... (More)

Electrophysiological studies in Drosophila melanogaster and Periplaneta americana have found that the receptor current in their microvillar photoreceptors is generated by two light-activated cationic channels, TRP (transient receptor potential) and TRPL (TRP-like), each having distinct properties. However, the relative contribution of the two channel types to sensory information coding by photoreceptors remains unclear. We recently showed that, in contrast to the diurnal Drosophila in which TRP is the principal phototransduction channel, photoreceptors of the nocturnal P americana strongly depend on TRPL. Here, we perform a functional analysis, using patch-clamp and intracellular recordings, of P americana photoreceptors after RNA interference to knock down TRP (TRPkd) and TRPL (TRPLkd). Several functional properties were changed in both knockdown phenotypes: Cell membrane capacitance was reduced 1.7-fold, light sensitivity was greatly reduced, and amplitudes of sustained light-induced currents and voltage responses decreased more than twofold over the entire range of light intensities. The information rate (IR) was tested using a Gaussian white-noise modulated light stimulus and was lower in TRPkd photoreceptors (28 ± 21 bits/s) than in controls (52 ± 13 bits/s) because of high levels of bump noise. In contrast, although signal amplitudes were smaller than in controls, the mean IR of TRPLkd photoreceptors was unchanged at 54 ± 29 bits/s1 because of proportionally lower noise. We conclude that TRPL channels provide high-gain/high-noise transduction, suitable for vision in dim light, whereas transduction by TRP channels is relatively low-gain/low-noise and allows better information transfer in bright light.

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author
organization
publishing date
type
Contribution to journal
publication status
published
subject
in
Journal of General Physiology
volume
149
issue
4
pages
10 pages
publisher
Rockefeller Institute for Medical Research
external identifiers
  • scopus:85021968869
  • wos:000403168100007
ISSN
0022-1295
DOI
10.1085/jgp.201611737
language
English
LU publication?
yes
id
db59a434-d2e2-4376-b2f9-f3bd0380ba23
date added to LUP
2017-07-24 13:05:49
date last changed
2018-01-07 12:12:47
@article{db59a434-d2e2-4376-b2f9-f3bd0380ba23,
  abstract     = {<p>Electrophysiological studies in Drosophila melanogaster and Periplaneta americana have found that the receptor current in their microvillar photoreceptors is generated by two light-activated cationic channels, TRP (transient receptor potential) and TRPL (TRP-like), each having distinct properties. However, the relative contribution of the two channel types to sensory information coding by photoreceptors remains unclear. We recently showed that, in contrast to the diurnal Drosophila in which TRP is the principal phototransduction channel, photoreceptors of the nocturnal P americana strongly depend on TRPL. Here, we perform a functional analysis, using patch-clamp and intracellular recordings, of P americana photoreceptors after RNA interference to knock down TRP (TRPkd) and TRPL (TRPLkd). Several functional properties were changed in both knockdown phenotypes: Cell membrane capacitance was reduced 1.7-fold, light sensitivity was greatly reduced, and amplitudes of sustained light-induced currents and voltage responses decreased more than twofold over the entire range of light intensities. The information rate (IR) was tested using a Gaussian white-noise modulated light stimulus and was lower in TRPkd photoreceptors (28 ± 21 bits/s) than in controls (52 ± 13 bits/s) because of high levels of bump noise. In contrast, although signal amplitudes were smaller than in controls, the mean IR of TRPLkd photoreceptors was unchanged at 54 ± 29 bits/s<sup>1</sup> because of proportionally lower noise. We conclude that TRPL channels provide high-gain/high-noise transduction, suitable for vision in dim light, whereas transduction by TRP channels is relatively low-gain/low-noise and allows better information transfer in bright light.</p>},
  author       = {Saari, Paulus and French, Andrew S. and Torkkeli, Päivi H. and Liu, Hongxia and Immonen, Esa Ville and Frolov, Roman V.},
  issn         = {0022-1295},
  language     = {eng},
  month        = {04},
  number       = {4},
  pages        = {455--464},
  publisher    = {Rockefeller Institute for Medical Research},
  series       = {Journal of General Physiology},
  title        = {Distinct roles of light-activated channels TRP and TRPL in photoreceptors of periplaneta americana},
  url          = {http://dx.doi.org/10.1085/jgp.201611737},
  volume       = {149},
  year         = {2017},
}