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Postembryonic developmental changes in photoreceptors of the stick insect Carausius morosus enhance the shift to an adult nocturnal life-style

Frolov, R.; Immonen, Esa-Ville LU ; Vahasoyrinki, M. and Weckstrom, M. (2012) In Journal of Neuroscience 32. p.16821-16831
Abstract
Optimization of sensory processing during development can be studied by using photoreceptors of hemimetabolous insects (with incomplete metamorphosis) as a research model. We have addressed this topic in the stick insect Carausius morosus, where retinal growth after hatching is accompanied by a diurnal-to-nocturnal shift in behavior, by recording from photoreceptors of first instar nymphs and adult animals using the patch-clamp method. In the nymphs, ommatidia were smaller and photoreceptors were on average 15-fold less sensitive to light than in adults. The magnitude of A-type K(+) current did not increase but the delayed rectifier doubled in adults compared with nymphs, the K(+) current densities being greater in the nymphs. By contrast,... (More)
Optimization of sensory processing during development can be studied by using photoreceptors of hemimetabolous insects (with incomplete metamorphosis) as a research model. We have addressed this topic in the stick insect Carausius morosus, where retinal growth after hatching is accompanied by a diurnal-to-nocturnal shift in behavior, by recording from photoreceptors of first instar nymphs and adult animals using the patch-clamp method. In the nymphs, ommatidia were smaller and photoreceptors were on average 15-fold less sensitive to light than in adults. The magnitude of A-type K(+) current did not increase but the delayed rectifier doubled in adults compared with nymphs, the K(+) current densities being greater in the nymphs. By contrast, the density of light-induced current did not increase, although its magnitude increased 8.6-fold, probably due to the growth of microvilli. Nymph photoreceptors performed poorly, demonstrating a peak information rate (IR) of 2.9 +/- 0.7 bits/s versus 34.1 +/- 5.0 bits/s in adults in response to white-noise stimulation. Strong correlations were found between photoreceptor capacitance (a proxy for cell size) and IR, and between light sensitivity and IR, with larger and more sensitive photoreceptors performing better. In adults, IR peaked at light intensities matching irradiation from the evening sky. Our results indicate that biophysical properties of photoreceptors at each age stage and visual behavior are interdependent and that developmental improvement in photoreceptor performance may facilitate the switch from the diurnal to the safer nocturnal lifestyle. This also has implications for how photoreceptors achieve optimal performance. (Less)
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author
publishing date
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Contribution to journal
publication status
published
subject
keywords
Larva, Noise, Photic Stimulation, Photoreceptor Cells, Invertebrate/metabolism/*physiology, Vision, Ocular/physiology, Light, Ion Channels/physiology, Insects/*physiology, Female, Energy Metabolism/physiology, Embryonic Development/physiology, Nonmammalian/metabolism/*physiology, Embryo, Statistical, Data Interpretation, Circadian Rhythm/*physiology, Acoustic Stimulation, Animals
in
Journal of Neuroscience
volume
32
pages
16821 - 16831
publisher
Society for Neuroscience
external identifiers
  • scopus:84870036882
ISSN
1529-2401
DOI
10.1523/JNEUROSCI.2612-12.2012
language
English
LU publication?
no
id
8af59b19-6483-4fcf-b865-ff7f9cc97f20 (old id 5431753)
alternative location
http://www.ncbi.nlm.nih.gov/pubmed/23175835
date added to LUP
2015-05-25 14:40:03
date last changed
2017-08-27 04:56:43
@article{8af59b19-6483-4fcf-b865-ff7f9cc97f20,
  abstract     = {Optimization of sensory processing during development can be studied by using photoreceptors of hemimetabolous insects (with incomplete metamorphosis) as a research model. We have addressed this topic in the stick insect Carausius morosus, where retinal growth after hatching is accompanied by a diurnal-to-nocturnal shift in behavior, by recording from photoreceptors of first instar nymphs and adult animals using the patch-clamp method. In the nymphs, ommatidia were smaller and photoreceptors were on average 15-fold less sensitive to light than in adults. The magnitude of A-type K(+) current did not increase but the delayed rectifier doubled in adults compared with nymphs, the K(+) current densities being greater in the nymphs. By contrast, the density of light-induced current did not increase, although its magnitude increased 8.6-fold, probably due to the growth of microvilli. Nymph photoreceptors performed poorly, demonstrating a peak information rate (IR) of 2.9 +/- 0.7 bits/s versus 34.1 +/- 5.0 bits/s in adults in response to white-noise stimulation. Strong correlations were found between photoreceptor capacitance (a proxy for cell size) and IR, and between light sensitivity and IR, with larger and more sensitive photoreceptors performing better. In adults, IR peaked at light intensities matching irradiation from the evening sky. Our results indicate that biophysical properties of photoreceptors at each age stage and visual behavior are interdependent and that developmental improvement in photoreceptor performance may facilitate the switch from the diurnal to the safer nocturnal lifestyle. This also has implications for how photoreceptors achieve optimal performance.},
  author       = {Frolov, R. and Immonen, Esa-Ville and Vahasoyrinki, M. and Weckstrom, M.},
  issn         = {1529-2401},
  keyword      = {Larva,Noise,Photic Stimulation,Photoreceptor Cells,Invertebrate/metabolism/*physiology,Vision,Ocular/physiology,Light,Ion Channels/physiology,Insects/*physiology,Female,Energy Metabolism/physiology,Embryonic Development/physiology,Nonmammalian/metabolism/*physiology,Embryo,Statistical,Data Interpretation,Circadian Rhythm/*physiology,Acoustic Stimulation,Animals},
  language     = {eng},
  pages        = {16821--16831},
  publisher    = {Society for Neuroscience},
  series       = {Journal of Neuroscience},
  title        = {Postembryonic developmental changes in photoreceptors of the stick insect Carausius morosus enhance the shift to an adult nocturnal life-style},
  url          = {http://dx.doi.org/10.1523/JNEUROSCI.2612-12.2012},
  volume       = {32},
  year         = {2012},
}