Advanced

Signal coding in cockroach photoreceptors is tuned to dim environments

Heimonen, K.; Immonen, Esa-Ville LU ; Frolov, R. V.; Salmela, I.; Juusola, M.; Vahasoyrinki, M. and Weckstrom, M. (2012) In Journal of Neurophysiology 108. p.2641-2652
Abstract
In dim light, scarcity of photons typically leads to poor vision. Nonetheless, many animals show visually guided behavior with dim environments. We investigated the signaling properties of photoreceptors of the dark active cockroach (Periplaneta americana) using intracellular and whole-cell patch-clamp recordings to determine whether they show selective functional adaptations to dark. Expectedly, dark-adapted photoreceptors generated large and slow responses to single photons. However, when light adapted, responses of both phototransduction and the nontransductive membrane to white noise (WN)-modulated stimuli remained slow with corner frequencies ~20 Hz. This promotes temporal integration of light inputs and maintains high sensitivity of... (More)
In dim light, scarcity of photons typically leads to poor vision. Nonetheless, many animals show visually guided behavior with dim environments. We investigated the signaling properties of photoreceptors of the dark active cockroach (Periplaneta americana) using intracellular and whole-cell patch-clamp recordings to determine whether they show selective functional adaptations to dark. Expectedly, dark-adapted photoreceptors generated large and slow responses to single photons. However, when light adapted, responses of both phototransduction and the nontransductive membrane to white noise (WN)-modulated stimuli remained slow with corner frequencies ~20 Hz. This promotes temporal integration of light inputs and maintains high sensitivity of vision. Adaptive changes in dynamics were limited to dim conditions. Characteristically, both step and frequency responses stayed effectively unchanged for intensities >1,000 photons/s/photoreceptor. A signal-to-noise ratio (SNR) of the light responses was transiently higher at frequencies <5 Hz for ~5 s after light onset but deteriorated to a lower value upon longer stimulation. Naturalistic light stimuli, as opposed to WN, evoked markedly larger responses with higher SNRs at low frequencies. This allowed realistic estimates of information transfer rates, which saturated at ~100 bits/s at low-light intensities. We found, therefore, selective adaptations beneficial for vision in dim environments in cockroach photoreceptors: large amplitude of single-photon responses, constant high level of temporal integration of light inputs, saturation of response properties at low intensities, and only transiently efficient encoding of light contrasts. The results also suggest that the sources of the large functional variability among different photoreceptors reside mostly in phototransduction processes and not in the properties of the nontransductive membrane. (Less)
Please use this url to cite or link to this publication:
author
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Periplaneta, Photons, Photoreceptor Cells, Invertebrate/*physiology, Darkness, Dark Adaptation/*physiology, Contrast Sensitivity, Action Potentials, Animals
in
Journal of Neurophysiology
volume
108
pages
2641 - 2652
publisher
American Physiological Society
external identifiers
  • scopus:84869158508
ISSN
0022-3077
DOI
10.1152/jn.00588.2012
language
English
LU publication?
no
id
8de0db43-9b73-4c6b-ae9b-67e6c70fe94f (old id 5431766)
alternative location
http://www.ncbi.nlm.nih.gov/pubmed/22933721
date added to LUP
2015-05-25 14:53:05
date last changed
2017-08-27 05:01:10
@article{8de0db43-9b73-4c6b-ae9b-67e6c70fe94f,
  abstract     = {In dim light, scarcity of photons typically leads to poor vision. Nonetheless, many animals show visually guided behavior with dim environments. We investigated the signaling properties of photoreceptors of the dark active cockroach (Periplaneta americana) using intracellular and whole-cell patch-clamp recordings to determine whether they show selective functional adaptations to dark. Expectedly, dark-adapted photoreceptors generated large and slow responses to single photons. However, when light adapted, responses of both phototransduction and the nontransductive membrane to white noise (WN)-modulated stimuli remained slow with corner frequencies ~20 Hz. This promotes temporal integration of light inputs and maintains high sensitivity of vision. Adaptive changes in dynamics were limited to dim conditions. Characteristically, both step and frequency responses stayed effectively unchanged for intensities &gt;1,000 photons/s/photoreceptor. A signal-to-noise ratio (SNR) of the light responses was transiently higher at frequencies &lt;5 Hz for ~5 s after light onset but deteriorated to a lower value upon longer stimulation. Naturalistic light stimuli, as opposed to WN, evoked markedly larger responses with higher SNRs at low frequencies. This allowed realistic estimates of information transfer rates, which saturated at ~100 bits/s at low-light intensities. We found, therefore, selective adaptations beneficial for vision in dim environments in cockroach photoreceptors: large amplitude of single-photon responses, constant high level of temporal integration of light inputs, saturation of response properties at low intensities, and only transiently efficient encoding of light contrasts. The results also suggest that the sources of the large functional variability among different photoreceptors reside mostly in phototransduction processes and not in the properties of the nontransductive membrane.},
  author       = {Heimonen, K. and Immonen, Esa-Ville and Frolov, R. V. and Salmela, I. and Juusola, M. and Vahasoyrinki, M. and Weckstrom, M.},
  issn         = {0022-3077},
  keyword      = {Periplaneta,Photons,Photoreceptor Cells,Invertebrate/*physiology,Darkness,Dark Adaptation/*physiology,Contrast Sensitivity,Action Potentials,Animals},
  language     = {eng},
  pages        = {2641--2652},
  publisher    = {American Physiological Society},
  series       = {Journal of Neurophysiology},
  title        = {Signal coding in cockroach photoreceptors is tuned to dim environments},
  url          = {http://dx.doi.org/10.1152/jn.00588.2012},
  volume       = {108},
  year         = {2012},
}