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Optimal processing of photoreceptor signals is required to maximize behavioural sensitivity.

Publication ,  Journal Article
Okawa, H; Miyagishima, KJ; Arman, AC; Hurley, JB; Field, GD; Sampath, AP
Published in: J Physiol
June 1, 2010

The sensitivity of receptor cells places a fundamental limit upon the sensitivity of sensory systems. For example, the signal-to-noise ratio of sensory receptors has been suggested to limit absolute thresholds in the visual and auditory systems. However, the necessity of optimally processing sensory receptor signals for behaviour to approach this limit has received less attention. We investigated the behavioural consequences of increasing the signal-to-noise ratio of the rod photoreceptor single-photon response in a transgenic mouse, the GCAPs-/- knockout. The loss of fast Ca2+ feedback to cGMP synthesis in phototransduction for GCAPs-/- mice increases the magnitude of the rod single-photon response and dark noise, with the increase in size of the single-photon response outweighing the increase in noise. Surprisingly, despite the increased rod signal-to-noise ratio, behavioural performance for GCAPs-/- mice was diminished near absolute visual threshold. We demonstrate in electrophysiological recordings that the diminished performance compared to wild-type mice is explained by poorly tuned postsynaptic processing of the rod single-photon response at the rod bipolar cell. In particular, the level of postsynaptic saturation in GCAPs-/- rod bipolar cells is not sufficient to eliminate rod noise, and degrades the single-photon response signal-to-noise ratio. Thus, it is critical for retinal processing to be optimally tuned near absolute threshold; otherwise the visual system fails to utilize fully the signals present in the rods.

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Published In

J Physiol

DOI

EISSN

1469-7793

Publication Date

June 1, 2010

Volume

588

Issue

Pt 11

Start / End Page

1947 / 1960

Location

England

Related Subject Headings

  • Retinal Rod Photoreceptor Cells
  • Retinal Bipolar Cells
  • Physiology
  • Mice, Knockout
  • Mice
  • Light
  • Guanylate Cyclase-Activating Proteins
  • Excitatory Postsynaptic Potentials
  • Electrophysiology
  • Calibration
 

Citation

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Okawa, H., Miyagishima, K. J., Arman, A. C., Hurley, J. B., Field, G. D., & Sampath, A. P. (2010). Optimal processing of photoreceptor signals is required to maximize behavioural sensitivity. J Physiol, 588(Pt 11), 1947–1960. https://doi.org/10.1113/jphysiol.2010.188573
Okawa, Haruhisa, K Joshua Miyagishima, A Cyrus Arman, James B. Hurley, Greg D. Field, and Alapakkam P. Sampath. “Optimal processing of photoreceptor signals is required to maximize behavioural sensitivity.J Physiol 588, no. Pt 11 (June 1, 2010): 1947–60. https://doi.org/10.1113/jphysiol.2010.188573.
Okawa H, Miyagishima KJ, Arman AC, Hurley JB, Field GD, Sampath AP. Optimal processing of photoreceptor signals is required to maximize behavioural sensitivity. J Physiol. 2010 Jun 1;588(Pt 11):1947–60.
Okawa, Haruhisa, et al. “Optimal processing of photoreceptor signals is required to maximize behavioural sensitivity.J Physiol, vol. 588, no. Pt 11, June 2010, pp. 1947–60. Pubmed, doi:10.1113/jphysiol.2010.188573.
Okawa H, Miyagishima KJ, Arman AC, Hurley JB, Field GD, Sampath AP. Optimal processing of photoreceptor signals is required to maximize behavioural sensitivity. J Physiol. 2010 Jun 1;588(Pt 11):1947–1960.
Journal cover image

Published In

J Physiol

DOI

EISSN

1469-7793

Publication Date

June 1, 2010

Volume

588

Issue

Pt 11

Start / End Page

1947 / 1960

Location

England

Related Subject Headings

  • Retinal Rod Photoreceptor Cells
  • Retinal Bipolar Cells
  • Physiology
  • Mice, Knockout
  • Mice
  • Light
  • Guanylate Cyclase-Activating Proteins
  • Excitatory Postsynaptic Potentials
  • Electrophysiology
  • Calibration