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Light adaptation controls visual sensitivity by adjusting the speed and gain of the response to light

The range of c. 10(12) ambient light levels to which we can be exposed massively exceeds the <10(3) response range of neurons in the visual system, but we can see well in dim starlight and bright sunlight. This remarkable ability is achieved largely by a speeding up of the visual response as ligh...

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Detalles Bibliográficos
Autores principales: Rider, Andrew T., Henning, G. Bruce, Stockman, Andrew
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6685682/
https://www.ncbi.nlm.nih.gov/pubmed/31390358
http://dx.doi.org/10.1371/journal.pone.0220358
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author Rider, Andrew T.
Henning, G. Bruce
Stockman, Andrew
author_facet Rider, Andrew T.
Henning, G. Bruce
Stockman, Andrew
author_sort Rider, Andrew T.
collection PubMed
description The range of c. 10(12) ambient light levels to which we can be exposed massively exceeds the <10(3) response range of neurons in the visual system, but we can see well in dim starlight and bright sunlight. This remarkable ability is achieved largely by a speeding up of the visual response as light levels increase, causing characteristic changes in our sensitivity to different rates of flicker. Here, we account for over 65 years of flicker-sensitivity measurements with an elegantly-simple, physiologically-relevant model built from first-order low-pass filters and subtractive inhibition. There are only two intensity-dependent model parameters: one adjusts the speed of the visual response by shortening the time constants of some of the filters in the direct cascade as well as those in the inhibitory stages; the other parameter adjusts the overall gain at higher light levels. After reviewing the physiological literature, we associate the variable gain and three of the variable-speed filters with biochemical processes in cone photoreceptors, and a further variable-speed filter with processes in ganglion cells. The variable-speed but fixed-strength subtractive inhibition is most likely associated with lateral connections in the retina. Additional fixed-speed filters may be more central. The model can explain the important characteristics of human flicker-sensitivity including the approximate dependences of low-frequency sensitivity on contrast (Weber’s law) and of high-frequency sensitivity on amplitude (“high-frequency linearity”), the exponential loss of high-frequency sensitivity with increasing frequency, and the logarithmic increase in temporal acuity with light level (Ferry-Porter law). In the time-domain, the model can account for several characteristics of flash sensitivity including changes in contrast sensitivity with light level (de Vries-Rose and Weber’s laws) and changes in temporal summation (Bloch’s law). The new model provides fundamental insights into the workings of the visual system and gives a simple account of many visual phenomena.
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spelling pubmed-66856822019-08-15 Light adaptation controls visual sensitivity by adjusting the speed and gain of the response to light Rider, Andrew T. Henning, G. Bruce Stockman, Andrew PLoS One Research Article The range of c. 10(12) ambient light levels to which we can be exposed massively exceeds the <10(3) response range of neurons in the visual system, but we can see well in dim starlight and bright sunlight. This remarkable ability is achieved largely by a speeding up of the visual response as light levels increase, causing characteristic changes in our sensitivity to different rates of flicker. Here, we account for over 65 years of flicker-sensitivity measurements with an elegantly-simple, physiologically-relevant model built from first-order low-pass filters and subtractive inhibition. There are only two intensity-dependent model parameters: one adjusts the speed of the visual response by shortening the time constants of some of the filters in the direct cascade as well as those in the inhibitory stages; the other parameter adjusts the overall gain at higher light levels. After reviewing the physiological literature, we associate the variable gain and three of the variable-speed filters with biochemical processes in cone photoreceptors, and a further variable-speed filter with processes in ganglion cells. The variable-speed but fixed-strength subtractive inhibition is most likely associated with lateral connections in the retina. Additional fixed-speed filters may be more central. The model can explain the important characteristics of human flicker-sensitivity including the approximate dependences of low-frequency sensitivity on contrast (Weber’s law) and of high-frequency sensitivity on amplitude (“high-frequency linearity”), the exponential loss of high-frequency sensitivity with increasing frequency, and the logarithmic increase in temporal acuity with light level (Ferry-Porter law). In the time-domain, the model can account for several characteristics of flash sensitivity including changes in contrast sensitivity with light level (de Vries-Rose and Weber’s laws) and changes in temporal summation (Bloch’s law). The new model provides fundamental insights into the workings of the visual system and gives a simple account of many visual phenomena. Public Library of Science 2019-08-07 /pmc/articles/PMC6685682/ /pubmed/31390358 http://dx.doi.org/10.1371/journal.pone.0220358 Text en © 2019 Rider et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Rider, Andrew T.
Henning, G. Bruce
Stockman, Andrew
Light adaptation controls visual sensitivity by adjusting the speed and gain of the response to light
title Light adaptation controls visual sensitivity by adjusting the speed and gain of the response to light
title_full Light adaptation controls visual sensitivity by adjusting the speed and gain of the response to light
title_fullStr Light adaptation controls visual sensitivity by adjusting the speed and gain of the response to light
title_full_unstemmed Light adaptation controls visual sensitivity by adjusting the speed and gain of the response to light
title_short Light adaptation controls visual sensitivity by adjusting the speed and gain of the response to light
title_sort light adaptation controls visual sensitivity by adjusting the speed and gain of the response to light
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6685682/
https://www.ncbi.nlm.nih.gov/pubmed/31390358
http://dx.doi.org/10.1371/journal.pone.0220358
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