Adaptation memory in photoreceptors: different mechanisms in rods and cones

Vertebrate rods and cones operate over a wide range of ambient illumination, which is provided by light adaptation mechanisms regulating the sensitivity and speed of the phototransduction cascade. Three calcium-sensitive feedback loops are well established in both rods and cones: acceleration of the...

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Main Authors: Darya A. Nikolaeva, Maria A. Nekrasova, Alexander Yu. Rotov, Luba A. Astakhova
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-04-01
Series:Frontiers in Molecular Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnmol.2023.1135088/full
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author Darya A. Nikolaeva
Maria A. Nekrasova
Alexander Yu. Rotov
Alexander Yu. Rotov
Luba A. Astakhova
author_facet Darya A. Nikolaeva
Maria A. Nekrasova
Alexander Yu. Rotov
Alexander Yu. Rotov
Luba A. Astakhova
author_sort Darya A. Nikolaeva
collection DOAJ
description Vertebrate rods and cones operate over a wide range of ambient illumination, which is provided by light adaptation mechanisms regulating the sensitivity and speed of the phototransduction cascade. Three calcium-sensitive feedback loops are well established in both rods and cones: acceleration of the quenching of a light-activated visual pigment and cGMP synthesis by guanylate cyclase, and increased affinity of ion channels for cGMP. Accumulating evidence suggests that the molecular mechanisms of light adaptation are more complex. While investigating these putative mechanisms, we discovered a novel phenomenon, observing that the recovery of light sensitivity in rods after turning off non-saturating adaptive light can take tens of seconds. Moreover, after a formal return of the membrane current to the dark level, cell sensitivity to the stimuli remains decreased for a further 1–2 min. We termed this phenomenon of prolonged photoreceptor desensitization ‘adaptation memory’ (of previous illumination) and the current study is focused on its detailed investigation in rods and an attempt to find the same phenomenon in cones. In rods, we have explored the dependencies of this phenomenon on adapting conditions, specifically, the intensity and duration of adapting illumination. Additionally, we report that fish and frog red-sensitive cones possess similar features of adaptation memory, such as a drop in sensitivity just after the steps of bright light and slow sensitivity recovery. However, we have found that the rate of this process and its nature are not the same as in rods. Our results indicate that the nature of the temporary drop in the sensitivity in rods and cones after adapting steps of light is different. In the rods, adaptation memory could be attributed to the existence of long-lasting modifications of the components of the phototransduction cascade after adapting illumination. In cones, the observed form of the adaptation memory seems to be due to the sensitivity drop caused by a decrease in the availability of the visual pigment, that is, by bleaching.
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spelling doaj.art-4372a74d31c14b42a1cc2d2657c44ec52023-04-24T04:32:55ZengFrontiers Media S.A.Frontiers in Molecular Neuroscience1662-50992023-04-011610.3389/fnmol.2023.11350881135088Adaptation memory in photoreceptors: different mechanisms in rods and conesDarya A. Nikolaeva0Maria A. Nekrasova1Alexander Yu. Rotov2Alexander Yu. Rotov3Luba A. Astakhova4Laboratory of Evolution of the Sense Organs, I.M. Sechenov Institute of Evolutionary Physiology and Biochemistry RAS, Saint Petersburg, RussiaLaboratory of Evolution of the Sense Organs, I.M. Sechenov Institute of Evolutionary Physiology and Biochemistry RAS, Saint Petersburg, RussiaLaboratory of Evolution of the Sense Organs, I.M. Sechenov Institute of Evolutionary Physiology and Biochemistry RAS, Saint Petersburg, RussiaLaboratory of Toxinology and Molecular Systematics, L.A. Orbeli Institute of Physiology NAS RA, Yerevan, ArmeniaLaboratory of Evolution of the Sense Organs, I.M. Sechenov Institute of Evolutionary Physiology and Biochemistry RAS, Saint Petersburg, RussiaVertebrate rods and cones operate over a wide range of ambient illumination, which is provided by light adaptation mechanisms regulating the sensitivity and speed of the phototransduction cascade. Three calcium-sensitive feedback loops are well established in both rods and cones: acceleration of the quenching of a light-activated visual pigment and cGMP synthesis by guanylate cyclase, and increased affinity of ion channels for cGMP. Accumulating evidence suggests that the molecular mechanisms of light adaptation are more complex. While investigating these putative mechanisms, we discovered a novel phenomenon, observing that the recovery of light sensitivity in rods after turning off non-saturating adaptive light can take tens of seconds. Moreover, after a formal return of the membrane current to the dark level, cell sensitivity to the stimuli remains decreased for a further 1–2 min. We termed this phenomenon of prolonged photoreceptor desensitization ‘adaptation memory’ (of previous illumination) and the current study is focused on its detailed investigation in rods and an attempt to find the same phenomenon in cones. In rods, we have explored the dependencies of this phenomenon on adapting conditions, specifically, the intensity and duration of adapting illumination. Additionally, we report that fish and frog red-sensitive cones possess similar features of adaptation memory, such as a drop in sensitivity just after the steps of bright light and slow sensitivity recovery. However, we have found that the rate of this process and its nature are not the same as in rods. Our results indicate that the nature of the temporary drop in the sensitivity in rods and cones after adapting steps of light is different. In the rods, adaptation memory could be attributed to the existence of long-lasting modifications of the components of the phototransduction cascade after adapting illumination. In cones, the observed form of the adaptation memory seems to be due to the sensitivity drop caused by a decrease in the availability of the visual pigment, that is, by bleaching.https://www.frontiersin.org/articles/10.3389/fnmol.2023.1135088/fullrodconephototransductionlight adaptationadaptation memorydark adaptation
spellingShingle Darya A. Nikolaeva
Maria A. Nekrasova
Alexander Yu. Rotov
Alexander Yu. Rotov
Luba A. Astakhova
Adaptation memory in photoreceptors: different mechanisms in rods and cones
Frontiers in Molecular Neuroscience
rod
cone
phototransduction
light adaptation
adaptation memory
dark adaptation
title Adaptation memory in photoreceptors: different mechanisms in rods and cones
title_full Adaptation memory in photoreceptors: different mechanisms in rods and cones
title_fullStr Adaptation memory in photoreceptors: different mechanisms in rods and cones
title_full_unstemmed Adaptation memory in photoreceptors: different mechanisms in rods and cones
title_short Adaptation memory in photoreceptors: different mechanisms in rods and cones
title_sort adaptation memory in photoreceptors different mechanisms in rods and cones
topic rod
cone
phototransduction
light adaptation
adaptation memory
dark adaptation
url https://www.frontiersin.org/articles/10.3389/fnmol.2023.1135088/full
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