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Effects of cell size and bicarbonate on single photon response variability in retinal rods
Accurate photon counting requires that rods generate highly amplified, reproducible single photon responses (SPRs). The SPR is generated within the rod outer segment (ROS), a multilayered structure built from membranous disks that house rhodopsin. Photoisomerization of rhodopsin at the disk rim caus...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Frontiers Media S.A.
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9796569/ https://www.ncbi.nlm.nih.gov/pubmed/36590910 http://dx.doi.org/10.3389/fnmol.2022.1050545 |
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author | Geva, Polina Caruso, Giovanni Klaus, Colin Hamm, Heidi E. Gurevich, Vsevolod V. DiBenedetto, Emmanuele Makino, Clint L. |
author_facet | Geva, Polina Caruso, Giovanni Klaus, Colin Hamm, Heidi E. Gurevich, Vsevolod V. DiBenedetto, Emmanuele Makino, Clint L. |
author_sort | Geva, Polina |
collection | PubMed |
description | Accurate photon counting requires that rods generate highly amplified, reproducible single photon responses (SPRs). The SPR is generated within the rod outer segment (ROS), a multilayered structure built from membranous disks that house rhodopsin. Photoisomerization of rhodopsin at the disk rim causes a local depletion of cGMP that closes ion channels in the plasmalemma located nearby with relative rapidity. In contrast, a photoisomerization at the disk center, distant from the plasmalemma, has a delayed impact on the ion channels due to the time required for cGMP redistribution. Radial differences should be greatest in large diameter rods. By affecting membrane guanylate cyclase activity, bicarbonate could impact spatial inhomogeneity in cGMP content. It was previously known that in the absence of bicarbonate, SPRs are larger and faster at the base of a toad ROS (where the ROS attaches to the rest of the cell) than at the distal tip. Given that bicarbonate enters the ROS at the base and diffuses to the tip and that it expedites flash response recovery, there should be an axial concentration gradient for bicarbonate that would accentuate the base-to-tip SPR differences. Seeking to understand how ROS geometry and bicarbonate affect SPR variability, we used mathematical modeling and made electrophysiological recordings of single rods. Modeling predicted and our experiments confirmed minor radial SPR variability in large diameter, salamander rods that was essentially unchanged by bicarbonate. SPRs elicited at the base and tip of salamander rods were similar in the absence of bicarbonate, but when treated with 30 mM bicarbonate, SPRs at the base became slightly faster than those at the tip, verifying the existence of an axial gradient for bicarbonate. The differences were small and unlikely to undermine visual signaling. However, in toad rods with longer ROSs, bicarbonate somehow suppressed the substantial, axial SPR variability that is naturally present in the absence of bicarbonate. Modeling suggested that the axial gradient of bicarbonate might dampen the primary phototransduction cascade at the base of the ROS. This novel effect of bicarbonate solves a mystery as to how toad vision is able to function effectively in extremely dim light. |
format | Online Article Text |
id | pubmed-9796569 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-97965692022-12-29 Effects of cell size and bicarbonate on single photon response variability in retinal rods Geva, Polina Caruso, Giovanni Klaus, Colin Hamm, Heidi E. Gurevich, Vsevolod V. DiBenedetto, Emmanuele Makino, Clint L. Front Mol Neurosci Molecular Neuroscience Accurate photon counting requires that rods generate highly amplified, reproducible single photon responses (SPRs). The SPR is generated within the rod outer segment (ROS), a multilayered structure built from membranous disks that house rhodopsin. Photoisomerization of rhodopsin at the disk rim causes a local depletion of cGMP that closes ion channels in the plasmalemma located nearby with relative rapidity. In contrast, a photoisomerization at the disk center, distant from the plasmalemma, has a delayed impact on the ion channels due to the time required for cGMP redistribution. Radial differences should be greatest in large diameter rods. By affecting membrane guanylate cyclase activity, bicarbonate could impact spatial inhomogeneity in cGMP content. It was previously known that in the absence of bicarbonate, SPRs are larger and faster at the base of a toad ROS (where the ROS attaches to the rest of the cell) than at the distal tip. Given that bicarbonate enters the ROS at the base and diffuses to the tip and that it expedites flash response recovery, there should be an axial concentration gradient for bicarbonate that would accentuate the base-to-tip SPR differences. Seeking to understand how ROS geometry and bicarbonate affect SPR variability, we used mathematical modeling and made electrophysiological recordings of single rods. Modeling predicted and our experiments confirmed minor radial SPR variability in large diameter, salamander rods that was essentially unchanged by bicarbonate. SPRs elicited at the base and tip of salamander rods were similar in the absence of bicarbonate, but when treated with 30 mM bicarbonate, SPRs at the base became slightly faster than those at the tip, verifying the existence of an axial gradient for bicarbonate. The differences were small and unlikely to undermine visual signaling. However, in toad rods with longer ROSs, bicarbonate somehow suppressed the substantial, axial SPR variability that is naturally present in the absence of bicarbonate. Modeling suggested that the axial gradient of bicarbonate might dampen the primary phototransduction cascade at the base of the ROS. This novel effect of bicarbonate solves a mystery as to how toad vision is able to function effectively in extremely dim light. Frontiers Media S.A. 2022-12-14 /pmc/articles/PMC9796569/ /pubmed/36590910 http://dx.doi.org/10.3389/fnmol.2022.1050545 Text en Copyright © 2022 Geva, Caruso, Klaus, Hamm, Gurevich, DiBenedetto and Makino. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Molecular Neuroscience Geva, Polina Caruso, Giovanni Klaus, Colin Hamm, Heidi E. Gurevich, Vsevolod V. DiBenedetto, Emmanuele Makino, Clint L. Effects of cell size and bicarbonate on single photon response variability in retinal rods |
title | Effects of cell size and bicarbonate on single photon response variability in retinal rods |
title_full | Effects of cell size and bicarbonate on single photon response variability in retinal rods |
title_fullStr | Effects of cell size and bicarbonate on single photon response variability in retinal rods |
title_full_unstemmed | Effects of cell size and bicarbonate on single photon response variability in retinal rods |
title_short | Effects of cell size and bicarbonate on single photon response variability in retinal rods |
title_sort | effects of cell size and bicarbonate on single photon response variability in retinal rods |
topic | Molecular Neuroscience |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9796569/ https://www.ncbi.nlm.nih.gov/pubmed/36590910 http://dx.doi.org/10.3389/fnmol.2022.1050545 |
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