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Dopaminergic Modulation of Signal Processing in a Subset of Retinal Bipolar Cells

The retina and the olfactory bulb are the gateways to the visual and olfactory systems, respectively, similarly using neural networks to initiate sensory signal processing. Sensory receptors receive signals that are transmitted to neural networks before projecting to primary cortices. These networks...

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Autores principales: Hellmer, Chase B., Bohl, Jeremy M., Hall, Leo M., Koehler, Christina C., Ichinose, Tomomi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7456991/
https://www.ncbi.nlm.nih.gov/pubmed/32922266
http://dx.doi.org/10.3389/fncel.2020.00253
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author Hellmer, Chase B.
Bohl, Jeremy M.
Hall, Leo M.
Koehler, Christina C.
Ichinose, Tomomi
author_facet Hellmer, Chase B.
Bohl, Jeremy M.
Hall, Leo M.
Koehler, Christina C.
Ichinose, Tomomi
author_sort Hellmer, Chase B.
collection PubMed
description The retina and the olfactory bulb are the gateways to the visual and olfactory systems, respectively, similarly using neural networks to initiate sensory signal processing. Sensory receptors receive signals that are transmitted to neural networks before projecting to primary cortices. These networks filter sensory signals based on their unique features and adjust their sensitivities by gain control systems. Interestingly, dopamine modulates sensory signal transduction in both systems. In the retina, dopamine adjusts the retinal network for daylight conditions (“light adaptation”). In the olfactory system, dopamine mediates lateral inhibition between the glomeruli, resulting in odorant signal decorrelation and discrimination. While dopamine is essential for signal discrimination in the olfactory system, it is not understood whether dopamine has similar roles in visual signal processing in the retina. To elucidate dopaminergic effects on visual processing, we conducted patch-clamp recording from second-order retinal bipolar cells, which exhibit multiple types that can convey different temporal features of light. We recorded excitatory postsynaptic potentials (EPSPs) evoked by various frequencies of sinusoidal light in the absence and presence of a dopamine receptor 1 (D(1)R) agonist or antagonist. Application of a D(1)R agonist, SKF-38393, shifted the peak temporal responses toward higher frequencies in a subset of bipolar cells. In contrast, a D(1)R antagonist, SCH-23390, reversed the effects of SKF on these types of bipolar cells. To examine the mechanism of dopaminergic modulation, we recorded voltage-gated currents, hyperpolarization-activated cyclic nucleotide-gated (HCN) channels, and low-voltage activated (LVA) Ca(2+) channels. SKF modulated HCN and LVA currents, suggesting that these channels are the target of D(1)R signaling to modulate visual signaling in these bipolar cells. Taken together, we found that dopamine modulates the temporal tuning of a subset of retinal bipolar cells. Consequently, we determined that dopamine plays a role in visual signal processing, which is similar to its role in signal decorrelation in the olfactory bulb.
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spelling pubmed-74569912020-09-11 Dopaminergic Modulation of Signal Processing in a Subset of Retinal Bipolar Cells Hellmer, Chase B. Bohl, Jeremy M. Hall, Leo M. Koehler, Christina C. Ichinose, Tomomi Front Cell Neurosci Cellular Neuroscience The retina and the olfactory bulb are the gateways to the visual and olfactory systems, respectively, similarly using neural networks to initiate sensory signal processing. Sensory receptors receive signals that are transmitted to neural networks before projecting to primary cortices. These networks filter sensory signals based on their unique features and adjust their sensitivities by gain control systems. Interestingly, dopamine modulates sensory signal transduction in both systems. In the retina, dopamine adjusts the retinal network for daylight conditions (“light adaptation”). In the olfactory system, dopamine mediates lateral inhibition between the glomeruli, resulting in odorant signal decorrelation and discrimination. While dopamine is essential for signal discrimination in the olfactory system, it is not understood whether dopamine has similar roles in visual signal processing in the retina. To elucidate dopaminergic effects on visual processing, we conducted patch-clamp recording from second-order retinal bipolar cells, which exhibit multiple types that can convey different temporal features of light. We recorded excitatory postsynaptic potentials (EPSPs) evoked by various frequencies of sinusoidal light in the absence and presence of a dopamine receptor 1 (D(1)R) agonist or antagonist. Application of a D(1)R agonist, SKF-38393, shifted the peak temporal responses toward higher frequencies in a subset of bipolar cells. In contrast, a D(1)R antagonist, SCH-23390, reversed the effects of SKF on these types of bipolar cells. To examine the mechanism of dopaminergic modulation, we recorded voltage-gated currents, hyperpolarization-activated cyclic nucleotide-gated (HCN) channels, and low-voltage activated (LVA) Ca(2+) channels. SKF modulated HCN and LVA currents, suggesting that these channels are the target of D(1)R signaling to modulate visual signaling in these bipolar cells. Taken together, we found that dopamine modulates the temporal tuning of a subset of retinal bipolar cells. Consequently, we determined that dopamine plays a role in visual signal processing, which is similar to its role in signal decorrelation in the olfactory bulb. Frontiers Media S.A. 2020-08-14 /pmc/articles/PMC7456991/ /pubmed/32922266 http://dx.doi.org/10.3389/fncel.2020.00253 Text en Copyright © 2020 Hellmer, Bohl, Hall, Koehler and Ichinose. http://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 Cellular Neuroscience
Hellmer, Chase B.
Bohl, Jeremy M.
Hall, Leo M.
Koehler, Christina C.
Ichinose, Tomomi
Dopaminergic Modulation of Signal Processing in a Subset of Retinal Bipolar Cells
title Dopaminergic Modulation of Signal Processing in a Subset of Retinal Bipolar Cells
title_full Dopaminergic Modulation of Signal Processing in a Subset of Retinal Bipolar Cells
title_fullStr Dopaminergic Modulation of Signal Processing in a Subset of Retinal Bipolar Cells
title_full_unstemmed Dopaminergic Modulation of Signal Processing in a Subset of Retinal Bipolar Cells
title_short Dopaminergic Modulation of Signal Processing in a Subset of Retinal Bipolar Cells
title_sort dopaminergic modulation of signal processing in a subset of retinal bipolar cells
topic Cellular Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7456991/
https://www.ncbi.nlm.nih.gov/pubmed/32922266
http://dx.doi.org/10.3389/fncel.2020.00253
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