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Correlated Activity in the Degenerate Retina Inhibits Focal Response to Electrical Stimulation

Retinal prostheses have shown some clinical success in patients with retinitis pigmentosa and age-related macular degeneration. However, even after the implantation of a retinal prosthesis, the patient’s visual acuity is at best less than 20/420. Reduced visual acuity may be explained by a decrease...

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Autores principales: Ahn, Jungryul, Cha, Seongkwang, Choi, Kwang-Eon, Kim, Seong-Woo, Yoo, Yongseok, Goo, Yong Sook
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9114441/
https://www.ncbi.nlm.nih.gov/pubmed/35602554
http://dx.doi.org/10.3389/fncel.2022.889663
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author Ahn, Jungryul
Cha, Seongkwang
Choi, Kwang-Eon
Kim, Seong-Woo
Yoo, Yongseok
Goo, Yong Sook
author_facet Ahn, Jungryul
Cha, Seongkwang
Choi, Kwang-Eon
Kim, Seong-Woo
Yoo, Yongseok
Goo, Yong Sook
author_sort Ahn, Jungryul
collection PubMed
description Retinal prostheses have shown some clinical success in patients with retinitis pigmentosa and age-related macular degeneration. However, even after the implantation of a retinal prosthesis, the patient’s visual acuity is at best less than 20/420. Reduced visual acuity may be explained by a decrease in the signal-to-noise ratio due to the spontaneous hyperactivity of retinal ganglion cells (RGCs) found in degenerate retinas. Unfortunately, abnormal retinal rewiring, commonly observed in degenerate retinas, has rarely been considered for the development of retinal prostheses. The purpose of this study was to investigate the aberrant retinal network response to electrical stimulation in terms of the spatial distribution of the electrically evoked RGC population. An 8 × 8 multielectrode array was used to measure the spiking activity of the RGC population. RGC spikes were recorded in wild-type [C57BL/6J; P56 (postnatal day 56)], rd1 (P56), rd10 (P14 and P56) mice, and macaque [wild-type and drug-induced retinal degeneration (RD) model] retinas. First, we performed a spike correlation analysis between RGCs to determine RGC connectivity. No correlation was observed between RGCs in the control group, including wild-type mice, rd10 P14 mice, and wild-type macaque retinas. In contrast, for the RD group, including rd1, rd10 P56, and RD macaque retinas, RGCs, up to approximately 400–600 μm apart, were significantly correlated. Moreover, to investigate the RGC population response to electrical stimulation, the number of electrically evoked RGC spikes was measured as a function of the distance between the stimulation and recording electrodes. With an increase in the interelectrode distance, the number of electrically evoked RGC spikes decreased exponentially in the control group. In contrast, electrically evoked RGC spikes were observed throughout the retina in the RD group, regardless of the inter-electrode distance. Taken together, in the degenerate retina, a more strongly coupled retinal network resulted in the widespread distribution of electrically evoked RGC spikes. This finding could explain the low-resolution vision in prosthesis-implanted patients.
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spelling pubmed-91144412022-05-19 Correlated Activity in the Degenerate Retina Inhibits Focal Response to Electrical Stimulation Ahn, Jungryul Cha, Seongkwang Choi, Kwang-Eon Kim, Seong-Woo Yoo, Yongseok Goo, Yong Sook Front Cell Neurosci Neuroscience Retinal prostheses have shown some clinical success in patients with retinitis pigmentosa and age-related macular degeneration. However, even after the implantation of a retinal prosthesis, the patient’s visual acuity is at best less than 20/420. Reduced visual acuity may be explained by a decrease in the signal-to-noise ratio due to the spontaneous hyperactivity of retinal ganglion cells (RGCs) found in degenerate retinas. Unfortunately, abnormal retinal rewiring, commonly observed in degenerate retinas, has rarely been considered for the development of retinal prostheses. The purpose of this study was to investigate the aberrant retinal network response to electrical stimulation in terms of the spatial distribution of the electrically evoked RGC population. An 8 × 8 multielectrode array was used to measure the spiking activity of the RGC population. RGC spikes were recorded in wild-type [C57BL/6J; P56 (postnatal day 56)], rd1 (P56), rd10 (P14 and P56) mice, and macaque [wild-type and drug-induced retinal degeneration (RD) model] retinas. First, we performed a spike correlation analysis between RGCs to determine RGC connectivity. No correlation was observed between RGCs in the control group, including wild-type mice, rd10 P14 mice, and wild-type macaque retinas. In contrast, for the RD group, including rd1, rd10 P56, and RD macaque retinas, RGCs, up to approximately 400–600 μm apart, were significantly correlated. Moreover, to investigate the RGC population response to electrical stimulation, the number of electrically evoked RGC spikes was measured as a function of the distance between the stimulation and recording electrodes. With an increase in the interelectrode distance, the number of electrically evoked RGC spikes decreased exponentially in the control group. In contrast, electrically evoked RGC spikes were observed throughout the retina in the RD group, regardless of the inter-electrode distance. Taken together, in the degenerate retina, a more strongly coupled retinal network resulted in the widespread distribution of electrically evoked RGC spikes. This finding could explain the low-resolution vision in prosthesis-implanted patients. Frontiers Media S.A. 2022-05-04 /pmc/articles/PMC9114441/ /pubmed/35602554 http://dx.doi.org/10.3389/fncel.2022.889663 Text en Copyright © 2022 Ahn, Cha, Choi, Kim, Yoo and Goo. 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 Neuroscience
Ahn, Jungryul
Cha, Seongkwang
Choi, Kwang-Eon
Kim, Seong-Woo
Yoo, Yongseok
Goo, Yong Sook
Correlated Activity in the Degenerate Retina Inhibits Focal Response to Electrical Stimulation
title Correlated Activity in the Degenerate Retina Inhibits Focal Response to Electrical Stimulation
title_full Correlated Activity in the Degenerate Retina Inhibits Focal Response to Electrical Stimulation
title_fullStr Correlated Activity in the Degenerate Retina Inhibits Focal Response to Electrical Stimulation
title_full_unstemmed Correlated Activity in the Degenerate Retina Inhibits Focal Response to Electrical Stimulation
title_short Correlated Activity in the Degenerate Retina Inhibits Focal Response to Electrical Stimulation
title_sort correlated activity in the degenerate retina inhibits focal response to electrical stimulation
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9114441/
https://www.ncbi.nlm.nih.gov/pubmed/35602554
http://dx.doi.org/10.3389/fncel.2022.889663
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