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Cited by 24Neuroscience and Neural EngineeringRetinal Development and DisordersPhotoreceptor and optogenetics research

Capacitive-like photovoltaic epiretinal stimulation enhances and narrows the network-mediated activity of retinal ganglion cells by recruiting the lateral inhibitory network

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Chenais, Naïg Aurelia Ludmilla, Leccardi, Marta Jole Ildelfonsa Airaghi, Ghezzi, Diego·2019·Journal of Neural Engineering
DOI 10.1088/1741-2552/ab3913
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Abstract

Photovoltaic retinal prostheses theoretically offer the possibility of stand-alone high-resolution electrical stimulation of the retina. However, achieving focused epiretinal stimulation is particularly challenging because of axonal activation and electrical cell coupling. Recent evidence shows that long electric pulses permit a more focal activation of retinal ganglion cells, and non-rectangular waveforms induce higher network-mediated indirect activity. OBJECTIVE: The role of the pulse shape in focusing the retinal ganglion cell activation and the underlying mechanisms are not yet fully understood. APPROACH: To address this question, we implemented a hybrid ex vivo and in silico approach. We recorded the evoked activity of retinas explanted from retinal degeneration ten mice upon photovoltaic and electrical stimulation with rectangular or non-rectangular capacitive-like voltage pulses. We used a biophysical model to investigate the role of the pulse shape and the pulse duration on the genesis and the extent of the network-mediated activity in retinal ganglion cells. MAIN RESULTS: Altogether, our results suggest that non-rectangular capacitive-like voltage pulses activate more strongly the inner excitatory and inhibitory layers of the retina, when compared to a rectangular stimulation with paired pulse amplitude and duration. This feature leads to an increase of the network-mediated activity and a decrease in the network-mediated electrical receptive field of the stimulated retinal ganglion cell. SIGNIFICANCE: These results demonstrate that recruiting the inner retinal cells with epiretinal stimulation enables us not only to bypass axonal stimulation, but also to obtain a more focal activation due to the natural lateral inhibition. The involvement of the inhibitory feedback from amacrine cells in the genesis of the network-mediated activity represents a novel biological tool with which to confine the response of the retinal ganglion cells. These results support future waveform engineering strategies and offer new perspectives on epiretinal devices to better shape prosthetic perception.

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Crossref · 10.1088/1741-2552/ab3913

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  • The device position and the characteristics of the electrical pulses determine which cell population is predominantly activated.

    “The device position (epiretinal, subretinal or suprachoroidal) and the characteristics of the electrical pulses (such as duration and waveform) determine which cell population is predominantly activated [28,29].”

    From Advances in visual prostheses: engineering and biological challenges (2022) · cites this paper as [29]

  • Using long and non-rectangular pulses mitigates elongated phosphenes by preferentially inducing network-mediated stimulation, resulting in a more localised activation.

    “A way to mitigate this phenomenon is to use long and non-rectangular pulses that will preferentially induce network-mediated stimulation, resulting in a more localised activation [29,31].”

    From Advances in visual prostheses: engineering and biological challenges (2022) · cites this paper as [29]

  • Increasing the pulse duration or using non-rectangular pulses facilitates network-mediated stimulation.

    “Otherwise, increasing the pulse duration [31] or using non-rectangular pulses [29] facilitates network-mediated stimulation.”

    From Advances in visual prostheses: engineering and biological challenges (2022) · cites this paper as [29]

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Authors
Chenais, N. A. L., Leccardi, M. J. I. A., & Ghezzi, D.
Affiliations
École Polytechnique Fédérale de Lausanne (CH)
Corresponding author
Ghezzi, Diego
ORCID
Venue
Journal of Neural Engineering
Publisher
IOP Publishing
Published
2019-10-18
Volume
16
Issue
6
Pages
066009
ISSN
  • 1741-2552 (ISSN-L)
  • 1741-2560
DOI
10.1088/1741-2552/ab3913
OpenAlex
W2966178365
Cited by
24
References
89
Citations by year
2026: 1 · 2025: 2 · 2024: 3 · 2023: 3 · 2022: 2 · 2021: 6 · 2020: 7
FWCI
1.79
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Neural Engineering (publishedVersion)
  • PubMed (publishedVersion)
  • Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
Funders
Fondation Pierre Mercier pour la science
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neural Engineering
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinal Development and Disorders
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Photoreceptor and optogenetics research
Keywords
epiretinal stimulation, retinal ganglion cells, pulse shape, lateral inhibition, amacrine cells, waveform engineering, retinal degeneration
MeSH terms
Animals, Female, Male, Nerve Net, Neural Inhibition, Photic Stimulation, Recruitment, Neurophysiological, Retinal Ganglion Cells, Electric Capacitance, Mice

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