High-fidelity reproduction of visual signals by electrical stimulation in the central primate retina
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Abstract Electrical stimulation of retinal ganglion cells (RGCs) with electronic implants provides rudimentary artificial vision to people blinded by retinal degeneration. However, current devices stimulate indiscriminately and therefore cannot reproduce the intricate neural code of the retina. Recent work has demonstrated more precise activation of RGCs using focal electrical stimulation with multi-electrode arrays in the peripheral macaque retina, but it is unclear how effective this can be in the central retina, which is required for high-resolution vision. This work probes the neural code and effectiveness of focal epiretinal stimulation in the central macaque retina, using large-scale electrical recording and stimulation ex vivo . The functional organization, light response properties, and electrical properties of the major RGC types in the central retina were mostly similar to the peripheral retina, with some notable differences in density, kinetics, linearity, spiking statistics and correlations. The major RGC types could be distinguished by their intrinsic electrical properties. Electrical stimulation targeting parasol cells revealed similar activation thresholds and reduced axon bundle activation in the central retina, but lower stimulation selectivity. Quantitative evaluation of the potential for image reconstruction from electrically-evoked parasol cell signals revealed higher overall expected image quality in the central retina. An exploration of inadvertent midget cell activation suggested that it could contribute high spatial frequency noise to the visual signal carried by parasol cells. These results support the possibility of reproducing high-acuity visual signals in the central retina with an epiretinal implant. Significance Statement Artificial restoration of vision with retinal implants is a major treatment for blindness. However, present-day implants do not provide high-resolution visual perception, in part because they do not reproduce the natural neural code of the retina. Here we demonstrate the level of visual signal reproduction that is possible with a future implant by examining how accurately responses to electrical stimulation of parasol retinal ganglion cells (RGCs) can convey visual signals. Although the precision of electrical stimulation in the central retina was diminished relative to the peripheral retina, the quality of expected visual signal reconstruction in parasol cells was greater. These findings suggest that visual signals could be restored with high fidelity in the central retina using a future retinal implant.
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One solution to improve resolution in epiretinal stimulation would be to selectively activate individual RGCs by establishing a one-to-one connection between RGCs and electrodes.
“One solution would be to selectively activate individual RGCs by establishing a one-to-one connection between RGCs and electrodes [137].”
From Advances in visual prostheses: engineering and biological challenges (2022) · cites this paper as [137]
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Cited by
Sorted by citations
Advances in visual prostheses: engineering and biological challenges
Borda, E., & Ghezzi, D. (2022) · Progress in Biomedical Engineering · doi:10.1088/2516-1091/ac812c · Cited by 44 · see citing works
Focal electrical stimulation of human retinal ganglion cells for vision restoration
Madugula, S. S., Gogliettino, A. R., Zaidi, M., Aggarwal, G., Kling, A., Shah, N. P., Brown, J. B., Vilkhu, R., Hays, M. R., Nguyen, H., et al. (2022) · Journal of Neural Engineering · doi:10.1088/1741-2552/aca5b5 · Cited by 26 · see citing works
Self-citation
- Authors
- Gogliettino, A. R., Madugula, S. S., Grosberg, L. E., Vilkhu, R. S., Brown, J., Nguyen, H., Kling, A., Hottowy, P., Dąbrowski, W., Sher, A., Litke, A. M., & Chichilnisky, E. J.
- Affiliations
- Stanford University (US)
- Stanford Medicine (US)
- AGH University of Krakow (PL)
- University of California, Santa Cruz (US)
- Corresponding author
- Gogliettino, Alex R.
- ORCID
- Venue
- bioRxiv (Cold Spring Harbor Laboratory)
- Publisher
- openRxiv
- Published
- 2022-05-25
- Volume
- 43
- Issue
- 25
- Pages
- 4625-4641
- ISSN
- 0270-6474 (ISSN-L)
- PMC
- PMC10286946
- OpenAlex
- W4376604073
- Cited by
- 30
- References
- 83
- Citations by year
- 2026: 10 · 2025: 8 · 2024: 9 · 2023: 1 · 2022: 2
- FWCI
- 3.40
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc-sa
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Research to Prevent Blindness
- Fondation Bertarelli
- Narodowe Centrum Nauki (DEC-2013/10/M/NZ4/00268)
- National Institutes of Health
- Stanford Bio-X
- Wu Tsai Neurosciences Institute, Stanford University
- National Institute of Mental Health (T32MH020016)
- National Eye Institute (EY019005, P30EY019005, R01EY032900, NEI R01, F30-EY030776-03, EY021271, F30EY030776, F31EY033636, R01EY021271, R01EY029247)
- Division of Undergraduate Education
- California National Primate Research Center
- 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 › Cognitive Neuroscience › Visual perception and processing mechanisms
- Keywords
- retinal prosthesis, epiretinal stimulation, retinal ganglion cells, parasol cells, midget cells, central retina, macaque retina, image reconstruction, neural code, retinal degeneration, artificial vision
- MeSH terms
- Animals, Electric Stimulation, Macaca, Photic Stimulation, Retina, Retinal Ganglion Cells, Prostheses and Implants, Visual Prosthesis
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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