High-Fidelity Reproduction of Visual Signals by Electrical Stimulation in the Central Primate Retina
Open accessAbstract
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 multielectrode 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 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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Generating a punctate percept through electrical stimulation would require appropriately stimulating many hundreds or thousands of neurons.
“Conversely, generating a punctate percept through electrical stimulation would require appropriately stimulating many hundreds or thousands of neurons95.”
From A virtual patient simulation modeling the neural and perceptual effects of human visual cortical stimulation, from pulse trains to percepts (2024) · cites this paper as [95]
Cites
Adam: A Method for Stochastic Optimization
Kingma, D. P., & Ba, J. (2014) · arXiv · doi:10.48550/arxiv.1412.6980 · Cited by 98,946 · see citing works
Image quality assessment: from error visibility to structural similarity
Wang, Z., Bovik, A. C., Sheikh, H. R., & Simoncelli, E. P. (2004) · IEEE Transactions on Image Processing · doi:10.1109/tip.2003.819861 · Cited by 57,892 · see citing works
SciPy 1.0: fundamental algorithms for scientific computing in Python
Virtanen, P., Gommers, R., Oliphant, T. E., Haberland, M., Reddy, T., Cournapeau, D., Burovski, E., Peterson, P., Weckesser, W., Bright, J., et al. (2020) · Nature Methods · doi:10.1038/s41592-019-0686-2 · Cited by 38,430 · see citing works
Harris, C. R., Millman, K. J., van der Walt, S. J., Gommers, R., Virtanen, P., Cournapeau, D., Wieser, E., Taylor, J., Berg, S., Smith, N. J., et al. (2020) · Nature · doi:10.1038/s41586-020-2649-2 · Cited by 23,826 · see citing works
SciPy 1.0: fundamental algorithms for scientific computing in Python
Virtanen, P., Gommers, R., Oliphant, T. E., Haberland, M., Reddy, T., Cournapeau, D., Burovski, E., Peterson, P., Weckesser, W., Bright, J., et al. (2019) · Apollo - University of Cambridge Repository · doi:10.17863/cam.64134 · Cited by 10,460 · see citing works
Frequency Dependence of Signal Power and Spatial Reach of the Local Field Potential
Leski, S., Lindén, H., Tetzlaff, T., Pettersen, K. H., & Einevoll, G. T. (2013) · PubMed Central · doi:10.18154/rwth-conv-084442 · Cited by 3,662 · see citing works
Spatio-temporal correlations and visual signalling in a complete neuronal population
Pillow, J. W., Shlens, J., Paninski, L., Sher, A., Litke, A. M., Chichilnisky, E. J., & Simoncelli, E. P. (2008) · Nature · doi:10.1038/nature07140 · Cited by 1,315 · see citing works
Self-citationA simple white noise analysis of neuronal light responses
Chichilnisky, E. J. (2001) · Network Computation in Neural Systems · doi:10.1080/net.12.2.199.213 · Cited by 788 · see citing works
Self-citationQuantitative analysis of cat retinal ganglion cell response to visual stimuli
Rodieck, R. W. (1965) · Vision Research · doi:10.1016/0042-6989(65)90033-7 · Cited by 766 · see citing works
Analysis of Models for External Stimulation of Axons
Rattay, F. (1986) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.1986.325670 · Cited by 681 · see citing works
The basic mechanism for the electrical stimulation of the nervous system
Rattay, F. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00330-3 · Cited by 572 · see citing works
Luminance and chromatic modulation sensitivity of macaque ganglion cells and human observers
Lee, B. B., Pokorny, J., Martin, P. R., Valbergt, A., & Smith, V. C. (1990) · Journal of the Optical Society of America A · doi:10.1364/josaa.7.002223 · Cited by 504 · see citing works
Dendritic field size and morphology of midget and parasol ganglion cells of the human retina.
Dacey, D. M., & Petersen, M. R. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.20.9666 · Cited by 495 · see citing works
The Structure of Multi-Neuron Firing Patterns in Primate Retina
Shlens, J., Field, G. D., Gauthier, J. L., Grivich, M. I., Petrusca, D., Sher, A., Litke, A. M., & Chichilnisky, E. J. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.1282-06.2006 · Cited by 471 · see citing works
Self-citationLinear and nonlinear spatial subunits in Y cat retinal ganglion cells.
Hochstein, S., & Shapley, R. M. (1976) · The Journal of Physiology · doi:10.1113/jphysiol.1976.sp011595 · Cited by 471 · see citing works
Functional Asymmetries in ON and OFF Ganglion Cells of Primate Retina
Chichilnisky, E. J., & Kalmar, R. S. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-07-02737.2002 · Cited by 463 · see citing works
Self-citationMeister, M., & Berry, M. J. (1999) · Neuron · doi:10.1016/s0896-6273(00)80700-x · Cited by 431 · see citing works
Decoding Visual Information From a Population of Retinal Ganglion Cells
Warland, D. K., Reinagel, P., & Meister, M. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.78.5.2336 · Cited by 415 · see citing works
Parasol and midget ganglion cells of the human retina
Rodieck, R. W., Binmoeller, K. F., & Dineen, J. T. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902330107 · Cited by 413 · see citing works
Functional connectivity in the retina at the resolution of photoreceptors
Field, G. D., Gauthier, J. L., Sher, A., Greschner, M., Machado, T. A., Jepson, L. H., Shlens, J., Gunning, D. E., Mathieson, K., Dąbrowski, W., et al. (2010) · Nature · doi:10.1038/nature09424 · Cited by 354 · see citing works
Self-citationElectrical Stimulation of Mammalian Retinal Ganglion Cells With Multielectrode Arrays
Sekirnjak, C., Hottowy, P., Sher, A., Dąbrowski, W., Litke, A. M., & Chichilnisky, E. J. (2006) · Journal of Neurophysiology · doi:10.1152/jn.01168.2005 · Cited by 336 · see citing works
Self-citationHigh-resolution CMOS MEA platform to study neurons at subcellular, cellular, and network levels
Müller, J., Ballini, M., Livi, P., Chen, Y., Radivojević, M., Shadmani, A., Viswam, V., Jones, I. L., Michele, F., Diggelmann, R., et al. (2015) · Lab on a Chip · doi:10.1039/c5lc00133a · Cited by 329 · see citing works
Sensitivity of macaque retinal ganglion cells to chromatic and luminance flicker.
Lee, B. B., Martin, P. R., & Valberg, A. (1989) · The Journal of Physiology · doi:10.1113/jphysiol.1989.sp017685 · Cited by 312 · see citing works
ImageNet: Constructing a large-scale image database
Fei-Fei, L., Deng, J., & Li, K. (2010) · Journal of Vision · doi:10.1167/9.8.1037 · Cited by 295 · see citing works
Parasol and midget ganglion cells of the primate retina
WATANABE, M., & Rodieck, R. W. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902890308 · Cited by 290 · see citing works
Litke, A. M., Bezayiff, N., Chichilnisky, E. J., Cunningham, W. R., Dąbrowski, W., Grillo, A. A., Grivich, M., Gryboś, P., Hottowy, P., Kachiguine, S., et al. (2004) · IEEE Transactions on Nuclear Science · doi:10.1109/tns.2004.832706 · Cited by 279 · see citing works
Self-citationHodgkin, A. L. (1954) · The Journal of Physiology · doi:10.1113/jphysiol.1954.sp005152 · Cited by 268 · see citing works
Correlated firing of cat retinal ganglion cells. I. Spontaneously active inputs to X- and Y-cells
Mastronarde, D. N. (1983) · Journal of Neurophysiology · doi:10.1152/jn.1983.49.2.303 · Cited by 260 · see citing works
Deep Learning Models of the Retinal Response to Natural Scenes.
McIntosh, L., Maheswaranathan, N., Nayebi, A., Ganguli, S., & Baccus, S. A. (2016) · PubMed · Cited by 205 · see citing works
Current focusing and steering: Modeling, physiology, and psychophysics
Bonham, B. H., & Litvak, L. M. (2008) · Hearing Research · doi:10.1016/j.heares.2008.03.006 · Cited by 198 · see citing works
A nerve cuff technique for selective excitation of peripheral nerve trunk regions
Sweeney, J. D., Ksienski, D. A., & Mortimer, J. T. (1990) · IEEE Transactions on Biomedical Engineering · doi:10.1109/10.55681 · Cited by 196 · see citing works
Retinal Prostheses: Current Clinical Results and Future Needs
Weiland, J. D., Cho, A. K., & Humayun, M. S. (2011) · Ophthalmology · doi:10.1016/j.ophtha.2011.08.042 · Cited by 196 · see citing works
High-Resolution Electrical Stimulation of Primate Retina for Epiretinal Implant Design
Sekirnjak, C., Hottowy, P., Sher, A., Dąbrowski, W., Litke, A. M., & Chichilnisky, E. J. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.5138-07.2008 · Cited by 195 · see citing works
Self-citationSpatial steering of deep brain stimulation volumes using a novel lead design
Martens, H. C. F., Toader, E., Decré, M., Anderson, D. J., Vetter, R. J., Kipke, D. R., Baker, K. B., Johnson, M. D., & Vitek, J. L. (2010) · Clinical Neurophysiology · doi:10.1016/j.clinph.2010.07.026 · Cited by 195 · see citing works
Field, G. D., Sher, A., Gauthier, J. L., Greschner, M., Shlens, J., Litke, A. M., & Chichilnisky, E. J. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3437-07.2007 · Cited by 185 · see citing works
Self-citationCellular and Circuit Mechanisms Shaping the Perceptual Properties of the Primate Fovea
Sinha, R., Hoon, M., Baudin, J., Okawa, H., Wong, R., & Rieke, F. M. (2017) · Cell · doi:10.1016/j.cell.2017.01.005 · Cited by 170 · see citing works
The Structure of Large-Scale Synchronized Firing in Primate Retina
Shlens, J., Field, G. D., Gauthier, J. L., Greschner, M., Sher, A., Litke, A. M., & Chichilnisky, E. J. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5187-08.2009 · Cited by 148 · see citing works
Self-citationIdentification and Characterization of a Y-Like Primate Retinal Ganglion Cell Type
Petrusca, D., Grivich, M. I., Sher, A., Field, G. D., Gauthier, J. L., Greschner, M., Shlens, J., Chichilnisky, E. J., & Litke, A. M. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2836-07.2007 · Cited by 148 · see citing works
Self-citationReduction of Electrical Interaction in Auditory Prostheses
Townshend, B., & White, R. L. (1987) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.1987.326102 · Cited by 139 · see citing works
Deep Learning Models of the Retinal Response to Natural ScenesPreprint
McIntosh, L., Maheswaranathan, N., Nayebi, A., Ganguli, S., & Baccus, S. A. (2017) · arXiv (Cornell University) · doi:10.48550/arxiv.1702.01825 · Cited by 139 · see citing works
Receptive Fields in Primate Retina Are Coordinated to Sample Visual Space More Uniformly
Gauthier, J. L., Field, G. D., Sher, A., Greschner, M., Shlens, J., Litke, A. M., & Chichilnisky, E. J. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000063 · Cited by 138 · see citing works
Self-citationOrigin of correlated activity between parasol retinal ganglion cells
Trong, P. K., & Rieke, F. M. (2008) · Nature Neuroscience · doi:10.1038/nn.2199 · Cited by 117 · see citing works
Spatially patterned electrical stimulation to enhance resolution of retinal prostheses
Jepson, L. H., Hottowy, P., Mathieson, K., Gunning, D. E., Dąbrowski, W., Litke, A. M., & Chichilnisky, E. J. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.2882-13.2014 · Cited by 103 · see citing works
Self-citationChanges in physiological properties of rat ganglion cells during retinal degeneration
Sekirnjak, C., Jepson, L. H., Hottowy, P., Sher, A., Dąbrowski, W., Litke, A. M., & Chichilnisky, E. J. (2011) · Journal of Neurophysiology · doi:10.1152/jn.01061.2010 · Cited by 102 · see citing works
Self-citationElectronic approaches to restoration of sight
Goetz, G. A., & Palanker, D. (2016) · Reports on Progress in Physics · doi:10.1088/0034-4885/79/9/096701 · Cited by 99 · see citing works
The number and diameter distribution of axons in the monkey optic nerve.
Sanchez, R. M., Dunkelberger, G. R., & Quigley, H. A. (1986) · PubMed · Cited by 97 · see citing works
Jepson, L. H., Hottowy, P., Mathieson, K., Gunning, D. E., Dąbrowski, W., Litke, A. M., & Chichilnisky, E. J. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.4967-12.2013 · Cited by 97 · see citing works
Self-citationThe Temporal Raphe of the Human Retina
Vrabec, F. (1966) · American Journal of Ophthalmology · doi:10.1016/0002-9394(66)91920-9 · Cited by 92 · see citing works
Electrical Stimulation of the Retina to Produce Artificial Vision
Weiland, J. D., Walston, S. T., & Humayun, M. S. (2016) · Annual Review of Vision Science · doi:10.1146/annurev-vision-111815-114425 · Cited by 85 · see citing works
Orientation sensitivity of ganglion cells in primate retina
Passaglia, C. L., Troy, J. B., Rüttiger, L., & Lee, B. B. (2002) · Vision Research · doi:10.1016/s0042-6989(01)00312-1 · Cited by 76 · see citing works
Testing pseudo-linear models of responses to natural scenes in primate retinaPreprint
Heitman, A., Brackbill, N., Greschner, M., Sher, A., Litke, A. M., & Chichilnisky, E. J. (2016) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/045336 · Cited by 73 · see citing works
Self-citationHigh-Fidelity Reproduction of Spatiotemporal Visual Signals for Retinal Prosthesis
Jepson, L. H., Hottowy, P., Weiner, G., Dąbrowski, W., Litke, A. M., & Chichilnisky, E. J. (2014) · Neuron · doi:10.1016/j.neuron.2014.04.044 · Cited by 71 · see citing works
Self-citationCorrelated firing among major ganglion cell types in primate retina
Greschner, M., Shlens, J., Bakolitsa, C., Field, G. D., Gauthier, J. L., Jepson, L. H., Sher, A., Litke, A. M., & Chichilnisky, E. J. (2010) · The Journal of Physiology · doi:10.1113/jphysiol.2010.193888 · Cited by 71 · see citing works
Self-citationEffective Electrode Configuration for Selective Stimulation With Inner Eye Prostheses
Rattay, F., & Resatz, S. (2004) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2004.828044 · Cited by 70 · see citing works
Activation of ganglion cells and axon bundles using epiretinal electrical stimulation
Grosberg, L. E., Ganesan, K., Goetz, G. A., Madugula, S. S., Bhaskhar, N., Fan, V., Li, P., Hottowy, P., Dabrowski, W., Sher, A., et al. (2017) · Journal of Neurophysiology · doi:10.1152/jn.00750.2016 · Cited by 70 · see citing works
Self-citationHottowy, P., Skoczeń, A., Gunning, D. E., Kachiguine, S., Mathieson, K., Sher, A., Wiącek, P., Litke, A. M., & Dąbrowski, W. (2012) · Journal of Neural Engineering · doi:10.1088/1741-2560/9/6/066005 · Cited by 67 · see citing works
Self-citationAmplitude and phase of responses of macaque retinal ganglion cells to flickering stimuli.
Lee, B. B., Martin, P. R., & Valberg, A. (1989) · The Journal of Physiology · doi:10.1113/jphysiol.1989.sp017686 · Cited by 66 · see citing works
Anatomical Identification of Extracellularly Recorded Cells in Large-Scale Multielectrode Recordings
Li, P. H., Gauthier, J. L., Schiff, M. L., Sher, A., Ahn, D., Field, G. D., Greschner, M., Callaway, E. M., Litke, A. M., & Chichilnisky, E. J. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.3675-14.2015 · Cited by 61 · see citing works
Self-citationReconstruction of natural visual scenes from neural spikes with deep neural networks
Zhang, Y., Jia, S., Zheng, Y., Yu, Z., Tian, Y., Ma, S., Huang, T., & Liu, J. K. (2020) · Neural Networks · doi:10.1016/j.neunet.2020.01.033 · Cited by 59 · see citing works
Unusual Physiological Properties of Smooth Monostratified Ganglion Cell Types in Primate Retina
Rhoades, C. E., Shah, N. P., Manookin, M. B., Brackbill, N., Kling, A., Goetz, G., Sher, A., Litke, A. M., & Chichilnisky, E. J. (2019) · Neuron · doi:10.1016/j.neuron.2019.05.036 · Cited by 58 · see citing works
Self-citationReconstruction of natural images from responses of primate retinal ganglion cells
Brackbill, N., Rhoades, C., Kling, A., Shah, N. P., Sher, A., Litke, A. M., & Chichilnisky, E. (2020) · eLife · doi:10.7554/elife.58516 · Cited by 57 · see citing works
Self-citationModulation sensitivity of ganglion cells in peripheral retina of macaque
Solomon, S. G., Martin, P. R., White, A. J. R., Rüttiger, L., & Lee, B. B. (2002) · Vision Research · doi:10.1016/s0042-6989(02)00414-5 · Cited by 56 · see citing works
Uniform Signal Redundancy of Parasol and Midget Ganglion Cells in Primate Retina
Gauthier, J. L., Field, G. D., Sher, A., Shlens, J., Greschner, M., Litke, A. M., & Chichilnisky, E. J. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5294-08.2009 · Cited by 53 · see citing works
Self-citationNeural Networks for Efficient Bayesian Decoding of Natural Images from Retinal NeuronsPreprint
Parthasarathy, N., Batty, E., Falcon, W., Rutten, T., Rajpal, M., Chichilnisky, E. J., & Paninski, L. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/153759 · Cited by 52 · see citing works
Self-citationEpiretinal stimulation with local returns enhances selectivity at cellular resolution
Fan, V. H., Grosberg, L. E., Madugula, S. S., Hottowy, P., Dąbrowski, W., Sher, A., Litke, A. M., & Chichilnisky, E. J. (2018) · Journal of Neural Engineering · doi:10.1088/1741-2552/aaeef1 · Cited by 43 · see citing works
Self-citationInference of nonlinear receptive field subunits with spike-triggered clustering
Shah, N. P., Brackbill, N., Rhoades, C. E., Kling, A., Goetz, G. A., Litke, A. M., Sher, A., Simoncelli, E. P., & Chichilnisky, E. J. (2020) · eLife · doi:10.7554/elife.45743 · Cited by 41 · see citing works
Self-citationOptimization of Electrical Stimulation for a High-Fidelity Artificial Retina
Shah, N. P., Madugula, S., Grosberg, L., Mena, G., Tandon, P., Hottowy, P., Sher, A., Litke, A., Mitra, S., & Chichilnisky, E. J. (2019) · 2019 9th International IEEE/EMBS Conference on Neural Engineering (NER) · doi:10.1109/ner.2019.8716987 · Cited by 32 · see citing works
Self-citationYu, W., Grzywacz, N. M., Lee, E.-J., & Field, G. D. (2017) · Journal of Neurophysiology · doi:10.1152/jn.00826.2016 · Cited by 30 · see citing works
Mean retinal ganglion cell axon diameter varies with location in the human retina
Fitzgibbon, T., & Taylor, S. F. (2012) · Japanese Journal of Ophthalmology · doi:10.1007/s10384-012-0185-9 · Cited by 27 · see citing works
Hottowy, P., Dąbrowski, W., Skoczeń, A., & Wiacek, P. K. (2007) · Analog Integrated Circuits and Signal Processing · doi:10.1007/s10470-007-9125-x · Cited by 27 · see citing works
Self-citationHsiao, C., Watanabe, M., & Fukuda, Y. (1984) · Brain Research · doi:10.1016/0006-8993(84)90604-8 · Cited by 26 · see citing works
Recognizing retinal ganglion cells in the dark
Richard, É., Goetz, G. A., & Chichilnisky, E. J. (2015) · neural information processing systems · Cited by 26 · see citing works
Self-citationNonlinear Decoding of Natural Images From Large-Scale Primate Retinal Ganglion Recordings
Kim, Y. J., Brackbill, N., Batty, E., Lee, J., Mitelut, C., Tong, W. L., Chichilnisky, E. J., & Paninski, L. (2021) · Neural Computation · doi:10.1162/neco_a_01395 · Cited by 26 · see citing works
Self-citationFocal 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-citationFukuda, Y., Watanabe, M., Wakakuwa, K., Sawai, H., & Morigiwa, K. (1988) · Neuroscience Research · doi:10.1016/0168-0102(88)90006-5 · Cited by 25 · see citing works
Spatially patterned bi-electrode epiretinal stimulation for axon avoidance at cellular resolution
Vilkhu, R. S., Madugula, S. S., Grosberg, L. E., Gogliettino, A. R., Hottowy, P., Dąbrowski, W., Sher, A., Litke, A. M., Mitra, S., & Chichilnisky, E. J. (2021) · Journal of Neural Engineering · doi:10.1088/1741-2552/ac3450 · Cited by 18 · see citing works
Self-citationIntraretinal axon diameters of a New World primate, the marmoset (Callithrix jacchus)
Walsh, N., Ghosh, K. K., & FitzGibbon, T. (2000) · Clinical and Experimental Ophthalmology · doi:10.1046/j.1442-9071.2000.00347.x · Cited by 17 · see citing works
Precise control of neural activity using dynamically optimized electrical stimulation
Shah, N. P., Phillips, A., Madugula, S., Lotlikar, A., Gogliettino, A. R., Hays, M. R., Grosberg, L., Brown, J., Dusi, A., Tandon, P., et al. (2024) · eLife · doi:10.7554/elife.83424 · Cited by 15 · see citing works
Self-citationChen, Z., Song, Y., Yao, J., Weng, C., & Yin, Z. Q. (2013) · Journal of Molecular Neuroscience · doi:10.1007/s12031-013-0082-9 · Cited by 14 · see citing works
Precise control of neural activity using dynamically optimized electrical stimulationPreprint
Shah, N. P., Phillips, A., Madugula, S., et al. (2024) · bioRxiv · doi:10.1101/2022.07.26.501643 · Cited by 14 · see citing works
Self-citationBestel, R., Appali, R., van Rienen, U., & Thielemann, C. (2017) · Neural Computation · doi:10.1162/neco_a_01019 · Cited by 13 · see citing works
Automatic Identification of Axon Bundle Activation for Epiretinal Prosthesis
Tandon, P., Bhaskhar, N., Shah, N. P., Madugula, S. S., Grosberg, L. E., Fan, V. H., Hottowy, P., Sher, A., Litke, A. M., Chichilnisky, E. J., et al. (2021) · IEEE Transactions on Neural Systems and Rehabilitation Engineering · doi:10.1109/tnsre.2021.3128486 · Cited by 11 · see citing works
Self-citationRetinal Ganglion Cells: Anatomy
MARSHAK, D. W. (2009) · Elsevier eBooks · doi:10.1016/b978-008045046-9.00897-4 · Cited by 10 · see citing works
Madugula, S. S., Vilkhu, R. S., Shah, N. P., Grosberg, L. E., Kling, A., Gogliettino, A. R., Nguyen, H., Hottowy, P., Sher, A., Litke, A. M., et al. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.1023-22.2023 · Cited by 10 · see citing works
Self-citationInferring light responses of primate retinal ganglion cells using intrinsic electrical signatures
Zaidi, M. H., Aggarwal, G., Shah, N. P., Karniol-Tambour, O., Goetz, G. A., Madugula, S. S., Gogliettino, A. R., Wu, E. G., Kling, A., Brackbill, N., et al. (2023) · Journal of Neural Engineering · doi:10.1088/1741-2552/ace657 · Cited by 8 · see citing works
Self-citationChanges in intrinsic excitability of ganglion cells in degenerated retinas of RCS rats
Ren, Y., Weng, C., Zhao, C., & Yin, Z. (2018) · International Journal of Ophthalmology · doi:10.18240/ijo.2018.05.07 · Cited by 6 · see citing works
Efficient characterization of electrically evoked responses for neural interfaces
Shah, N. P., Madugula, S. S., Hottowy, P., Sher, A., Litke, A. M., Paninski, L., & Chichilnisky, E. J. (2019) · neural information processing systems · Cited by 6 · see citing works
Self-citationWu, E. G., Brackbill, N., Sher, A., Litke, A. M., Simoncelli, E. P., & Chichilnisky, E. J. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.05.19.492737 · Cited by 4 · see citing works
Self-citationMadugula, S. S., Vilkhu, R. S., Shah, N. P., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.10.22.465478 · Cited by 3 · see citing works
Self-citationInferring light responses of primate retinal ganglion cells using intrinsic electrical signaturesPreprint
Zaidi, M. H., Aggarwal, G., Shah, N. P., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.05.29.493858 · Cited by 3 · see citing works
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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-citationNeural vs Neuromorphic Interfaces: Where Are We Standing?
Rana, D., Babushkina, N., Gini, M., Cáceres, A., Li, H., Maybeck, V., Criscuolo, V., Mayer, D., Ienca, M., Musall, S., et al. (2025) · Chemical Reviews · doi:10.1021/acs.chemrev.4c00862 · Cited by 29 · see citing works
Fine, I., & Boynton, G. M. (2024) · Scientific Reports · doi:10.1038/s41598-024-65337-1 · Cited by 19 · see citing works
Precise control of neural activity using dynamically optimized electrical stimulation
Shah, N. P., Phillips, A., Madugula, S., Lotlikar, A., Gogliettino, A. R., Hays, M. R., Grosberg, L., Brown, J., Dusi, A., Tandon, P., et al. (2024) · eLife · doi:10.7554/elife.83424 · Cited by 15 · see citing works
Self-citationDecoding dynamic visual scenes across the brain hierarchy
Chen, Y., Beech, P., Yin, Z., Jia, S., Zhang, J., Yu, Z., & Liu, J. K. (2024) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1012297 · Cited by 12 · see citing works
Ly, K., Italiano, M. L., Shivdasani, M. N., Tsai, D., Zhang, J., Jiang, C., Lovell, N. H., Dokos, S., & Guo, T. (2025) · Brain stimulation · doi:10.1016/j.brs.2025.01.013 · Cited by 12 · see citing works
Understanding responses to multi-electrode epiretinal stimulation using a biophysical model
Vilkhu, R. S., Vasireddy, P. K., Kish, K. E., Gogliettino, A. R., Lotlikar, A., Hottowy, P., Dąbrowski, W., Sher, A., Litke, A. M., Mitra, S., et al. (2024) · Journal of Neural Engineering · doi:10.1088/1741-2552/ada1fe · Cited by 8 · see citing works
Self-citationAvoidance of axonal stimulation with sinusoidal epiretinal stimulation
Corna, A., Cojocaru, A.-E., Bui, M. T., Werginz, P., & Zeck, G. M. (2024) · Journal of Neural Engineering · doi:10.1088/1741-2552/ad38de · Cited by 8 · see citing works
Asymmetric activation of retinal ON and OFF pathways by AOSLO raster-scanned visual stimuli
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Physiological basis of resolution acuity in vision
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Self-citationVasireddy, P. K., Vilkhu, R. S., Lotlikar, A., Brown, J. B., Phillips, A., Gogliettino, A. R., Hays, M. R., Baum, C., Kato, E. J., Sharon, A., et al. (2026) · Cell Reports · doi:10.1016/j.celrep.2025.116917 · Cited by 3 · see citing works
Self-citationEfficient Modeling and Calibration of Multi-Electrode Stimuli for Epiretinal Implants
Vasireddy, P. K., Gogliettino, A. R., Brown, J. B., Vilkhu, R. S., Madugula, S. S., Phillips, A. J., Mitral, S., Hottowy, P., Sher, A., Litke, A., et al. (2023) · 2023 11th International IEEE/EMBS Conference on Neural Engineering (NER) · doi:10.1109/ner52421.2023.10123907 · Cited by 2 · see citing works
Self-citationInsights into retinal remodeling in retinal degenerative disease
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Spike sorting in the presence of stimulation artifacts: a dynamical control systems approach
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Self-citationBaez, H. C., LaPorta, J. M., Walker, A. D., Fischer, W. S., Hollar, R., Patterson, S. S., DiLoreto, D. A., Gullapalli, V. K., & McGregor, J. E. (2025) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.66.12.25 · Cited by 1 · see citing works
Comparison of modulation efficiency between normal and degenerated primate retina
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Short Pulse Epiretinal Stimulation Allows Focal Activation of Retinal Ganglion Cells
Koppenwallner, L. X., Zeck, G. M., & Werginz, P. (2025) · IEEE Transactions on Neural Systems and Rehabilitation Engineering · doi:10.1109/tnsre.2025.3529940
Partial input loss differentially modifies neural pathwaysPreprint
Lee, J. Y., Yang, J., Harris, S. C., John, J. V., Stone, N. S., Santina, L. D., Kastner, D. B., & Dunn, F. A. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.02.14.638366
Retinal Ganglion Cell Diversity in Disease: Clinical Implications and Type-Specific Evaluation
Makam, R., Rider, A. T., Yu‐Wai‐Man, P., & Gilhooley, M. J. (2025) · Journal of Neuro-Ophthalmology · doi:10.1097/wno.0000000000002381
Functional Imaging of Cone Photoreceptors
Sincich, L. C., Sabesan, R., Tuten, W. S., Meadway, A., Roorda, A., & Harmening, W. M. (2026) · Springer series in vision research · doi:10.1007/978-3-032-09457-5_4
An Invitation to Visual Computing
Zhu, Y. (2026) · Synthesis lectures on computer architecture · doi:10.1007/978-3-032-05018-2_1
A Novel, Low-Cost, 3D-Printed Motorized Injector for Retinal Sheet Transplantation
Lim, J., Ung, F., Malhotra, S., Diaz, J., Hamilton, A., Chen, C., Tang, W. C., Seiler, M. J., & Browne, A. W. (2026) · Bioengineering · doi:10.3390/bioengineering13020188
Cottaris, N. P., Wandell, B. A., & Brainard, D. H. (2026) · Journal of Computational Neuroscience · doi:10.1007/s10827-026-00930-z
Phillips, A., Lotlikar, A., Kling, A., Hays, M. R., Vasireddy, P. K., Hofflich, B., Sharon, A., Sommeling, M., Brown, J. B., Baum, C., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.05.04.721188
Self-citationKato, E. J., Vasireddy, P. K., Lotlikar, A., Brown, J. B., Phillips, A., Hottowy, P., Sher, A., Litke, A. M., Mitra, S., Shah, N. P., et al. (2025) · International IEEE/EMBS Conference on Neural Engineering · doi:10.1109/ner61569.2025.11588965
Self-citationPartial input loss differentially modifies neural pathwaysPreprint
Lee, J. Y., Yang, J., Harris, S. C., John, J. V., Stone, N. S., Santina, L. D., Kastner, D. B., & Dunn, F. A. (2026) · eLife · doi:10.7554/elife.112552
Partial input loss differentially modifies neural pathwaysPreprint
Lee, J. Y., Yang, J., Harris, S. C., John, J. V., Stone, N. S., Santina, L. D., Kastner, D. B., & Dunn, F. A. (2026) · eLife · doi:10.7554/elife.112552.1
- 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
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2023-05-15
- Volume
- 43
- Issue
- 25
- Pages
- 4625-4641
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC10286946
- OpenAlex
- W4376604073
- Cited by
- 30
- References
- 88
- Citations by year
- 2026: 10 · 2025: 8 · 2024: 9 · 2023: 1 · 2022: 2
- FWCI
- 3.38
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- HHS | NIH | National Eye Institute (F31EY033636, F30-EY030776-03, R01-EY021271, R01-EY029247, P30-EY019005)
- Polish National Science Centre (DEC-2013/10/M/NZ4/00268)
- 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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