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Research Articles, Systems/Circuits

Inference of Electrical Stimulation Sensitivity from Recorded Activity of Primate Retinal Ganglion Cells

Sasidhar S. Madugula, Ramandeep Vilkhu, Nishal P. Shah, Lauren E. Grosberg, Alexandra Kling, Alex R. Gogliettino, Huy Nguyen, Paweł Hottowy, Alexander Sher, Alan M. Litke and E.J. Chichilnisky
Journal of Neuroscience 28 June 2023, 43 (26) 4808-4820; DOI: https://doi.org/10.1523/JNEUROSCI.1023-22.2023
Sasidhar S. Madugula
3Neurosciences PhD Program, Stanford University, Stanford, California 94305
4School of Medicine, Stanford University, Stanford, California 94305
7Hansen Experimental Physics Laboratory, Stanford University, Stanford, California 94305
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Ramandeep Vilkhu
2Department of Electrical Engineering, Stanford University, Stanford, California 94305
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Nishal P. Shah
1Department of Neurosurgery, Stanford University, Stanford, California 94305
2Department of Electrical Engineering, Stanford University, Stanford, California 94305
7Hansen Experimental Physics Laboratory, Stanford University, Stanford, California 94305
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Lauren E. Grosberg
1Department of Neurosurgery, Stanford University, Stanford, California 94305
7Hansen Experimental Physics Laboratory, Stanford University, Stanford, California 94305
9Facebook Reality Labs, Facebook, Mountain View, California 94040
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Alexandra Kling
1Department of Neurosurgery, Stanford University, Stanford, California 94305
7Hansen Experimental Physics Laboratory, Stanford University, Stanford, California 94305
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Alex R. Gogliettino
3Neurosciences PhD Program, Stanford University, Stanford, California 94305
7Hansen Experimental Physics Laboratory, Stanford University, Stanford, California 94305
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Huy Nguyen
1Department of Neurosurgery, Stanford University, Stanford, California 94305
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Paweł Hottowy
8Faculty of Physics and Applied Computer Science, AGH University of Science and Technology, Krakow, Poland 30-059
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Alexander Sher
5Santa Cruz Institute for Particle Physics, University of California, Santa Cruz, California 95064
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Alan M. Litke
5Santa Cruz Institute for Particle Physics, University of California, Santa Cruz, California 95064
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E.J. Chichilnisky
1Department of Neurosurgery, Stanford University, Stanford, California 94305
6Department of Ophthalmology, Stanford University, Stanford, California 94305
7Hansen Experimental Physics Laboratory, Stanford University, Stanford, California 94305
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Abstract

High-fidelity electronic implants can in principle restore the function of neural circuits by precisely activating neurons via extracellular stimulation. However, direct characterization of the individual electrical sensitivity of a large population of target neurons, to precisely control their activity, can be difficult or impossible. A potential solution is to leverage biophysical principles to infer sensitivity to electrical stimulation from features of spontaneous electrical activity, which can be recorded relatively easily. Here, this approach is developed and its potential value for vision restoration is tested quantitatively using large-scale multielectrode stimulation and recording from retinal ganglion cells (RGCs) of male and female macaque monkeys ex vivo. Electrodes recording larger spikes from a given cell exhibited lower stimulation thresholds across cell types, retinas, and eccentricities, with systematic and distinct trends for somas and axons. Thresholds for somatic stimulation increased with distance from the axon initial segment. The dependence of spike probability on injected current was inversely related to threshold, and was substantially steeper for axonal than somatic compartments, which could be identified by their recorded electrical signatures. Dendritic stimulation was largely ineffective for eliciting spikes. These trends were quantitatively reproduced with biophysical simulations. Results from human RGCs were broadly similar. The inference of stimulation sensitivity from recorded electrical features was tested in a data-driven simulation of visual reconstruction, revealing that the approach could significantly improve the function of future high-fidelity retinal implants.

SIGNIFICANCE STATEMENT This study demonstrates that individual in situ primate retinal ganglion cells of different types respond to artificially generated, external electrical fields in a systematic manner, in accordance with theoretical predictions, that allows for prediction of electrical stimulus sensitivity from recorded spontaneous activity. It also provides evidence that such an approach could be immensely helpful in the calibration of clinical retinal implants.

  • biophysics
  • macular degeneration
  • multielectrode array
  • primate
  • retinal electrophysiology
  • retinal ganglion cells

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The Journal of Neuroscience: 43 (26)
Journal of Neuroscience
Vol. 43, Issue 26
28 Jun 2023
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Inference of Electrical Stimulation Sensitivity from Recorded Activity of Primate Retinal Ganglion Cells
Sasidhar S. Madugula, Ramandeep Vilkhu, Nishal P. Shah, Lauren E. Grosberg, Alexandra Kling, Alex R. Gogliettino, Huy Nguyen, Paweł Hottowy, Alexander Sher, Alan M. Litke, E.J. Chichilnisky
Journal of Neuroscience 28 June 2023, 43 (26) 4808-4820; DOI: 10.1523/JNEUROSCI.1023-22.2023

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Inference of Electrical Stimulation Sensitivity from Recorded Activity of Primate Retinal Ganglion Cells
Sasidhar S. Madugula, Ramandeep Vilkhu, Nishal P. Shah, Lauren E. Grosberg, Alexandra Kling, Alex R. Gogliettino, Huy Nguyen, Paweł Hottowy, Alexander Sher, Alan M. Litke, E.J. Chichilnisky
Journal of Neuroscience 28 June 2023, 43 (26) 4808-4820; DOI: 10.1523/JNEUROSCI.1023-22.2023
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Keywords

  • biophysics
  • macular degeneration
  • multielectrode array
  • primate
  • retinal electrophysiology
  • retinal ganglion cells

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