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Spatially selective activation of the visual cortex via intraneural stimulation of the optic nerve

Nature Biomedical Engineering volume 4, pages 181–194 (2020)Cite this article

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Abstract

Retinal prostheses can restore a functional form of vision in patients affected by dystrophies of the outer retinal layer. Beyond clinical utility, prostheses for the stimulation of the optic nerve, the visual thalamus or the visual cortex could also serve as tools for studying the visual system. Optic-nerve stimulation is particularly promising because it directly activates nerve fibres, takes advantage of the high-level information processing occurring downstream in the visual pathway, does not require optical transparency and could be effective in cases of eye trauma. Here we show, in anaesthetized rabbits and with support from numerical modelling, that an intraneural electrode array with high mechanical stability placed in the intracranial segment of the optic nerve induces, on electrical stimulation, selective activation patterns in the visual cortex. These patterns are measured as electrically evoked cortical potentials via an ECoG array placed in the contralateral cortex. The intraneural electrode array should enable further investigations of the effects of electrical stimulation in the visual system and could be further developed as a visual prosthesis for blind patients.

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Fig. 1: The intraneural electrode array OpticSELINE.
Fig. 2: Electrochemical and mechanical characterization.
Fig. 3: Visually evoked cortical potentials.
Fig. 4: Electrically evoked cortical potentials.
Fig. 5: Cortical activation maps.
Fig. 6: Distribution map of the independent components within the optic nerve.
Fig. 7: Probability activation map of the optic nerve.
Fig. 8: High-frequency stimulation of the optic nerve.

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Data availability

The authors declare that all data supporting the results in this study are available within the paper and its Supplementary Information. The raw and analysed datasets generated during the study are available for research purposes from the corresponding author on reasonable request.

Code availability

Code used for the hybrid FEA model and NEURON simulation is available at https://github.com/lne-lab/nBME2019. The authors declare that the algorithm used for blind source separation is described in the referenced papers. The source code can be obtained from S.M. (silvestro.micera@epfl.ch) upon reasonable request.

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Acknowledgements

We acknowledge the support from the Bioelectron Microscopy Core Facility (BIOEM) of École polytechnique fédérale de Lausanne. This work has been supported by École polytechnique fédérale de Lausanne, Medtronic, Bertarelli Foundation and Wyss Center for Bio and Neuroengineering. F.A. is supported by the European Union’s Horizon 2020 research and innovation programme under Marie Skłodowska-Curie Action agreement no. 750947 (BIREHAB).

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Author notes

  1. These authors contributed equally: Vivien Gaillet, Annarita Cutrone, Fiorenzo Artoni.

  2. These authors jointly supervised this work: Silvestro Micera, Diego Ghezzi.

Authors and Affiliations

  1. Medtronic Chair in Neuroengineering, Center for Neuroprosthetics and Institute of Bioengineering, School of Engineering, École polytechnique fédérale de Lausanne, Geneva, Switzerland

    Vivien Gaillet, Paola Vagni, Ariastity Mega Pratiwi, Sandra Alejandra Romero & Diego Ghezzi

  2. The BioRobotics Institute, Scuola Superiore Sant’Anna, Pisa, Italy

    Annarita Cutrone, Fiorenzo Artoni, Dario Lipucci Di Paola & Silvestro Micera

  3. Bertarelli Foundation Chair in Translational Neuroengineering, Center for Neuroprosthetics and Institute of Bioengineering, School of Engineering, École polytechnique fédérale de Lausanne, Geneva, Switzerland

    Fiorenzo Artoni & Silvestro Micera

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  1. Vivien Gaillet
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Contributions

V.G. designed the stimulation protocol and performed the modelling and simulation, blind source separation and data analysis. A.C. designed and fabricated the OpticSELINE and performed mechanical and electrochemical characterizations. F.A. conceived and performed the blind source separation approach. P.V. performed in vivo and histological experiments. A.M.P. performed the modelling and simulation. S.A.R. participated in the design of the stimulation protocol and data analysis. D.L.D.P. participated in the design and microfabrication of the OpticSELINE and performed mechanical characterizations. S.M. supervised the activities related to electrode development and the blind source separation approach. D.G. designed the study, led the project and wrote the manuscript. All the authors read, edited, and accepted the manuscript.

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Correspondence to Diego Ghezzi.

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Gaillet, V., Cutrone, A., Artoni, F. et al. Spatially selective activation of the visual cortex via intraneural stimulation of the optic nerve. Nat Biomed Eng 4, 181–194 (2020). https://doi.org/10.1038/s41551-019-0446-8

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