Optogenetic activation of visual thalamus generates artificial visual percepts

Abstract

The lateral geniculate nucleus (LGN), a retinotopic relay center where visual inputs from the retina are processed and relayed to the visual cortex, has been proposed as a potential target for artificial vision. At present, it is unknown whether optogenetic LGN stimulation is sufficient to elicit behaviorally relevant percepts, and the properties of LGN neural responses relevant for artificial vision have not been thoroughly characterized. Here, we demonstrate that tree shrews pretrained on a visual detection task can detect optogenetic LGN activation using an AAV2-CamKIIα-ChR2 construct and readily generalize from visual to optogenetic detection. Simultaneous recordings of LGN spiking activity and primary visual cortex (V1) local field potentials (LFP) during optogenetic LGN stimulation show that LGN neurons reliably follow optogenetic stimulation at frequencies up to 60 Hz, and uncovered a striking phase locking between the V1 local field potential (LFP) and the evoked spiking activity in LGN. These phase relationships were maintained over a broad range of LGN stimulation frequencies, up to 80 Hz, with spike field coherence values favoring higher frequencies, indicating the ability to relay temporally precise information to V1 using light activation of the LGN. Finally, V1 LFP responses showed sensitivity values to LGN optogenetic activation that were similar to the animal's behavioral performance. Taken together, our findings confirm the LGN as a potential target for visual prosthetics in a highly visual mammal closely related to primates.

Data availability

All data used in the production of the figures in this manuscript is freely available at https://datadryad.org/stash/dataset/doi:10.5061/dryad.2z34tmpqk

The following data sets were generated

Article and author information

Author details

  1. Jing Wang

    Department of Medicine, University of Fribourg, Fribourgs, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  2. Hamid Azimi

    Department of Medicine, University of Fribourg, Fribourg, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  3. Yilei Zhao

    Department of Medicine, University of Fribourg, Fribourg, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5146-8493
  4. Melanie Kaeser

    Department of Medicine, University of Fribourg, Fribourg, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  5. Pilar Vaca Sánchez

    Department of Medicine, University of Fribourg, Fribourg, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  6. Abraham Vazquez-Guardado

    Department of Material Science and Engineering, Northwestern University, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0648-5921
  7. John A Rogers

    Department of Material Science and Engineering, Northwestern University, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Michael Harvey

    Department of Medicine, University of Fribourg, Fribourg, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0477-6100
  9. Gregor Rainer

    Department of Medicine, University of Fribourg, Fribourg, Switzerland
    For correspondence
    gregor.rainer@unifr.ch
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5805-2220

Funding

SNSF (182504)

  • Gregor Rainer

University of Fribourg

  • Gregor Rainer

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Kristine Krug, Otto-von-Guericke University Magdeburg, Germany

Ethics

Animal experimentation: All procedures for animal experiments were approved by the local ethical committee on animal experimentation, canton of Fribourg. License number:33056

Version history

  1. Preprint posted: December 8, 2022 (view preprint)
  2. Received: June 23, 2023
  3. Accepted: October 3, 2023
  4. Accepted Manuscript published: October 4, 2023 (version 1)
  5. Version of Record published: October 23, 2023 (version 2)

Copyright

© 2023, Wang et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Jing Wang
  2. Hamid Azimi
  3. Yilei Zhao
  4. Melanie Kaeser
  5. Pilar Vaca Sánchez
  6. Abraham Vazquez-Guardado
  7. John A Rogers
  8. Michael Harvey
  9. Gregor Rainer
(2023)
Optogenetic activation of visual thalamus generates artificial visual percepts
eLife 12:e90431.
https://doi.org/10.7554/eLife.90431

Share this article

https://doi.org/10.7554/eLife.90431

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