Similar neural and perceptual masking effects of low-power optogenetic stimulation in primate V1

  1. Spencer Chin-Yu Chen
  2. Giacomo Benvenuti
  3. Yuzhi Chen
  4. Satwant Kumar
  5. Charu Ramakrishnan
  6. Karl Deisseroth
  7. Wilson S Geisler
  8. Eyal Seidemann  Is a corresponding author
  1. Rutgers University, United States
  2. The University of Texas at Austin, United States
  3. Stanford University, United States

Abstract

Can direct stimulation of primate V1 substitute for a visual stimulus and mimic its perceptual effect? To address this question, we developed an optical-genetic toolkit to 'read' neural population responses using widefield calcium imaging, while simultaneously using optogenetics to 'write' neural responses into V1 of behaving macaques. We focused on the phenomenon of visual masking, where detection of a dim target is significantly reduced by a co-localized medium-brightness mask [1, 2]. Using our toolkit, we tested whether V1 optogenetic stimulation can recapitulate the perceptual masking effect of a visual mask. We find that, similar to a visual mask, low-power optostimulation can significantly reduce visual detection sensitivity, that a sublinear interaction between visual and optogenetic evoked V1 responses could account for this perceptual effect, and that these neural and behavioral effects are spatially selective. Our toolkit and results open the door for further exploration of perceptual substitutions by direct stimulation of sensory cortex.

Data availability

The data and Matlab code for visualization are available on Dryad Digital Repository, doi:10.5061/dryad.00000003h.

The following data sets were generated

Article and author information

Author details

  1. Spencer Chin-Yu Chen

    Department of Neurosurgery, Rutgers University, New Brunswick, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Giacomo Benvenuti

    Center for Perceptual Systems, The University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5234-6260
  3. Yuzhi Chen

    Center for Perceptual Systems, The University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Satwant Kumar

    Center for Perceptual Systems, The University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Charu Ramakrishnan

    Department of Bioengineering, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Karl Deisseroth

    Department of Bioengineering, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Wilson S Geisler

    Center for Perceptual Systems, The University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Eyal Seidemann

    Center for Perceptual Systems, The University of Texas at Austin, Austin, United States
    For correspondence
    eyal@austin.utexas.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2841-5948

Funding

NIH Blueprint for Neuroscience Research (EY-016454)

  • Eyal Seidemann

NIH Blueprint for Neuroscience Research (EY-024662)

  • Wilson S Geisler

NIH Blueprint for Neuroscience Research (BRAIN U01-NS099720)

  • Wilson S Geisler
  • Eyal Seidemann

DARPA-NESD (N66001-17-C-4012)

  • Eyal Seidemann

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

Ethics

Animal experimentation: All procedures have been approved by the University of Texas Institutional Animal Care and Use Committee (IACUC protocol #AUP-2016-00274) and conform to NIH standards.

Copyright

© 2022, Chen 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.

Metrics

  • 1,512
    views
  • 218
    downloads
  • 8
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Spencer Chin-Yu Chen
  2. Giacomo Benvenuti
  3. Yuzhi Chen
  4. Satwant Kumar
  5. Charu Ramakrishnan
  6. Karl Deisseroth
  7. Wilson S Geisler
  8. Eyal Seidemann
(2022)
Similar neural and perceptual masking effects of low-power optogenetic stimulation in primate V1
eLife 11:e68393.
https://doi.org/10.7554/eLife.68393

Share this article

https://doi.org/10.7554/eLife.68393

Further reading

    1. Neuroscience
    Jacob A Miller
    Insight

    When navigating environments with changing rules, human brain circuits flexibly adapt how and where we retain information to help us achieve our immediate goals.

    1. Neuroscience
    Gáspár Oláh, Rajmund Lákovics ... Gábor Tamás
    Research Article

    Human-specific cognitive abilities depend on information processing in the cerebral cortex, where the neurons are significantly larger and their processes longer and sparser compared to rodents. We found that, in synaptically connected layer 2/3 pyramidal cells (L2/3 PCs), the delay in signal propagation from soma to soma is similar in humans and rodents. To compensate for the longer processes of neurons, membrane potential changes in human axons and/or dendrites must propagate faster. Axonal and dendritic recordings show that the propagation speed of action potentials (APs) is similar in human and rat axons, but the forward propagation of excitatory postsynaptic potentials (EPSPs) and the backward propagation of APs are 26 and 47% faster in human dendrites, respectively. Experimentally-based detailed biophysical models have shown that the key factor responsible for the accelerated EPSP propagation in human cortical dendrites is the large conductance load imposed at the soma by the large basal dendritic tree. Additionally, larger dendritic diameters and differences in cable and ion channel properties in humans contribute to enhanced signal propagation. Our integrative experimental and modeling study provides new insights into the scaling rules that help maintain information processing speed albeit the large and sparse neurons in the human cortex.