1. Neuroscience
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Specialized contributions of mid-tier stages of dorsal and ventral pathways to stereoscopic processing in macaque

  1. Toshihide W Yoshioka
  2. Takahiro Doi  Is a corresponding author
  3. Mohammad Abdolrahmani
  4. Ichiro Fujita  Is a corresponding author
  1. Osaka University, Japan
  2. University of Pennsylvania, United States
  3. RIKEN Center for Brain Science (CBS), Japan
Research Article
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Cite this article as: eLife 2021;10:e58749 doi: 10.7554/eLife.58749

Abstract

The division of labor between the dorsal and ventral visual pathways has been well studied, but not often with direct comparison at the single-neuron resolution with matched stimuli. Here we directly compared how single neurons in MT and V4, mid-tier areas of the two pathways, process binocular disparity, a powerful cue for 3D perception and actions. We found that MT neurons transmitted disparity signals more quickly and robustly, whereas V4 or its upstream neurons transformed the signals into sophisticated representations more prominently. Therefore, signaling speed and robustness were traded for transformation between the dorsal and ventral pathways. The key factor in this tradeoff was disparity-tuning shape: V4 neurons had more even-symmetric tuning than MT neurons. Moreover, the tuning symmetry predicted the degree of signal transformation across neurons similarly within each area, implying a general role of tuning symmetry in the stereoscopic processing by the two pathways.

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Source data files have been provided for all data figures.

Article and author information

Author details

  1. Toshihide W Yoshioka

    Graduate School of Frontier Biosciences, Osaka University, Suita, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6475-4627
  2. Takahiro Doi

    Departments of Neuroscience and Psychology, University of Pennsylvania, Philadelphia, United States
    For correspondence
    doi.takah@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9650-972X
  3. Mohammad Abdolrahmani

    Laboratory for Neural Circuits and Behavior, RIKEN Center for Brain Science (CBS), Wako, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3658-2623
  4. Ichiro Fujita

    Graduate School of Frontier Biosciences, Osaka University, Suita, Japan
    For correspondence
    fujita@fbs.osaka-u.ac.jp
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3293-8610

Funding

Ministry of Education, Culture, Sports, Science and Technology (2324007)

  • Ichiro Fujita

Ministry of Education, Culture, Sports, Science and Technology (15H01437)

  • Ichiro Fujita

Ministry of Education, Culture, Sports, Science and Technology (17H01381)

  • Ichiro Fujita

Ministry of Education, Culture, Sports, Science and Technology (18H05007)

  • Ichiro Fujita

Ministry of Internal Affairs and Communications

  • Ichiro Fujita

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 experimental procedures in this study were approved by the Animal Experiment Committee (Permit Numbers: FBS-12-016, FBS-13-003-1) of Osaka University, and conformed to the Guide for the Care and Use of Laboratory Animals issued by the National Institutes of Health, USA.

Reviewing Editor

  1. Anna Wang Roe, Zhejiang University, China

Publication history

  1. Received: May 9, 2020
  2. Accepted: February 18, 2021
  3. Accepted Manuscript published: February 24, 2021 (version 1)
  4. Version of Record published: March 15, 2021 (version 2)

Copyright

© 2021, Yoshioka 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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