Parallel processing, hierarchical transformations, and sensorimotor associations along the 'where' pathway

  1. Raymond Doudlah
  2. Ting-Yu Chang
  3. Lowell W Thompson
  4. Byounghoon Kim
  5. Adhira Sunkara
  6. Ari Rosenberg  Is a corresponding author
  1. University of Wisconsin-Madison, United States
  2. WiSys Technology Foundation, United States

Abstract

Visually guided behaviors require the brain to transform ambiguous retinal images into object-level spatial representations and implement sensorimotor transformations. These processes are supported by the dorsal 'where' pathway. However, the specific functional contributions of areas along this pathway remain elusive due in part to methodological differences across studies. We previously showed that macaque caudal intraparietal (CIP) area neurons possess robust three-dimensional (3D) visual representations, carry choice- and saccade-related activity, and exhibit experience-dependent sensorimotor associations (Chang et al., 2020b). Here, we used a common experimental design to reveal parallel processing, hierarchical transformations, and the formation of sensorimotor associations along the 'where' pathway by extending the investigation to V3A, a major feedforward input to CIP. Higher-level 3D representations and choice-related activity were more prevalent in CIP than V3A. Both areas contained saccade-related activity that predicted the direction/timing of eye movements. Intriguingly, the time-course of saccade-related activity in CIP aligned with the temporally integrated V3A output. Sensorimotor associations between 3D orientation and saccade direction preferences were stronger in CIP than V3A, and moderated by choice signals in both areas. Together, the results explicate parallel representations, hierarchical transformations, and functional associations of visual and saccade-related signals at a key juncture in the 'where' pathway.

Data availability

All data generated or analyzed during this study are available through the Open Science Framework. https://osf.io/8wxk7/

Article and author information

Author details

  1. Raymond Doudlah

    Department of Neuroscience, University of Wisconsin-Madison, Madison, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3631-5947
  2. Ting-Yu Chang

    Department of Neuroscience, University of Wisconsin-Madison, Madison, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3964-0905
  3. Lowell W Thompson

    Department of Neuroscience, University of Wisconsin-Madison, Madison, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Byounghoon Kim

    Department of Neuroscience, University of Wisconsin-Madison, Madison, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7159-5134
  5. Adhira Sunkara

    WiSys Technology Foundation, Madison, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Ari Rosenberg

    Department of Neuroscience, University of Wisconsin-Madison, Madison, United States
    For correspondence
    ari.rosenberg@wisc.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8606-2987

Funding

National Institutes of Health (T32EY027721)

  • Raymond Doudlah

National Science Foundation (DGE-1545481)

  • Raymond Doudlah
  • Lowell W Thompson

National Institutes of Health (T32NS105602)

  • Lowell W Thompson

McPherson Eye Research Institute (Graduate Student Support Initiative)

  • Lowell W Thompson

Alfred P. Sloan Foundation (FG-2016-6468)

  • Ari Rosenberg

Whitehall Foundation (2016-08-18)

  • Ari Rosenberg

Greater Milwaukee Foundation (Shaw Scientist Award)

  • Ari Rosenberg

National Institutes of Health (EY029438)

  • Ari Rosenberg

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

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations of the National Institutes of Health's Guide for the Care and Use of Laboratory Animals. All experimental procedures and surgeries were approved by the Institutional Animal Care and Use Committee (IACUC) at the University of Wisconsin-Madison (Protocol #: G005229).

Reviewing Editor

  1. David J Freedman, The University of Chicago, United States

Publication history

  1. Received: March 22, 2022
  2. Preprint posted: March 23, 2022 (view preprint)
  3. Accepted: August 10, 2022
  4. Accepted Manuscript published: August 11, 2022 (version 1)
  5. Version of Record published: September 2, 2022 (version 2)

Copyright

© 2022, Doudlah 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. Raymond Doudlah
  2. Ting-Yu Chang
  3. Lowell W Thompson
  4. Byounghoon Kim
  5. Adhira Sunkara
  6. Ari Rosenberg
(2022)
Parallel processing, hierarchical transformations, and sensorimotor associations along the 'where' pathway
eLife 11:e78712.
https://doi.org/10.7554/eLife.78712

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