1. Neuroscience

Experience transforms crossmodal object representations in the anterior temporal lobes

  1. Aedan Yue Li  Is a corresponding author
  2. Natalia Ladyka-Wojcik
  3. Heba Qazilbash
  4. Ali Golestani
  5. Dirk B Walther
  6. Chris B Martin
  7. Morgan Barense
  1. University of Toronto, Canada
  2. University of Calgary, Canada
  3. Florida State University, United States
https://doi.org/10.7554/eLife.83382
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Cite this article
  1. Aedan Yue Li
  2. Natalia Ladyka-Wojcik
  3. Heba Qazilbash
  4. Ali Golestani
  5. Dirk B Walther
  6. Chris B Martin
  7. Morgan Barense
(2024)
Experience transforms crossmodal object representations in the anterior temporal lobes
eLife 13:e83382.
https://doi.org/10.7554/eLife.83382
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Abstract

Combining information from multiple senses is essential to object recognition, core to the ability to learn concepts, make new inferences, and generalize across distinct entities. Yet how the mind combines sensory input into coherent crossmodal representations - the crossmodal binding problem - remains poorly understood. Here, we applied multi-echo fMRI across a four-day paradigm, in which participants learned 3-dimensional crossmodal representations created from well-characterized unimodal visual shape and sound features. Our novel paradigm decoupled the learned crossmodal object representations from their baseline unimodal shapes and sounds, thus allowing us to track the emergence of crossmodal object representations as they were learned by healthy adults. Critically, we found that two anterior temporal lobe structures - temporal pole and perirhinal cortex - differentiated learned from non-learned crossmodal objects, even when controlling for the unimodal features that composed those objects. These results provide evidence for integrated crossmodal object representations in the anterior temporal lobes that were different from the representations for the unimodal features. Furthermore, we found that perirhinal cortex representations were by default biased towards visual shape, but this initial visual bias was attenuated by crossmodal learning. Thus, crossmodal learning transformed perirhinal representations such that they were no longer predominantly grounded in the visual modality, which may be a mechanism by which object concepts gain their abstraction.

Data availability

Anonymized data are available on the Open Science Framework: https://osf.io/vq4wj/.Univariate maps are available on NeuroVault: https://neurovault.org/collections/LFDCGMAY/

The following data sets were generated

Article and author information

Author details

  1. Aedan Yue Li

    Department of Psychology, University of Toronto, Toronto, Canada
    For correspondence
    aedanyue.li@utoronto.ca
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0580-4676

  2. Natalia Ladyka-Wojcik

    Department of Psychology, University of Toronto, Toronto, Canada
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1218-0080

  3. Heba Qazilbash

    Department of Psychology, University of Toronto, Toronto, Canada
    Competing interests
    No competing interests declared.

  4. Ali Golestani

    Department of Physics and Astronomy, University of Calgary, Toronto, Canada
    Competing interests
    No competing interests declared.

  5. Dirk B Walther

    Department of Psychology, University of Toronto, Toronto, Canada
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8585-9858

  6. Chris B Martin

    Department of Psychology, Florida State University, Tallahasse, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7014-4371

  7. Morgan Barense

    Department of Psychology, University of Toronto, Toronto, Canada
    Competing interests
    Morgan Barense, Reviewing editor, eLife.

Funding

Natural Sciences and Engineering Research Council of Canada (Alexander Graham Bell Canada Graduate Scholarship-Doctoral)

  • Aedan Yue Li

Natural Sciences and Engineering Research Council of Canada (Discovery Grant (RGPIN-2020-05747))

  • Morgan Barense

James S. McDonnell Foundation (Scholar Award)

  • Morgan Barense

Canada Research Chairs

  • Morgan Barense

Ontario Ministry of Research and Innovation (Early Researcher Award)

  • Morgan Barense

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

Reviewing Editor

  1. Marius V Peelen, Radboud University Nijmegen, Netherlands

Ethics

Human subjects: All experiments described in this study were approved by the University of Toronto Ethics Review Board: 37590. Informed consent was obtained for all participants in the study.

Version history

  1. Received: September 9, 2022
  2. Accepted: April 19, 2024
  3. Accepted Manuscript published: April 22, 2024 (version 1)
  4. Accepted Manuscript updated: April 23, 2024 (version 2)

Copyright

© 2024, Li 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. Aedan Yue Li
  2. Natalia Ladyka-Wojcik
  3. Heba Qazilbash
  4. Ali Golestani
  5. Dirk B Walther
  6. Chris B Martin
  7. Morgan Barense
(2024)
Experience transforms crossmodal object representations in the anterior temporal lobes
eLife 13:e83382.
https://doi.org/10.7554/eLife.83382

Share this article

https://doi.org/10.7554/eLife.83382

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