Experience transforms crossmodal object representations in the anterior temporal lobes
- University of Toronto, Canada
- University of Calgary, Canada
- Florida State University, United States
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/
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Crossmodal Object Representations Rely on Integrative CodingOpen Science Framework, https://doi.org/10.17605/OSF.IO/VQ4WJ.
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https://neurovault.org/collections/LFDCGMAY/NeuroVault, https://identifiers.org/neurovault.collection:12807.
Article and author information
Author details
Natalia Ladyka-Wojcik
Dirk Bernhardt-Walther
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
- 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
- Preprint posted: September 1, 2022 (view preprint)
- Received: September 9, 2022
- Accepted: April 19, 2024
- Accepted Manuscript published: April 22, 2024 (version 1)
- Accepted Manuscript updated: April 23, 2024 (version 2)
- Version of Record published: May 9, 2024 (version 3)
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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Experience transforms crossmodal object representations in the anterior temporal lobes
eLife 13:e83382.
https://doi.org/10.7554/eLife.83382
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