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
Share this article
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
  2. Download BibTeX
  3. Download .RIS

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.

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.

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.

Metrics

  • 755
    views
  • 141
    downloads
  • 0
    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. 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

Categories and tags

Research organism

Further reading

    1. Neuroscience

    Electrophysiological dynamics of salience, default mode, and frontoparietal networks during episodic memory formation and recall revealed through multi-experiment iEEG replication

    Anup Das, Vinod Menon
    Research Article

    Dynamic interactions between large-scale brain networks underpin human cognitive processes, but their electrophysiological mechanisms remain elusive. The triple network model, encompassing the salience network (SN), default mode network (DMN), and frontoparietal network (FPN), provides a framework for understanding these interactions. We analyzed intracranial electroencephalography (EEG) recordings from 177 participants across four diverse episodic memory experiments, each involving encoding as well as recall phases. Phase transfer entropy analysis revealed consistently higher directed information flow from the anterior insula (AI), a key SN node, to both DMN and FPN nodes. This directed influence was significantly stronger during memory tasks compared to resting state, highlighting the AI’s task-specific role in coordinating large-scale network interactions. This pattern persisted across externally driven memory encoding and internally governed free recall. Control analyses using the inferior frontal gyrus (IFG) showed an inverse pattern, with DMN and FPN exerting higher influence on IFG, underscoring the AI’s unique role. We observed task-specific suppression of high-gamma power in the posterior cingulate cortex/precuneus node of the DMN during memory encoding, but not recall. Crucially, these results were replicated across all four experiments spanning verbal and spatial memory domains with high Bayes replication factors. Our findings advance understanding of how coordinated neural network interactions support memory processes, highlighting the AI’s critical role in orchestrating large-scale brain network dynamics during both memory encoding and retrieval. By elucidating the electrophysiological basis of triple network interactions in episodic memory, our study provides insights into neural circuit dynamics underlying memory function and offer a framework for investigating network disruptions in memory-related disorders.

    1. Neuroscience

    Patch-walking, a coordinated multi-pipette patch clamp for efficiently finding synaptic connections

    Mighten C Yip, Mercedes M Gonzalez ... Craig R Forest
    Tools and Resources

    Significant technical challenges exist when measuring synaptic connections between neurons in living brain tissue. The patch clamping technique, when used to probe for synaptic connections, is manually laborious and time-consuming. To improve its efficiency, we pursued another approach: instead of retracting all patch clamping electrodes after each recording attempt, we cleaned just one of them and reused it to obtain another recording while maintaining the others. With one new patch clamp recording attempt, many new connections can be probed. By placing one pipette in front of the others in this way, one can ‘walk’ across the mouse brain slice, termed ‘patch-walking.’ We performed 136 patch clamp attempts for two pipettes, achieving 71 successful whole cell recordings (52.2%). Of these, we probed 29 pairs (i.e. 58 bidirectional probed connections) averaging 91 μm intersomatic distance, finding three connections. Patch-walking yields 80–92% more probed connections, for experiments with 10–100 cells than the traditional synaptic connection searching method.

    1. Neuroscience

    Brain state and cortical layer-specific mechanisms underlying perception at threshold

    Mitchell P Morton, Sachira Denagamage ... Anirvan S Nandy
    Research Article

    Identical stimuli can be perceived or go unnoticed across successive presentations, producing divergent behavioral outcomes despite similarities in sensory input. We sought to understand how fluctuations in behavioral state and cortical layer and cell class-specific neural activity underlie this perceptual variability. We analyzed physiological measurements of state and laminar electrophysiological activity in visual area V4 while monkeys were rewarded for correctly reporting a stimulus change at perceptual threshold. Hit trials were characterized by a behavioral state with heightened arousal, greater eye position stability, and enhanced decoding performance of stimulus identity from neural activity. Target stimuli evoked stronger responses in V4 in hit trials, and excitatory neurons in the superficial layers, the primary feed-forward output of the cortical column, exhibited lower variability. Feed-forward interlaminar population correlations were stronger on hits. Hit trials were further characterized by greater synchrony between the output layers of the cortex during spontaneous activity, while the stimulus-evoked period showed elevated synchrony in the feed-forward pathway. Taken together, these results suggest that a state of elevated arousal and stable retinal images allow enhanced processing of sensory stimuli, which contributes to hits at perceptual threshold.