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 Bernhardt-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 Bernhardt-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 Bernhardt-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

  • 814
    views
  • 150
    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 Bernhardt-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

    Post-retrieval noradrenergic activation impairs subsequent memory depending on cortico-hippocampal reactivation

    Hendrik Heinbockel, Gregor Leicht ... Lars Schwabe
    Research Article

    When retrieved, seemingly stable memories can become sensitive to significant events, such as acute stress. The mechanisms underlying these memory dynamics remain poorly understood. Here, we show that noradrenergic stimulation after memory retrieval impairs subsequent remembering, depending on hippocampal and cortical signals emerging during retrieval. In a three-day study, we measured brain activity using fMRI during initial encoding, 24 hr-delayed memory cueing followed by pharmacological elevations of glucocorticoid or noradrenergic activity, and final recall. While post-retrieval glucocorticoids did not affect subsequent memory, the impairing effect of noradrenergic arousal on final recall depended on hippocampal reactivation and category-level reinstatement in the ventral temporal cortex during memory cueing. These effects did not require a reactivation of the original memory trace and did not interact with offline reinstatement during rest. Our findings demonstrate that, depending on the retrieval-related neural reactivation of memories, noradrenergic arousal after retrieval can alter the future accessibility of consolidated memories.

    1. Neuroscience

    Nutritional state-dependent modulation of insulin-producing cells in Drosophila

    Rituja S Bisen, Fathima Mukthar Iqbal ... Jan M Ache
    Research Article

    Insulin plays a key role in metabolic homeostasis. Drosophila insulin-producing cells (IPCs) are functional analogues of mammalian pancreatic beta cells and release insulin directly into circulation. To investigate the in vivo dynamics of IPC activity, we quantified the effects of nutritional and internal state changes on IPCs using electrophysiological recordings. We found that the nutritional state strongly modulates IPC activity. IPC activity decreased with increasing periods of starvation. Refeeding flies with glucose or fructose, two nutritive sugars, significantly increased IPC activity, whereas non-nutritive sugars had no effect. In contrast to feeding, glucose perfusion did not affect IPC activity. This was reminiscent of the mammalian incretin effect, where glucose ingestion drives higher insulin release than intravenous application. Contrary to IPCs, Diuretic hormone 44-expressing neurons in the pars intercerebralis (DH44PINs) responded to glucose perfusion. Functional connectivity experiments demonstrated that these DH44PINs do not affect IPC activity, while other DH44Ns inhibit them. Hence, populations of autonomously and systemically sugar-sensing neurons work in parallel to maintain metabolic homeostasis. Accordingly, activating IPCs had a small, satiety-like effect on food-searching behavior and reduced starvation-induced hyperactivity, whereas activating DH44Ns strongly increased hyperactivity. Taken together, we demonstrate that IPCs and DH44Ns are an integral part of a modulatory network that orchestrates glucose homeostasis and adaptive behavior in response to shifts in the metabolic state.

    1. Neuroscience

    Driver lines for studying associative learning in Drosophila

    Yichun Shuai, Megan Sammons ... Yoshinori Aso
    Tools and Resources

    The mushroom body (MB) is the center for associative learning in insects. In Drosophila, intersectional split-GAL4 drivers and electron microscopy (EM) connectomes have laid the foundation for precise interrogation of the MB neural circuits. However, investigation of many cell types upstream and downstream of the MB has been hindered due to lack of specific driver lines. Here we describe a new collection of over 800 split-GAL4 and split-LexA drivers that cover approximately 300 cell types, including sugar sensory neurons, putative nociceptive ascending neurons, olfactory and thermo-/hygro-sensory projection neurons, interneurons connected with the MB-extrinsic neurons, and various other cell types. We characterized activation phenotypes for a subset of these lines and identified a sugar sensory neuron line most suitable for reward substitution. Leveraging the thousands of confocal microscopy images associated with the collection, we analyzed neuronal morphological stereotypy and discovered that one set of mushroom body output neurons, MBON08/MBON09, exhibits striking individuality and asymmetry across animals. In conjunction with the EM connectome maps, the driver lines reported here offer a powerful resource for functional dissection of neural circuits for associative learning in adult Drosophila.