Shared and modality-specific brain regions that mediate auditory and visual word comprehension

  1. Anne Keitel  Is a corresponding author
  2. Joachim Gross
  3. Christoph Kayser
  1. University of Dundee, United Kingdom
  2. University of Muenster, Germany
  3. Bielefeld University, Germany

Abstract

Visual speech carried by lip movements is an integral part of communication. Yet, it remains unclear in how far visual and acoustic speech comprehension are mediated by the same brain regions. Using multivariate classification of full-brain MEG data, we first probed where the brain represents acoustically and visually conveyed word identities. We then tested where these sensory-driven representations are predictive of participants' trial-wise comprehension. The comprehension-relevant representations of auditory and visual speech converged only in anterior angular and inferior frontal regions and were spatially dissociated from those representations that best reflected the sensory-driven word identity. These results provide a neural explanation for the behavioural dissociation of acoustic and visual speech comprehension and suggest that cerebral representations encoding word identities may be more modality-specific than often upheld.

Data availability

All relevant data and stimuli lists have been deposited to Dryad, under the DOI:10.5061/dryad.zkh18937w.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Anne Keitel

    Psychology, University of Dundee, Dundee, United Kingdom
    For correspondence
    a.keitel@dundee.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4498-0146
  2. Joachim Gross

    Institute for Biomagnetism and Biosignalanalysis, University of Muenster, Muenster, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Christoph Kayser

    Department for Cognitive Neuroscience, Faculty of Biology, Bielefeld University, Bielefeld, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7362-5704

Funding

Biotechnology and Biological Sciences Research Council (BB/L027534/1)

  • Joachim Gross
  • Christoph Kayser

H2020 European Research Council (ERC-2014-CoG; grant No 646657)

  • Christoph Kayser

Wellcome (Joint Senior Investigator Grant,No 098433)

  • Joachim Gross

Deutsche Forschungsgemeinschaft (GR 2024/5-1)

  • Joachim Gross

IZKF (Gro3/001/19)

  • Joachim Gross

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 participants provided written informed consent prior to testing and received monetary compensation of £10/h. The experiment was approved by the ethics committee of the College of Science and Engineering, University of Glasgow (approval number 300140078), and conducted in compliance with the Declaration of Helsinki.

Copyright

© 2020, Keitel 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

  • 1,829
    views
  • 274
    downloads
  • 14
    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. Anne Keitel
  2. Joachim Gross
  3. Christoph Kayser
(2020)
Shared and modality-specific brain regions that mediate auditory and visual word comprehension
eLife 9:e56972.
https://doi.org/10.7554/eLife.56972

Share this article

https://doi.org/10.7554/eLife.56972

Further reading

    1. Computational and Systems Biology
    2. Neuroscience
    Sebastian Quiroz Monnens, Casper Peters ... Bernhard Englitz
    Research Advance

    Animal behaviour alternates between stochastic exploration and goal-directed actions, which are generated by the underlying neural dynamics. Previously, we demonstrated that the compositional Restricted Boltzmann Machine (cRBM) can decompose whole-brain activity of larval zebrafish data at the neural level into a small number (∼100-200) of assemblies that can account for the stochasticity of the neural activity (van der Plas et al., eLife, 2023). Here, we advance this representation by extending to a combined stochastic-dynamical representation to account for both aspects using the recurrent temporal RBM (RTRBM) and transfer-learning based on the cRBM estimate. We demonstrate that the functional advantage of the RTRBM is captured in the temporal weights on the hidden units, representing neural assemblies, for both simulated and experimental data. Our results show that the temporal expansion outperforms the stochastic-only cRBM in terms of generalization error and achieves a more accurate representation of the moments in time. Lastly, we demonstrate that we can identify the original time-scale of assembly dynamics by estimating multiple RTRBMs at different temporal resolutions. Together, we propose that RTRBMs are a valuable tool for capturing the combined stochastic and time-predictive dynamics of large-scale data sets.

    1. Computational and Systems Biology
    2. Physics of Living Systems
    Ju Kang, Shijie Zhang ... Xin Wang
    Research Article

    Explaining biodiversity is a fundamental issue in ecology. A long-standing puzzle lies in the paradox of the plankton: many species of plankton feeding on a limited variety of resources coexist, apparently flouting the competitive exclusion principle (CEP), which holds that the number of predator (consumer) species cannot exceed that of the resources at a steady state. Here, we present a mechanistic model and demonstrate that intraspecific interference among the consumers enables a plethora of consumer species to coexist at constant population densities with only one or a handful of resource species. This facilitated biodiversity is resistant to stochasticity, either with the stochastic simulation algorithm or individual-based modeling. Our model naturally explains the classical experiments that invalidate the CEP, quantitatively illustrates the universal S-shaped pattern of the rank-abundance curves across a wide range of ecological communities, and can be broadly used to resolve the mystery of biodiversity in many natural ecosystems.