1. Neuroscience
Download icon

Resolving multisensory and attentional influences across cortical depth in sensory cortices

  1. Remi Gau  Is a corresponding author
  2. Pierre-Louis Bazin
  3. Robert Trampel
  4. Robert Turner
  5. Uta Noppeney
  1. University of Birmingham, United Kingdom
  2. Max Planck Institute for Human Cognitive and Brain Sciences, Germany
Research Article
  • Cited 10
  • Views 2,551
  • Annotations
Cite this article as: eLife 2020;9:e46856 doi: 10.7554/eLife.46856

Abstract

In our environment our senses are bombarded with a myriad of signals, only a subset of which is relevant for our goals. Using sub-millimeter-resolution fMRI at 7T we resolved BOLD-response and activation patterns across cortical depth in early sensory cortices to auditory, visual and audiovisual stimuli under auditory or visual attention. In visual cortices, auditory stimulation induced widespread inhibition irrespective of attention, whereas auditory relative to visual attention suppressed mainly central visual field representations. In auditory cortices, visual stimulation suppressed activations, but amplified responses to concurrent auditory stimuli, in a patchy topography. Critically, multisensory interactions in auditory cortices were stronger in deeper laminae, while attentional influences were greatest at the surface. These distinct depth-dependent profiles suggest that multisensory and attentional mechanisms regulate sensory processing via partly distinct circuitries. Our findings are crucial for understanding how the brain regulates information flow across senses to interact with our complex multisensory world.

Article and author information

Author details

  1. Remi Gau

    Computational Neuroscience and Cognitive Robotics Centre, University of Birmingham, Birmingham, United Kingdom
    For correspondence
    remi_gau@hotmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1535-9767
  2. Pierre-Louis Bazin

    Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Robert Trampel

    Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Robert Turner

    Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Uta Noppeney

    Computational Neuroscience and Cognitive Robotics Centre, University of Birmingham, Birmingham, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.

Funding

European Research Council (Mult-sens)

  • Uta Noppeney

Max Planck Society

  • Robert Turner

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 procedures were approved by the Ethics Committee of the University of Leipzig under the protocol number 273-14: "Magnetresonanz-Untersuchungen am Menschen bei 7 Tesla". Participants gave written informed consent to participate in this fMRI study.

Reviewing Editor

  1. Floris P de Lange, Radboud University, Netherlands

Publication history

  1. Received: March 14, 2019
  2. Accepted: January 7, 2020
  3. Accepted Manuscript published: January 8, 2020 (version 1)
  4. Version of Record published: January 27, 2020 (version 2)

Copyright

© 2020, Gau 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

  • 2,551
    Page views
  • 431
    Downloads
  • 10
    Citations

Article citation count generated by polling the highest count across the following sources: Scopus, Crossref, PubMed Central.

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)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Further reading

    1. Neuroscience
    Daniela Saderi et al.
    Research Article Updated

    Both generalized arousal and engagement in a specific task influence sensory neural processing. To isolate effects of these state variables in the auditory system, we recorded single-unit activity from primary auditory cortex (A1) and inferior colliculus (IC) of ferrets during a tone detection task, while monitoring arousal via changes in pupil size. We used a generalized linear model to assess the influence of task engagement and pupil size on sound-evoked activity. In both areas, these two variables affected independent neural populations. Pupil size effects were more prominent in IC, while pupil and task engagement effects were equally likely in A1. Task engagement was correlated with larger pupil; thus, some apparent effects of task engagement should in fact be attributed to fluctuations in pupil size. These results indicate a hierarchy of auditory processing, where generalized arousal enhances activity in midbrain, and effects specific to task engagement become more prominent in cortex.

    1. Neuroscience
    Pratish Thakore et al.
    Research Article

    Cerebral blood flow is dynamically regulated by neurovascular coupling to meet the dynamic metabolic demands of the brain. We hypothesized that TRPA1 channels in capillary endothelial cells are stimulated by neuronal activity and instigate a propagating retrograde signal that dilates upstream parenchymal arterioles to initiate functional hyperemia. We find that activation of TRPA1 in capillary beds and post-arteriole transitional segments with mural cell coverage initiates retrograde signals that dilate upstream arterioles. These signals exhibit a unique mode of biphasic propagation. Slow, short-range intercellular Ca2+ signals in the capillary network are converted to rapid electrical signals in transitional segments that propagate to and dilate upstream arterioles. We further demonstrate that TRPA1 is necessary for functional hyperemia and neurovascular coupling within the somatosensory cortex of mice in vivo. These data establish endothelial cell TRPA1 channels as neuronal activity sensors that initiate microvascular vasodilatory responses to redirect blood to regions of metabolic demand.