1. Neuroscience

Modality-specific tracking of attention and sensory statistics in the human electrophysiological spectral exponent

  1. Leonhard Waschke  Is a corresponding author
  2. Thomas Donoghue
  3. Lorenz Fiedler
  4. Sydney Smith
  5. Douglas D Garrett
  6. Bradley Voytek
  7. Jonas Obleser
  1. MPI for Human Development, Germany
  2. University of California, San Diego, United States
  3. Eriksholm Research Centre, Oticon A/S, Denmark
  4. Max Planck Institute for Human Development, Germany
  5. University of Lübeck, Germany
https://doi.org/10.7554/eLife.70068
Share this article
Cite this article
  1. Leonhard Waschke
  2. Thomas Donoghue
  3. Lorenz Fiedler
  4. Sydney Smith
  5. Douglas D Garrett
  6. Bradley Voytek
  7. Jonas Obleser
(2021)
Modality-specific tracking of attention and sensory statistics in the human electrophysiological spectral exponent
eLife 10:e70068.
https://doi.org/10.7554/eLife.70068
  2. Download BibTeX
  3. Download .RIS

Abstract

A hallmark of electrophysiological brain activity is its 1/f-like spectrum - power decreases with increasing frequency. The steepness of this 'roll-off' is approximated by the spectral exponent, which in invasively recorded neural populations reflects the balance of excitatory to inhibitory neural activity (E:I balance). Here, we first establish that the spectral exponent of non-invasive electroencephalography (EEG) recordings is highly sensitive to general (i.e., anaesthesia-driven) changes in E:I balance. Building on the EEG spectral exponent as a viable marker of E:I, we then demonstrate its sensitivity to the focus of selective attention in an EEG experiment during which participants detected targets in simultaneous audio-visual noise. In addition to these endogenous changes in E:I balance, EEG spectral exponents over auditory and visual sensory cortices also tracked auditory and visual stimulus spectral exponents, respectively. Individuals' degree of this selective stimulus-brain coupling in spectral exponents predicted behavioural performance. Our results highlight the rich information contained in 1/f-like neural activity, providing a window into diverse neural processes previously thought to be inaccessible in non-invasive human recordings.

Data availability

Data and code have been deposited on OSF (https://osf.io/wyzrg/).

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

Article and author information

Author details

  1. Leonhard Waschke

    MPI for Human Development, Berlin, Germany
    For correspondence
    waschke@mpib-berlin.mpg.de
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1248-9259

  2. Thomas Donoghue

    University of California, San Diego, San Diego, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5911-0472

  3. Lorenz Fiedler

    Eriksholm Research Centre, Oticon A/S, Snekkersten,, Denmark
    Competing interests
    No competing interests declared.

  4. Sydney Smith

    University of California, San Diego, San Diego, United States
    Competing interests
    No competing interests declared.

  5. Douglas D Garrett

    Max Planck UCL Centre for Computational Psychiatry and Ageing Research, Max Planck Institute for Human Development, Berlin, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0629-7672

  6. Bradley Voytek

    Cognitive Science, University of California, San Diego, La Jolla, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1640-2525

  7. Jonas Obleser

    Department of Psychology, University of Lübeck, Lübeck, Germany
    Competing interests
    Jonas Obleser, Reviewing Editor for eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7619-0459

Funding

Deutsche Forschungsgemeinschaft (Emmy Noether Programme)

  • Leonhard Waschke
  • Douglas D Garrett

H2020 European Research Council (ERC-CoG-2014-646696)

  • Jonas Obleser

Max Planck UCL Centre for Computational Psychiatry and Ageing Research

  • Leonhard Waschke
  • Douglas D Garrett

Whitehall Foundation (2017-12-73)

  • Bradley Voytek

National Science Foundation (BCS-1736028)

  • Bradley Voytek

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Maria Chait, University College London, United Kingdom

Ethics

Human subjects: All participants gave written informed consent, reported normalhearing and had normal or corrected to normal vision. All experimental procedures wereapproved by the institutional review board of the University of California, San Diego, Human Research Protections Program (UCSD IRB Protocol #150834. ).

Version history

  1. Preprint posted: January 14, 2021 (view preprint)
  2. Received: May 5, 2021
  3. Accepted: October 18, 2021
  4. Accepted Manuscript published: October 21, 2021 (version 1)
  5. Version of Record published: November 11, 2021 (version 2)

Copyright

© 2021, Waschke 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

  • 3,087
    views
  • 420
    downloads
  • 101
    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. Leonhard Waschke
  2. Thomas Donoghue
  3. Lorenz Fiedler
  4. Sydney Smith
  5. Douglas D Garrett
  6. Bradley Voytek
  7. Jonas Obleser
(2021)
Modality-specific tracking of attention and sensory statistics in the human electrophysiological spectral exponent
eLife 10:e70068.
https://doi.org/10.7554/eLife.70068

Share this article

https://doi.org/10.7554/eLife.70068

Categories and tags

Research organism

Further reading

    1. Neuroscience

    Determinantal point process attention over grid cell code supports out of distribution generalization

    Shanka Subhra Mondal, Steven Frankland ... Jonathan D Cohen
    Research Article

    Deep neural networks have made tremendous gains in emulating human-like intelligence, and have been used increasingly as ways of understanding how the brain may solve the complex computational problems on which this relies. However, these still fall short of, and therefore fail to provide insight into how the brain supports strong forms of generalization of which humans are capable. One such case is out-of-distribution (OOD) generalization – successful performance on test examples that lie outside the distribution of the training set. Here, we identify properties of processing in the brain that may contribute to this ability. We describe a two-part algorithm that draws on specific features of neural computation to achieve OOD generalization, and provide a proof of concept by evaluating performance on two challenging cognitive tasks. First we draw on the fact that the mammalian brain represents metric spaces using grid cell code (e.g., in the entorhinal cortex): abstract representations of relational structure, organized in recurring motifs that cover the representational space. Second, we propose an attentional mechanism that operates over the grid cell code using determinantal point process (DPP), that we call DPP attention (DPP-A) – a transformation that ensures maximum sparseness in the coverage of that space. We show that a loss function that combines standard task-optimized error with DPP-A can exploit the recurring motifs in the grid cell code, and can be integrated with common architectures to achieve strong OOD generalization performance on analogy and arithmetic tasks. This provides both an interpretation of how the grid cell code in the mammalian brain may contribute to generalization performance, and at the same time a potential means for improving such capabilities in artificial neural networks.

    1. Neuroscience

    Bidirectional fear modulation by discrete anterior insular circuits in male mice

    Sanggeon Park, Yeowool Huh ... Jeiwon Cho
    Research Article

    The brain’s ability to appraise threats and execute appropriate defensive responses is essential for survival in a dynamic environment. Humans studies have implicated the anterior insular cortex (aIC) in subjective fear regulation and its abnormal activity in fear/anxiety disorders. However, the complex aIC connectivity patterns involved in regulating fear remain under investigated. To address this, we recorded single units in the aIC of freely moving male mice that had previously undergone auditory fear conditioning, assessed the effect of optogenetically activating specific aIC output structures in fear, and examined the organization of aIC neurons projecting to the specific structures with retrograde tracing. Single-unit recordings revealed that a balanced number of aIC pyramidal neurons’ activity either positively or negatively correlated with a conditioned tone-induced freezing (fear) response. Optogenetic manipulations of aIC pyramidal neuronal activity during conditioned tone presentation altered the expression of conditioned freezing. Neural tracing showed that non-overlapping populations of aIC neurons project to the amygdala or the medial thalamus, and the pathway bidirectionally modulated conditioned fear. Specifically, optogenetic stimulation of the aIC-amygdala pathway increased conditioned freezing, while optogenetic stimulation of the aIC-medial thalamus pathway decreased it. Our findings suggest that the balance of freezing-excited and freezing-inhibited neuronal activity in the aIC and the distinct efferent circuits interact collectively to modulate fear behavior.

    1. Neuroscience

    Fundamental processes in sensorimotor learning: Reasoning, refinement, and retrieval

    Jonathan S Tsay, Hyosub E Kim ... Richard B Ivry
    Review Article

    Motor learning is often viewed as a unitary process that operates outside of conscious awareness. This perspective has led to the development of sophisticated models designed to elucidate the mechanisms of implicit sensorimotor learning. In this review, we argue for a broader perspective, emphasizing the contribution of explicit strategies to sensorimotor learning tasks. Furthermore, we propose a theoretical framework for motor learning that consists of three fundamental processes: reasoning, the process of understanding action–outcome relationships; refinement, the process of optimizing sensorimotor and cognitive parameters to achieve motor goals; and retrieval, the process of inferring the context and recalling a control policy. We anticipate that this ‘3R’ framework for understanding how complex movements are learned will open exciting avenues for future research at the intersection between cognition and action.