Decoding hierarchical control of sequential behavior in oscillatory EEG activity

  1. Atsushi Kikumoto
  2. Ulrich Mayr  Is a corresponding author
  1. University of Oregon, United States

Abstract

Despite strong theoretical reasons for assuming that abstract representations organize complex action sequences in terms of subplans (chunks) and sequential positions, we lack methods to directly track such content-independent, hierarchical representations in humans. We applied time-resolved, multivariate decoding analysis to the pattern of rhythmic EEG activity that was registered while participants planned and executed individual elements from pre-learned, structured sequences. Across three experiments, the theta and alpha-band activity coded basic elements and abstract control representations, in particular the ordinal position of basic elements, but also the identity and position of chunks. Further, a robust representation of higher-level, chunk identity information was only found in individuals with above-median working memory capacity, potentially providing a neural-level explanation for working-memory differences in sequential performance. Our results suggest that by decoding oscillatory activity we can track how the cognitive system traverses through the states of a hierarchical control structure.

Data availability

All data and analysis scripts have been deposited at OSF (https://osf.io/6hmrz/).

The following data sets were generated

Article and author information

Author details

  1. Atsushi Kikumoto

    Department of Psychology, University of Oregon, Eugene, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Ulrich Mayr

    Department of Psychology, University of Oregon, Eugene, United States
    For correspondence
    mayr@uoregon.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7512-4556

Funding

National Science Foundation (1734264)

  • Ulrich Mayr

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

Ethics

Human subjects: We obtained informed consent from human subjects. Consent and study procedures were approved by the University of Oregon's Human Subjects Institutional Review Board (Protocol 10272010.016).

Reviewing Editor

  1. David Badre, Brown University, United States

Publication history

  1. Received: May 22, 2018
  2. Accepted: November 8, 2018
  3. Accepted Manuscript published: November 14, 2018 (version 1)
  4. Version of Record published: November 27, 2018 (version 2)

Copyright

© 2018, Kikumoto & Mayr

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

  • 2,872
    Page views
  • 422
    Downloads
  • 7
    Citations

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

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. Atsushi Kikumoto
  2. Ulrich Mayr
(2018)
Decoding hierarchical control of sequential behavior in oscillatory EEG activity
eLife 7:e38550.
https://doi.org/10.7554/eLife.38550

Further reading

    1. Neuroscience
    Orie T Shafer et al.
    Research Article Updated

    The circadian clock orchestrates daily changes in physiology and behavior to ensure internal temporal order and optimal timing across the day. In animals, a central brain clock coordinates circadian rhythms throughout the body and is characterized by a remarkable robustness that depends on synaptic connections between constituent neurons. The clock neuron network of Drosophila, which shares network motifs with clock networks in the mammalian brain yet is built of many fewer neurons, offers a powerful model for understanding the network properties of circadian timekeeping. Here, we report an assessment of synaptic connectivity within a clock network, focusing on the critical lateral neuron (LN) clock neuron classes within the Janelia hemibrain dataset. Our results reveal that previously identified anatomical and functional subclasses of LNs represent distinct connectomic types. Moreover, we identify a small number of non-clock cell subtypes representing highly synaptically coupled nodes within the clock neuron network. This suggests that neurons lacking molecular timekeeping likely play integral roles within the circadian timekeeping network. To our knowledge, this represents the first comprehensive connectomic analysis of a circadian neuronal network.

    1. Neuroscience
    Ling Bai et al.
    Research Article Updated

    Animals must learn through experience which foods are nutritious and should be consumed, and which are toxic and should be avoided. Enteroendocrine cells (EECs) are the principal chemosensors in the GI tract, but investigation of their role in behavior has been limited by the difficulty of selectively targeting these cells in vivo. Here, we describe an intersectional genetic approach for manipulating EEC subtypes in behaving mice. We show that multiple EEC subtypes inhibit food intake but have different effects on learning. Conditioned flavor preference is driven by release of cholecystokinin whereas conditioned taste aversion is mediated by serotonin and substance P. These positive and negative valence signals are transmitted by vagal and spinal afferents, respectively. These findings establish a cellular basis for how chemosensing in the gut drives learning about food.