Theta oscillations locked to intended actions rhythmically modulate perception

  1. Alice Tomassini  Is a corresponding author
  2. Luca Ambrogioni
  3. W Pieter Medendorp
  4. Eric Maris  Is a corresponding author
  1. Radboud University Nijmegen, Netherlands
  2. Radboud University, Netherlands

Abstract

Ongoing brain oscillations are known to influence perception, and to be reset by exogenous stimulations. Voluntary action is also accompanied by prominent rhythmic activity, and recent behavioral evidence suggests that this might be coupled with perception. Here, we reveal the neurophysiological underpinnings of this sensorimotor coupling in humans. We link the trial-by-trial dynamics of EEG oscillatory activity during movement preparation to the corresponding dynamics in perception, for two unrelated visual and motor tasks. The phase of theta oscillations (~4 Hz) predicts perceptual performance, even >1 s before movement. Moreover, theta oscillations are phase-locked to the onset of the movement. Remarkably, the alignment of theta phase and its perceptual relevance unfold with similar non-monotonic profiles, suggesting their relatedness. The present work shows that perception and movement initiation are automatically synchronized since the early stages of motor planning through neuronal oscillatory activity in the theta range.

Article and author information

Author details

  1. Alice Tomassini

    Donders Institute for Brain, Cognition and Behavior, Centre for Cognition (DCC), Radboud University Nijmegen, Nijmegen, Netherlands
    For correspondence
    a.tomassini@donders.ru.nl
    Competing interests
    The authors declare that no competing interests exist.
  2. Luca Ambrogioni

    Donders Institute for Brain, Cognition and Behavior, Centre for Cognition (DCC), Radboud University Nijmegen, Nijmegen, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  3. W Pieter Medendorp

    Donders Institute for Brain, Cognition and Behavior, Centre for Cognition (DCC), Radboud University, Nijmegen, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9615-4220
  4. Eric Maris

    Donders Institute for Brain, Cognition and Behavior, Centre for Cognition (DCC), Radboud University, Nijmegen, Netherlands
    For correspondence
    e.maris@donders.ru.nl
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5166-1800

Funding

European Research Council (EU-ERC-238-567)

  • W Pieter Medendorp

Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO-VICI: 453-11-00)

  • W Pieter Medendorp

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

Reviewing Editor

  1. Benjamin Morillon, Aix-Marseille University, France

Ethics

Human subjects: The study and experimental procedures were approved by the local Ethical Review Board (Ethics Committee of the Faculty of Social Sciences, Radboud University, The Netherlands). Participants provided written, informed consent after explanation of the task and experimental procedures, in accordance with the guidelines of the local Ethical Review Board.

Version history

  1. Received: January 31, 2017
  2. Accepted: July 6, 2017
  3. Accepted Manuscript published: July 7, 2017 (version 1)
  4. Version of Record published: August 11, 2017 (version 2)

Copyright

© 2017, Tomassini 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

  • 3,231
    views
  • 576
    downloads
  • 71
    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. Alice Tomassini
  2. Luca Ambrogioni
  3. W Pieter Medendorp
  4. Eric Maris
(2017)
Theta oscillations locked to intended actions rhythmically modulate perception
eLife 6:e25618.
https://doi.org/10.7554/eLife.25618

Share this article

https://doi.org/10.7554/eLife.25618

Further reading

    1. Genetics and Genomics
    2. Neuroscience
    Bohan Zhu, Richard I Ainsworth ... Javier González-Maeso
    Research Article

    Genome-wide association studies have revealed >270 loci associated with schizophrenia risk, yet these genetic factors do not seem to be sufficient to fully explain the molecular determinants behind this psychiatric condition. Epigenetic marks such as post-translational histone modifications remain largely plastic during development and adulthood, allowing a dynamic impact of environmental factors, including antipsychotic medications, on access to genes and regulatory elements. However, few studies so far have profiled cell-specific genome-wide histone modifications in postmortem brain samples from schizophrenia subjects, or the effect of antipsychotic treatment on such epigenetic marks. Here, we conducted ChIP-seq analyses focusing on histone marks indicative of active enhancers (H3K27ac) and active promoters (H3K4me3), alongside RNA-seq, using frontal cortex samples from antipsychotic-free (AF) and antipsychotic-treated (AT) individuals with schizophrenia, as well as individually matched controls (n=58). Schizophrenia subjects exhibited thousands of neuronal and non-neuronal epigenetic differences at regions that included several susceptibility genetic loci, such as NRG1, DISC1, and DRD3. By analyzing the AF and AT cohorts separately, we identified schizophrenia-associated alterations in specific transcription factors, their regulatees, and epigenomic and transcriptomic features that were reversed by antipsychotic treatment; as well as those that represented a consequence of antipsychotic medication rather than a hallmark of schizophrenia in postmortem human brain samples. Notably, we also found that the effect of age on epigenomic landscapes was more pronounced in frontal cortex of AT-schizophrenics, as compared to AF-schizophrenics and controls. Together, these data provide important evidence of epigenetic alterations in the frontal cortex of individuals with schizophrenia, and remark for the first time on the impact of age and antipsychotic treatment on chromatin organization.

    1. Neuroscience
    Katharina Eichler, Stefanie Hampel ... Andrew M Seeds
    Research Advance

    Mechanosensory neurons located across the body surface respond to tactile stimuli and elicit diverse behavioral responses, from relatively simple stimulus location-aimed movements to complex movement sequences. How mechanosensory neurons and their postsynaptic circuits influence such diverse behaviors remains unclear. We previously discovered that Drosophila perform a body location-prioritized grooming sequence when mechanosensory neurons at different locations on the head and body are simultaneously stimulated by dust (Hampel et al., 2017; Seeds et al., 2014). Here, we identify nearly all mechanosensory neurons on the Drosophila head that individually elicit aimed grooming of specific head locations, while collectively eliciting a whole head grooming sequence. Different tracing methods were used to reconstruct the projections of these neurons from different locations on the head to their distinct arborizations in the brain. This provides the first synaptic resolution somatotopic map of a head, and defines the parallel-projecting mechanosensory pathways that elicit head grooming.