Adapting non-invasive human recordings along multiple task-axes shows unfolding of spontaneous and over-trained choice

Abstract

Choices rely on a transformation of sensory inputs into motor responses. Using invasive single neuron recordings, the evolution of a choice process has been tracked by projecting population neural responses into state spaces. Here we develop an approach that allows us to recover similar trajectories on a millisecond timescale in non-invasive human recordings. We selectively suppress activity related to three task-axes, relevant and irrelevant sensory inputs and response direction in magnetoencephalography data acquired during context-dependent choices. Recordings from premotor cortex show a progression from processing sensory input to processing the response. In contrast to previous macaque recordings, information related to choice-irrelevant features is represented more weakly than choice-relevant sensory information. To test whether this mechanistic difference between species is caused by extensive overtraining common in non-human primate studies, we trained humans on >20,000 trials of the task. Choice-irrelevant features were still weaker than relevant features in premotor cortex after overtraining.

Data availability

Source data files for figures 2, 3, 4, and are provided.All datasets and codes for reproducing the results will be uploaded to Open Science Framework (OSF) after acceptance.

Article and author information

Author details

  1. Yu Takagi

    Wellcome Centre for Integrative Neuroimaging (WIN), University of Oxford, Oxford, United Kingdom
    For correspondence
    yutakagi322@gmail.com
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0503-785X
  2. Laurence Tudor Hunt

    Wellcome Centre for Integrative Neuroimaging, Department of Psychiatry, University of Oxford, Oxford, United Kingdom
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8393-8533
  3. Mark W Woolrich

    Oxford Centre for Human Brain Activity (OHBA), Wellcome Centre for Integrative NeuroImaging, Department of Psychiatry, University of Oxford, Oxford, United Kingdom
    Competing interests
    No competing interests declared.
  4. Timothy E Behrens

    Wellcome Trust Centre for Neuroimaging, University of Oxford, Oxford, United Kingdom
    Competing interests
    Timothy E Behrens, Senior/Deputy editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0048-1177
  5. Miriam C Klein-Flügge

    Wellcome Centre for Integrative Neuroimaging (WIN), Department of Experimental Psychology, University of Oxford, Oxford, United Kingdom
    For correspondence
    miriam.klein-flugge@psy.ox.ac.uk
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5156-9833

Funding

Japan Society for the Promotion of Science (23118001,23118002)

  • Yu Takagi

Uehara Memorial Foundation

  • Yu Takagi

Sir Henry Wellcome Fellowship (103184/Z/13/Z)

  • Miriam C Klein-Flügge

Wellcome Senior Research Fellowship (104765/Z/14/Z)

  • Timothy E Behrens

Wellcome Principal Research Fellowship (219525/Z/19/Z)

  • Timothy E Behrens

JS McDonnell Foundation award (JSMF220020372)

  • Timothy E Behrens

Wellcome Collaborator award (214314/Z/18/Z)

  • Timothy E Behrens

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

Reviewing Editor

  1. J Matias Palva, University of Helsinki, Finland

Ethics

Human subjects: The study was approved by the University College London (UCL) Research Ethics Committee (reference 1825/005) and all participants gave written informed consent.

Version history

  1. Received: July 13, 2020
  2. Accepted: April 26, 2021
  3. Accepted Manuscript published: May 11, 2021 (version 1)
  4. Version of Record published: May 24, 2021 (version 2)

Copyright

© 2021, Takagi 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.

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  1. Yu Takagi
  2. Laurence Tudor Hunt
  3. Mark W Woolrich
  4. Timothy E Behrens
  5. Miriam C Klein-Flügge
(2021)
Adapting non-invasive human recordings along multiple task-axes shows unfolding of spontaneous and over-trained choice
eLife 10:e60988.
https://doi.org/10.7554/eLife.60988

Share this article

https://doi.org/10.7554/eLife.60988

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