Cortico-subcortical β burst dynamics underlying movement cancellation in humans

  1. Darcy A Diesburg  Is a corresponding author
  2. Jeremy DW Greenlee
  3. Jan R Wessel  Is a corresponding author
  1. University of Iowa, United States

Abstract

Dominant neuroanatomical models hold that humans regulate their movements via loop-like cortico-subcortical networks, which include the subthalamic nucleus (STN), motor thalamus, and sensorimotor cortex (SMC). Inhibitory commands across these networks are purportedly sent via transient, burst-like signals in the β frequency (15-29Hz). However, since human depth-recording studies are typically limited to one recording site, direct evidence for this proposition is hitherto lacking. Here, we present simultaneous multi-site recordings from SMC and either STN or motor thalamus in humans performing the stop-signal task. In line with their purported function as inhibitory signals, subcortical β-bursts were increased on successful stop-trials. STN bursts in particular were followed within 50ms by increased β-bursting over SMC. Moreover, between-site comparisons (including in a patient with simultaneous recordings from SMC, thalamus, and STN) confirmed that β-bursts in STN temporally precede thalamic β-bursts. This highly unique set of recordings provides empirical evidence for the role of β-bursts in conveying inhibitory commands along long-proposed cortico-subcortical networks underlying movement regulation in humans.

Data availability

All data analyzed during this study and scripts used for analyses are available on Dryad.

The following data sets were generated

Article and author information

Author details

  1. Darcy A Diesburg

    Department of Psychological and Brain Sciences, University of Iowa, Iowa City, United States
    For correspondence
    darcy-diesburg@uiowa.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3489-7624
  2. Jeremy DW Greenlee

    Department of Neurosurgery, University of Iowa, Iowa City, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8481-8517
  3. Jan R Wessel

    Department of Neurology, University of Iowa, Iowa City, United States
    For correspondence
    jan-wessel@uiowa.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7298-6601

Funding

National Institutes of Health (T32GSMC08540)

  • Darcy A Diesburg

National Institutes of Health (R01NS117753)

  • Jan R Wessel

National Science Foundation (CAREER 1752355)

  • Jan R Wessel

Carver College of Medicine & Iowa Neuroscience Institute (Research Program of Excellence Funding)

  • Jeremy DW Greenlee

Carver College of Medicine & Iowa Neuroscience Institute (Research Program of Excellence Funding)

  • Jan R Wessel

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

Ethics

Human subjects: Research participants signed a written informed consent document during a clinic visit prior to surgery. Experimental protocols were approved by the University of Iowa's Institutional Review Board (#201402720).

Reviewing Editor

  1. Nicole C Swann, University of Oregon, United States

Publication history

  1. Received: May 11, 2021
  2. Accepted: December 6, 2021
  3. Accepted Manuscript published: December 7, 2021 (version 1)
  4. Version of Record published: December 21, 2021 (version 2)

Copyright

© 2021, Diesburg 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

  • 699
    Page views
  • 113
    Downloads
  • 0
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, 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. Darcy A Diesburg
  2. Jeremy DW Greenlee
  3. Jan R Wessel
(2021)
Cortico-subcortical β burst dynamics underlying movement cancellation in humans
eLife 10:e70270.
https://doi.org/10.7554/eLife.70270
  1. Further reading

Further reading

    1. Neuroscience
    Mingchao Yan et al.
    Tools and Resources

    Resolving trajectories of axonal pathways in the primate prefrontal cortex remains crucial to gain insights into higher-order processes of cognition and emotion, which requires a comprehensive map of axonal projections linking demarcated subdivisions of prefrontal cortex and the rest of brain. Here, we report a mesoscale excitatory projectome issued from the ventrolateral prefrontal cortex (vlPFC) to the entire macaque brain by using viral-based genetic axonal tracing in tandem with high-throughput serial two-photon tomography, which demonstrated prominent monosynaptic projections to other prefrontal areas, temporal, limbic, and subcortical areas, relatively weak projections to parietal and insular regions but no projections directly to the occipital lobe. In a common 3D space, we quantitatively validated an atlas of diffusion tractography-derived vlPFC connections with correlative green fluorescent protein-labeled axonal tracing, and observed generally good agreement except a major difference in the posterior projections of inferior fronto-occipital fasciculus. These findings raise an intriguing question as to how neural information passes along long-range association fiber bundles in macaque brains, and call for the caution of using diffusion tractography to map the wiring diagram of brain circuits.

    1. Medicine
    2. Neuroscience
    Simon Oxenford et al.
    Tools and Resources

    Background: Deep Brain Stimulation (DBS) electrode implant trajectories are stereotactically defined using preoperative neuroimaging. To validate the correct trajectory, microelectrode recordings (MER) or local field potential recordings (LFP) can be used to extend neuroanatomical information (defined by magnetic resonance imaging) with neurophysiological activity patterns recorded from micro- and macroelectrodes probing the surgical target site. Currently, these two sources of information (imaging vs. electrophysiology) are analyzed separately, while means to fuse both data streams have not been introduced.

    Methods: Here we present a tool that integrates resources from stereotactic planning, neuroimaging, MER and high-resolution atlas data to create a real-time visualization of the implant trajectory. We validate the tool based on a retrospective cohort of DBS patients (𝑁 = 52) offline and present single use cases of the real-time platform. Results: We establish an open-source software tool for multimodal data visualization and analysis during DBS surgery. We show a general correspondence between features derived from neuroimaging and electrophysiological recordings and present examples that demonstrate the functionality of the tool.

    Conclusions: This novel software platform for multimodal data visualization and analysis bears translational potential to improve accuracy of DBS surgery. The toolbox is made openly available and is extendable to integrate with additional software packages.

    Funding: Deutsche Forschungsgesellschaft (410169619, 424778381), Deutsches Zentrum für Luftund Raumfahrt (DynaSti), National Institutes of Health (2R01 MH113929), Foundation for OCD Research (FFOR).