1. Neuroscience

Temporal cascade of frontal, motor and muscle processes underlying human action-stopping

  1. Sumitash Jana  Is a corresponding author
  2. Ricci Hannah  Is a corresponding author
  3. Vignesh Muralidharan
  4. Adam R Aron
  1. University of California, San Diego, United States
https://doi.org/10.7554/eLife.50371
Share this article
Cite this article
  1. Sumitash Jana
  2. Ricci Hannah
  3. Vignesh Muralidharan
  4. Adam R Aron
(2020)
Temporal cascade of frontal, motor and muscle processes underlying human action-stopping
eLife 9:e50371.
https://doi.org/10.7554/eLife.50371
  2. Download BibTeX
  3. Download .RIS

Abstract

Action-stopping is a canonical executive function thought to involve top-down control over the motor system. Here we aimed to validate this stopping system using high temporal resolution methods in humans. We show that, following the requirement to stop, there was an increase of right frontal beta (~13 to 30 Hz) at ~120 ms, likely a proxy of right inferior frontal gyrus; then, at 140 ms, there was a broad skeletomotor suppression, likely reflecting the impact of the subthalamic nucleus on basal ganglia output; then, at ~160 ms, suppression was detected in the muscle, and, finally, the behavioral time of stopping was ~220 ms. This temporal cascade supports a physiological model of action-stopping, and partitions it into subprocesses that are isolable to different nodes and are more precise than the behavioral latency of stopping. Variation in these subprocesses, including at the single-trial level, could better explain individual differences in impulse control.

Data availability

A core element of this paper is a novel method of calculating single-trial stopping speed from EMG. Accordingly, we provide the EMG and behavioral data from 10 participants in study 1, along with analysis scripts, and a brief description of how to execute the scripts (https://osf.io/b2ng5/).

The following data sets were generated

Article and author information

Author details

  1. Sumitash Jana

    Department of Psychology, University of California, San Diego, San Diego, United States
    For correspondence
    s2jana@ucsd.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3742-3958

  2. Ricci Hannah

    Department of Psychology, University of California, San Diego, San Diego, United States
    For correspondence
    rhannah@ucsd.edu
    Competing interests
    No competing interests declared.

  3. Vignesh Muralidharan

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

  4. Adam R Aron

    Department of Psychology, University of California, San Diego, San Diego, United States
    Competing interests
    Adam R Aron, Reviewing editor, eLife.

Funding

National Institutes of Health (NS 106822,DA 026452)

  • Sumitash Jana
  • Ricci Hannah
  • Vignesh Muralidharan
  • Adam R Aron

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

Reviewing Editor

  1. Wery van den Wildenberg, Universiteit van Amsterdam, Netherlands

Ethics

Human subjects: All human volunteers provided written informed consent prior to their participation. The participants were compensated at $20/hour. The University of California San Diego Institutional Review Board approved all the studies (protocol #171285).

Version history

  1. Received: July 20, 2019
  2. Accepted: March 17, 2020
  3. Accepted Manuscript published: March 18, 2020 (version 1)
  4. Version of Record published: April 15, 2020 (version 2)

Copyright

© 2020, Jana 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

  • 3,142
    views
  • 453
    downloads
  • 115
    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. Sumitash Jana
  2. Ricci Hannah
  3. Vignesh Muralidharan
  4. Adam R Aron
(2020)
Temporal cascade of frontal, motor and muscle processes underlying human action-stopping
eLife 9:e50371.
https://doi.org/10.7554/eLife.50371

Share this article

https://doi.org/10.7554/eLife.50371

Categories and tags

Research organism

Further reading

    1. Developmental Biology
    2. Neuroscience

    Spatiotemporal changes in Netrin/Dscam1 signaling dictate axonal projection direction in Drosophila small ventral lateral clock neurons

    Jingjing Liu, Yuedong Wang ... Yao Tian
    Research Article

    Axon projection is a spatial- and temporal-specific process in which the growth cone receives environmental signals guiding axons to their final destination. However, the mechanisms underlying changes in axonal projection direction without well-defined landmarks remain elusive. Here, we present evidence showcasing the dynamic nature of axonal projections in Drosophila’s small ventral lateral clock neurons (s-LNvs). Our findings reveal that these axons undergo an initial vertical projection in the early larval stage, followed by a subsequent transition to a horizontal projection in the early-to-mid third instar larvae. The vertical projection of s-LNv axons correlates with mushroom body calyx expansion, while the s-LNv-expressed Down syndrome cell adhesion molecule (Dscam1) interacts with Netrins to regulate the horizontal projection. During a specific temporal window, locally newborn dorsal clock neurons secrete Netrins, facilitating the transition of axonal projection direction in s-LNvs. Our study establishes a compelling in vivo model to probe the mechanisms of axonal projection direction switching in the absence of clear landmarks. These findings underscore the significance of dynamic local microenvironments in the complementary regulation of axonal projection direction transitions.

    1. Neuroscience

    Cerebellum: Linking abnormal neural activity patterns to motor deficits

    David J Herzfeld
    Insight

    Abnormal activity in the cerebellar nuclei can be used to predict motor symptoms and induce them experimentally, pointing to potential therapeutic strategies.

    1. Cell Biology
    2. Neuroscience

    Presynaptic Rac1 in the hippocampus selectively regulates working memory

    Jaebin Kim, Edwin Bustamante ... Scott H Soderling
    Research Article

    One of the most extensively studied members of the Ras superfamily of small GTPases, Rac1 is an intracellular signal transducer that remodels actin and phosphorylation signaling networks. Previous studies have shown that Rac1-mediated signaling is associated with hippocampal-dependent working memory and longer-term forms of learning and memory and that Rac1 can modulate forms of both pre- and postsynaptic plasticity. How these different cognitive functions and forms of plasticity mediated by Rac1 are linked, however, is unclear. Here, we show that spatial working memory in mice is selectively impaired following the expression of a genetically encoded Rac1 inhibitor at presynaptic terminals, while longer-term cognitive processes are affected by Rac1 inhibition at postsynaptic sites. To investigate the regulatory mechanisms of this presynaptic process, we leveraged new advances in mass spectrometry to identify the proteomic and post-translational landscape of presynaptic Rac1 signaling. We identified serine/threonine kinases and phosphorylated cytoskeletal signaling and synaptic vesicle proteins enriched with active Rac1. The phosphorylated sites in these proteins are at positions likely to have regulatory effects on synaptic vesicles. Consistent with this, we also report changes in the distribution and morphology of synaptic vesicles and in postsynaptic ultrastructure following presynaptic Rac1 inhibition. Overall, this study reveals a previously unrecognized presynaptic role of Rac1 signaling in cognitive processes and provides insights into its potential regulatory mechanisms.