Non-selective inhibition of inappropriate motor-tendencies during response-conflict by a fronto-subthalamic mechanism

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

Abstract

To effectively interact with their environment, humans must often select actions from multiple incompatible options. Existing theories propose that during motoric response-conflict, inappropriate motor activity is actively (and perhaps non-selectively) suppressed by an inhibitory fronto-basal ganglia mechanism. We here tested this theory across three experiments. First, using scalp-EEG, we found that both outright action-stopping and response-conflict during action-selection invoke low-frequency activity of a common fronto-central source, whose activity relates to trial-by-trial behavioral indices of inhibition in both tasks. Second, using simultaneous intracranial recordings from the basal ganglia and motor cortex, we found that response-conflict increases the influence of the subthalamic nucleus on M1-representations of incorrect response-tendencies. Finally, using transcranial magnetic stimulation, we found that during the same time period when conflict-related STN-to-M1 communication is increased, cortico-spinal excitability is broadly suppressed. Together, these findings demonstrate that fronto-BG networks buttress action-selection under response-conflict by rapidly and non-selectively net-inhibiting inappropriate motor tendencies.

Data availability

The experimental code, data, and analysis routines underlying this research can be found on the Open Science Framework at the following URL: https://osf.io/k3ypt/.

The following data sets were generated

Article and author information

Author details

  1. Jan R Wessel

    Department of Neurology, University of Iowa Hospitals and Clinics, 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
  2. Darcy A Waller

    Department of Psychological and Brain Sciences, University of Iowa, Iowa City, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Jeremy DW Greenlee

    Department of Neurosurgery, University of Iowa Hospitals and Clinics, Iowa City, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Institute of Neurological Disorders and Stroke (R01 NS102201)

  • Jan R Wessel

National Science Foundation (CAREER 1752355)

  • 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: Informed consent was collected from all subjects and all procedures were approved by the local ethics committee at the University of Iowa (IRB #201511709, IRB # 201402720, IRB #201612707).

Copyright

© 2019, Wessel 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

  • 1,809
    views
  • 231
    downloads
  • 57
    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. Jan R Wessel
  2. Darcy A Waller
  3. Jeremy DW Greenlee
(2019)
Non-selective inhibition of inappropriate motor-tendencies during response-conflict by a fronto-subthalamic mechanism
eLife 8:e42959.
https://doi.org/10.7554/eLife.42959

Share this article

https://doi.org/10.7554/eLife.42959

Further reading

    1. Neuroscience
    Mihály Vöröslakos, Yunchang Zhang ... György Buzsáki
    Tools and Resources

    Brain states fluctuate between exploratory and consummatory phases of behavior. These state changes affect both internal computation and the organism’s responses to sensory inputs. Understanding neuronal mechanisms supporting exploratory and consummatory states and their switching requires experimental control of behavioral shifts and collecting sufficient amounts of brain data. To achieve this goal, we developed the ThermoMaze, which exploits the animal’s natural warmth-seeking homeostatic behavior. By decreasing the floor temperature and selectively heating unmarked areas, we observed that mice avoided the aversive state by exploring the maze and finding the warm spot. In its design, the ThermoMaze is analogous to the widely used water maze but without the inconvenience of a wet environment and, therefore, allows the collection of physiological data in many trials. We combined the ThermoMaze with electrophysiology recording, and report that spiking activity of hippocampal CA1 neurons during sharp-wave ripple events encode the position of mice. Thus, place-specific firing is not confined to locomotion and associated theta oscillations but persist during waking immobility and sleep at the same location. The ThermoMaze will allow for detailed studies of brain correlates of immobility, preparatory–consummatory transitions, and open new options for studying behavior-mediated temperature homeostasis.

    1. Neuroscience
    Sainan Liu, Jiepin Huang ... Yan Yang
    Research Article

    Social relationships guide individual behavior and ultimately shape the fabric of society. Primates exhibit particularly complex, differentiated, and multidimensional social relationships, which form interwoven social networks, reflecting both individual social tendencies and specific dyadic interactions. How the patterns of behavior that underlie these social relationships emerge from moment-to-moment patterns of social information processing remains unclear. Here, we assess social relationships among a group of four monkeys, focusing on aggression, grooming, and proximity. We show that individual differences in social attention vary with individual differences in patterns of general social tendencies and patterns of individual engagement with specific partners. Oxytocin administration altered social attention and its relationship to both social tendencies and dyadic relationships, particularly grooming and aggression. Our findings link the dynamics of visual information sampling to the dynamics of primate social networks.