Distinct population code for movement kinematics and changes of ongoing movements in human subthalamic nucleus

  1. Dennis London  Is a corresponding author
  2. Arash Fazl
  3. Kalman Katlowitz
  4. Marisol Soula
  5. Michael Pourfar
  6. Alon Mogilner
  7. Roozbeh Kiani  Is a corresponding author
  1. New York University, United States
  2. NYU Langone Health, United States

Abstract

The subthalamic nucleus (STN) is theorized to globally suppress movement through connections with downstream basal ganglia structures. Current theories are supported by increased STN activity when subjects withhold an uninitiated action plan, but a critical test of these theories requires studying STN responses when an ongoing action is replaced with an alternative. We perform this test in subjects with Parkinson's disease using an extended reaching task where the movement trajectory changes mid-action. We show that STN activity decreases during action switches, contrary to prevalent theories. Further, beta oscillations in the STN local field potential, which are associated with movement inhibition, do not show increased power or spiking entrainment during switches. We report an inhomogeneous population neural code in STN, with one sub-population encoding movement kinematics and direction and another encoding unexpected action switches. We suggest an elaborate neural code in STN that contributes to planning actions and changing the plans.

Data availability

All raw and processed data has been uploaded to Dryad. DOI: 10.5061/dryad.2jm63xsq2

The following data sets were generated

Article and author information

Author details

  1. Dennis London

    Center for Neural Science, New York University, New York, United States
    For correspondence
    dennis.london@nyulangone.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8134-2683
  2. Arash Fazl

    Center for Neuromodulation, Department of Neurosurgery, NYU Langone Health, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Kalman Katlowitz

    Neuroscience Institute, NYU Langone Health, New York, NY, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Marisol Soula

    Neuroscience Institute, NYU Langone Health, New York, NY, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Michael Pourfar

    Center for Neuromodulation, Department of Neurosurgery, NYU Langone Health, New York, NY, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Alon Mogilner

    Center for Neuromodulation, Department of Neurosurgery, NYU Langone Health, New York, NY, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Roozbeh Kiani

    Center for Neural Science, New York University, New York, United States
    For correspondence
    roozbeh@nyu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0614-6791

Funding

Simons Collaboration on the Global Brain (542997,543009)

  • Roozbeh Kiani

McKnight Scholar Award

  • Roozbeh Kiani

Pew Scholarship in the Biomedical Sciences

  • Roozbeh Kiani

National Institutes of Mental Health R01 (MH109180-01)

  • Roozbeh Kiani

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

Ethics

Human subjects: Subjects signed informed consent including consent to publish. The study protocol was approved by the NYU School of Medicine Office of Science and Research Institutional Review Board. Study ID: S16-01855

Reviewing Editor

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

Publication history

  1. Preprint posted: November 12, 2020 (view preprint)
  2. Received: November 13, 2020
  3. Accepted: September 14, 2021
  4. Accepted Manuscript published: September 14, 2021 (version 1)
  5. Version of Record published: October 8, 2021 (version 2)

Copyright

© 2021, London 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

  • 1,391
    Page views
  • 164
    Downloads
  • 1
    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. Dennis London
  2. Arash Fazl
  3. Kalman Katlowitz
  4. Marisol Soula
  5. Michael Pourfar
  6. Alon Mogilner
  7. Roozbeh Kiani
(2021)
Distinct population code for movement kinematics and changes of ongoing movements in human subthalamic nucleus
eLife 10:e64893.
https://doi.org/10.7554/eLife.64893

Further reading

    1. Neuroscience
    2. Physics of Living Systems
    Sabrina A Jones, Jacob H Barfield ... Woodrow L Shew
    Research Article

    Naturally occurring body movements and collective neural activity both exhibit complex dynamics, often with scale-free, fractal spatiotemporal structure. Scale-free dynamics of both brain and behavior are important because each is associated with functional benefits to the organism. Despite their similarities, scale-free brain activity and scale-free behavior have been studied separately, without a unified explanation. Here we show that scale-free dynamics of mouse behavior and neurons in visual cortex are strongly related. Surprisingly, the scale-free neural activity is limited to specific subsets of neurons, and these scale-free subsets exhibit stochastic winner-take-all competition with other neural subsets. This observation is inconsistent with prevailing theories of scale-free dynamics in neural systems, which stem from the criticality hypothesis. We develop a computational model which incorporates known cell-type-specific circuit structure, explaining our findings with a new type of critical dynamics. Our results establish neural underpinnings of scale-free behavior and clear behavioral relevance of scale-free neural activity.

    1. Neuroscience
    Barna Zajzon, David Dahmen ... Renato Duarte
    Research Article

    Information from the sensory periphery is conveyed to the cortex via structured projection pathways that spatially segregate stimulus features, providing a robust and efficient encoding strategy. Beyond sensory encoding, this prominent anatomical feature extends throughout the neocortex. However, the extent to which it influences cortical processing is unclear. In this study, we combine cortical circuit modeling with network theory to demonstrate that the sharpness of topographic projections acts as a bifurcation parameter, controlling the macroscopic dynamics and representational precision across a modular network. By shifting the balance of excitation and inhibition, topographic modularity gradually increases task performance and improves the signal-to-noise ratio across the system. We demonstrate that in biologically constrained networks, such a denoising behavior is contingent on recurrent inhibition. We show that this is a robust and generic structural feature that enables a broad range of behaviorally-relevant operating regimes, and provide an in-depth theoretical analysis unravelling the dynamical principles underlying the mechanism.