Beta band oscillations in motor cortex reflect neural population signals that delay movement onset

  1. Preeya Khanna
  2. Jose M Carmena  Is a corresponding author
  1. University of California, Berkeley, United States

Abstract

Motor cortical beta oscillations have been reported for decades, yet their behavioral correlates remain disputed. Some studies link beta oscillations to changes in underlying neural activity, but the specific behavioral manifestations of these reported changes remain elusive. To investigate how changes in population neural activity, beta oscillations, and behavior are linked, we recorded multi-scale neural activity from motor cortex while three macaques performed a novel neurofeedback task. Subjects volitionally brought their beta power to an instructed state and subsequently executed an arm reach. Reaches preceded by a reduction in beta power exhibited significantly faster movement onset times than reaches preceded by an increase in beta power. Further, population neural activity was found to shift farther from a movement onset state during beta oscillations that were neurofeedback-induced or naturally occurring during reaching tasks. This finding establishes a population neural basis for slowing during periods of beta oscillatory activity.

Article and author information

Author details

  1. Preeya Khanna

    UC Berkeley-UCSF Joint Graduate Program in Bioengineering, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Jose M Carmena

    UC Berkeley-UCSF Joint Graduate Program in Bioengineering, University of California, Berkeley, Berkeley, United States
    For correspondence
    jcarmena@berkeley.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0214-2489

Funding

National Science Foundation

  • Preeya Khanna

Defense Sciences Office, DARPA (W911NF-14- 2-0043)

  • Jose M Carmena

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

Ethics

Animal experimentation: All procedures were conducted in compliance with the NIH Guide for the Care and Use of Laboratory Animals and were approved by the University of California, Berkeley Institutional Animal Care and Use Committee (protocol AUP-2014-09-6720)

Copyright

© 2017, Khanna & Carmena

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.

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. Preeya Khanna
  2. Jose M Carmena
(2017)
Beta band oscillations in motor cortex reflect neural population signals that delay movement onset
eLife 6:e24573.
https://doi.org/10.7554/eLife.24573

Share this article

https://doi.org/10.7554/eLife.24573

Further reading

    1. Neuroscience
    Sven Ohl, Martin Rolfs
    Research Article

    Detecting causal relations structures our perception of events in the world. Here, we determined for visual interactions whether generalized (i.e. feature-invariant) or specialized (i.e. feature-selective) visual routines underlie the perception of causality. To this end, we applied a visual adaptation protocol to assess the adaptability of specific features in classical launching events of simple geometric shapes. We asked observers to report whether they observed a launch or a pass in ambiguous test events (i.e. the overlap between two discs varied from trial to trial). After prolonged exposure to causal launch events (the adaptor) defined by a particular set of features (i.e. a particular motion direction, motion speed, or feature conjunction), observers were less likely to see causal launches in subsequent ambiguous test events than before adaptation. Crucially, adaptation was contingent on the causal impression in launches as demonstrated by a lack of adaptation in non-causal control events. We assessed whether this negative aftereffect transfers to test events with a new set of feature values that were not presented during adaptation. Processing in specialized (as opposed to generalized) visual routines predicts that the transfer of visual adaptation depends on the feature similarity of the adaptor and the test event. We show that the negative aftereffects do not transfer to unadapted launch directions but do transfer to launch events of different speeds. Finally, we used colored discs to assign distinct feature-based identities to the launching and the launched stimulus. We found that the adaptation transferred across colors if the test event had the same motion direction as the adaptor. In summary, visual adaptation allowed us to carve out a visual feature space underlying the perception of causality and revealed specialized visual routines that are tuned to a launch’s motion direction.

    1. Neuroscience
    Ulrike Pech, Jasper Janssens ... Patrik Verstreken
    Research Article

    The classical diagnosis of Parkinsonism is based on motor symptoms that are the consequence of nigrostriatal pathway dysfunction and reduced dopaminergic output. However, a decade prior to the emergence of motor issues, patients frequently experience non-motor symptoms, such as a reduced sense of smell (hyposmia). The cellular and molecular bases for these early defects remain enigmatic. To explore this, we developed a new collection of five fruit fly models of familial Parkinsonism and conducted single-cell RNA sequencing on young brains of these models. Interestingly, cholinergic projection neurons are the most vulnerable cells, and genes associated with presynaptic function are the most deregulated. Additional single nucleus sequencing of three specific brain regions of Parkinson’s disease patients confirms these findings. Indeed, the disturbances lead to early synaptic dysfunction, notably affecting cholinergic olfactory projection neurons crucial for olfactory function in flies. Correcting these defects specifically in olfactory cholinergic interneurons in flies or inducing cholinergic signaling in Parkinson mutant human induced dopaminergic neurons in vitro using nicotine, both rescue age-dependent dopaminergic neuron decline. Hence, our research uncovers that one of the earliest indicators of disease in five different models of familial Parkinsonism is synaptic dysfunction in higher-order cholinergic projection neurons and this contributes to the development of hyposmia. Furthermore, the shared pathways of synaptic failure in these cholinergic neurons ultimately contribute to dopaminergic dysfunction later in life.