Wireless recording from unrestrained monkeys reveals motor goal encoding beyond immediate reach in frontoparietal cortex

  1. Michael Berger  Is a corresponding author
  2. Naubahar Shahryar Agha
  3. Alexander Gail
  1. German Primate Center, Germany

Abstract

System neuroscience of motor cognition regarding the space beyond immediate reach mandates free, yet experimentally controlled movements. We present an experimental environment (Reach Cage) and a versatile visuo-haptic interaction system (MaCaQuE) for investigating goal-directed whole-body movements of unrestrained monkeys. Two rhesus monkeys conducted instructed walk-and-reach movements towards targets flexibly positioned in the cage. We tracked 3D multi-joint arm and head movements using markerless motion capture. Movements show small trial-to-trial variability despite being unrestrained. We wirelessly recorded 192 broad-band neural signals from three cortical sensorimotor areas simultaneously. Single unit activity is selective for different reach and walk-and-reach movements. Walk-and-reach targets could be decoded from premotor and parietal but not motor cortical activity during movement planning. The Reach Cage allows systems-level sensorimotor neuroscience studies with full-body movements in a configurable 3D spatial setting with unrestrained monkeys. We conclude that the primate frontoparietal network encodes reach goals beyond immediate reach during movement planning.

Data availability

All data (schematics, soft- and hardware documentation) for constructing the MaCaQuE or equivalent systems is made available via GitHub: https://github.com/sensorimotorgroupdpz/MaCaQuE

The following data sets were generated

Article and author information

Author details

  1. Michael Berger

    Sensorimotor Group, German Primate Center, Göttingen, Germany
    For correspondence
    mberger@dpz.eu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7239-1675
  2. Naubahar Shahryar Agha

    Sensorimotor Group, German Primate Center, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Alexander Gail

    Sensorimotor Group, German Primate Center, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1165-4646

Funding

Deutsche Forschungsgemeinschaft (DFG RU-1847,grant GA1475-C1)

  • Alexander Gail

European Commission (EC-H2020-FETPROACT-16 732266 WP1)

  • Alexander Gail

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

Reviewing Editor

  1. Bijan Pesaran

Ethics

Animal experimentation: Both animals were housed in social groups with one (monkey L) or two (monkey K) male conspecifics in facilities of the German Primate Center. The facilities provide cage sizes exceeding the requirements by German and European regulations, access to an enriched environment including wooden structures and various toys (Calapai et al. 2017). All procedures have been approved by the responsible regional government office [Niedersächsisches Landesamt für Verbraucherschutz und Lebensmittelsicherheit (LAVES)] under permit numbers 3392 42502-04-13/1100 and comply with German Law and the European Directive 2010/63/EU regulating use of animals in research.

Version history

  1. Received: August 28, 2019
  2. Accepted: May 2, 2020
  3. Accepted Manuscript published: May 4, 2020 (version 1)
  4. Version of Record published: May 15, 2020 (version 2)
  5. Version of Record updated: April 13, 2021 (version 3)

Copyright

© 2020, Berger 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

  • 4,781
    views
  • 601
    downloads
  • 34
    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. Michael Berger
  2. Naubahar Shahryar Agha
  3. Alexander Gail
(2020)
Wireless recording from unrestrained monkeys reveals motor goal encoding beyond immediate reach in frontoparietal cortex
eLife 9:e51322.
https://doi.org/10.7554/eLife.51322

Share this article

https://doi.org/10.7554/eLife.51322

Further reading

    1. Neuroscience
    Ya-Hui Lin, Li-Wen Wang ... Li-An Chu
    Research Article

    Tissue-clearing and labeling techniques have revolutionized brain-wide imaging and analysis, yet their application to clinical formalin-fixed paraffin-embedded (FFPE) blocks remains challenging. We introduce HIF-Clear, a novel method for efficiently clearing and labeling centimeter-thick FFPE specimens using elevated temperature and concentrated detergents. HIF-Clear with multi-round immunolabeling reveals neuron circuitry regulating multiple neurotransmitter systems in a whole FFPE mouse brain and is able to be used as the evaluation of disease treatment efficiency. HIF-Clear also supports expansion microscopy and can be performed on a non-sectioned 15-year-old FFPE specimen, as well as a 3-month formalin-fixed mouse brain. Thus, HIF-Clear represents a feasible approach for researching archived FFPE specimens for future neuroscientific and 3D neuropathological analyses.