Wireless recording from unrestrained monkeys reveals motor goal encoding beyond immediate reach in frontoparietal cortex
- 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
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sensorimotorgroupdpz/MaCaQuEZenodo, doi:10.5281/zenodo.3685793.
Article and author information
Author details
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.
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.
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.
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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
Further reading
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- Neuroscience
When holding visual information temporarily in working memory (WM), the neural representation of the memorandum is distributed across various cortical regions, including visual and frontal cortices. However, the role of stimulus representation in visual and frontal cortices during WM has been controversial. Here, we tested the hypothesis that stimulus representation persists in the frontal cortex to facilitate flexible control demands in WM. During functional MRI, participants flexibly switched between simple WM maintenance of visual stimulus or more complex rule-based categorization of maintained stimulus on a trial-by-trial basis. Our results demonstrated enhanced stimulus representation in the frontal cortex that tracked demands for active WM control and enhanced stimulus representation in the visual cortex that tracked demands for precise WM maintenance. This differential frontal stimulus representation traded off with the newly-generated category representation with varying control demands. Simulation using multi-module recurrent neural networks replicated human neural patterns when stimulus information was preserved for network readout. Altogether, these findings help reconcile the long-standing debate in WM research, and provide empirical and computational evidence that flexible stimulus representation in the frontal cortex during WM serves as a potential neural coding scheme to accommodate the ever-changing environment.
