Early life experience sets hard limits on motor learning as evidenced from artificial arm use

  1. Roni O Maimon-Mor  Is a corresponding author
  2. Hunter R Schone
  3. David Henderson Slater
  4. Aldo A Faisal
  5. Tamar R Makin
  1. University of Oxford, United Kingdom
  2. University College London, United Kingdom
  3. Nuffield Orthopaedic Centre, United Kingdom
  4. Imperial College London, United Kingdom

Abstract

The study of artificial arms provides a unique opportunity to address long-standing questions on sensorimotor plasticity and development. Learning to use an artificial arm arguably depends on fundamental building blocks of body representation and would therefore be impacted by early-life experience. We tested artificial arm motor-control in two adult populations with upper-limb deficiencies: a congenital group - individuals who were born with a partial arm, and an acquired group - who lost their arm following amputation in adulthood. Brain plasticity research teaches us that the earlier we train to acquire new skills (or use a new technology) the better we benefit from this practice as adults. Instead, we found that although the congenital group started using an artificial arm as toddlers, they produced increased error noise and directional errors when reaching to visual targets, relative to the acquired group who performed similarly to controls. However, the earlier an individual with a congenital limb difference was fitted with an artificial arm, the better their motor control was. Since we found no group differences when reaching without visual feedback, we suggest that the ability to perform efficient visual-based corrective movements is highly dependent on either biological or artificial arm experience at a very young age. Subsequently, opportunities for sensorimotor plasticity become more limited.

Data availability

All data generated and analysed during this study can be found at https://osf.io/quyke/

The following data sets were generated
    1. Maimon Mor RO
    2. Makin TR
    (2021) Artificial-arm (prosthesis) motor control
    Open Science Framework, DOI 10.17605/OSF.IO/QUYKE.

Article and author information

Author details

  1. Roni O Maimon-Mor

    WIN Centre, Nuffield Department of Clinical Neuroscience, University of Oxford, Oxford, United Kingdom
    For correspondence
    roni.maimonmor@ndcn.ox.ac.uk
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5262-9976
  2. Hunter R Schone

    Institute of Cognitive Neuroscience, University College London, London, United Kingdom
    Competing interests
    No competing interests declared.
  3. David Henderson Slater

    Oxford Centre for Enablement, Nuffield Orthopaedic Centre, Oxford, United Kingdom
    Competing interests
    No competing interests declared.
  4. Aldo A Faisal

    Department of Bioengineering, Imperial College London, London, United Kingdom
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0813-7207
  5. Tamar R Makin

    Institute of Cognitive Neuroscience, University College London, London, United Kingdom
    Competing interests
    Tamar R Makin, Senior editor, eLife.The authors are currently engaged in collaborations with Chris Baker (Senior Editor) and Joern Diedrichsen (BRE). The authors are affiliated with the same institutions as Tim Behrens (Deputy Editor)..
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5816-8979

Funding

H2020 European Research Council (715022 EmbodiedTech)

  • Tamar R Makin

Wellcome Trust (Senior Research Fellowship (215575/Z/19/Z))

  • Tamar R Makin

Clarendon Fund (Graduate Student fellowship)

  • Roni O Maimon-Mor

University College, Oxford (Graduate Student fellowship)

  • Roni O Maimon-Mor

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

Ethics

Human subjects: Participants were recruited to the study between October 2017 and December 2018, based on the guidelines in our ethical approvals (UCL REC: 9937/001; NHS National Research Ethics service: 18/LO/0474), and in accordance with the declaration of Helsinki. All participants gave full written informed consent for their participation, data storage and dissemination.

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

Metrics

  • 1,361
    views
  • 200
    downloads
  • 6
    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. Roni O Maimon-Mor
  2. Hunter R Schone
  3. David Henderson Slater
  4. Aldo A Faisal
  5. Tamar R Makin
(2021)
Early life experience sets hard limits on motor learning as evidenced from artificial arm use
eLife 10:e66320.
https://doi.org/10.7554/eLife.66320

Share this article

https://doi.org/10.7554/eLife.66320

Further reading

    1. Computational and Systems Biology
    2. Neuroscience
    Anna Cattani, Don B Arnold ... Nancy Kopell
    Research Article

    The basolateral amygdala (BLA) is a key site where fear learning takes place through synaptic plasticity. Rodent research shows prominent low theta (~3–6 Hz), high theta (~6–12 Hz), and gamma (>30 Hz) rhythms in the BLA local field potential recordings. However, it is not understood what role these rhythms play in supporting the plasticity. Here, we create a biophysically detailed model of the BLA circuit to show that several classes of interneurons (PV, SOM, and VIP) in the BLA can be critically involved in producing the rhythms; these rhythms promote the formation of a dedicated fear circuit shaped through spike-timing-dependent plasticity. Each class of interneurons is necessary for the plasticity. We find that the low theta rhythm is a biomarker of successful fear conditioning. The model makes use of interneurons commonly found in the cortex and, hence, may apply to a wide variety of associative learning situations.

    1. Neuroscience
    Mazen Makke, Alejandro Pastor-Ruiz ... Dieter Bruns
    Research Article

    Complexin determines magnitude and kinetics of synchronized secretion, but the underlying molecular mechanisms remained unclear. Here, we show that the hydrophobic face of the amphipathic helix at the C-terminus of Complexin II (CpxII, amino acids 115–134) binds to fusion-promoting SNARE proteins, prevents premature secretion, and allows vesicles to accumulate in a release-ready state in mouse chromaffin cells. Specifically, we demonstrate that an unrelated amphipathic helix functionally substitutes for the C-terminal domain (CTD) of CpxII and that amino acid substitutions on the hydrophobic side compromise the arrest of the pre-fusion intermediate. To facilitate synchronous vesicle fusion, the N-terminal domain (NTD) of CpxII (amino acids 1–27) specifically cooperates with synaptotagmin I (SytI), but not with synaptotagmin VII. Expression of CpxII rescues the slow release kinetics of the Ca2+-binding mutant Syt I R233Q, whereas the N-terminally truncated variant of CpxII further delays it. These results indicate that the CpxII NTD regulates mechanisms which are governed by the forward rate of Ca2+ binding to Syt I. Overall, our results shed new light on key molecular properties of CpxII that hinder premature exocytosis and accelerate synchronous exocytosis.