1. Neuroscience
Download icon

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
Research Article
  • Cited 0
  • Views 646
  • Annotations
Cite this article as: eLife 2021;10:e66320 doi: 10.7554/eLife.66320

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.

Reviewing Editor

  1. Amy J Bastian, Kennedy Krieger Institute, United States

Publication history

  1. Received: January 7, 2021
  2. Preprint posted: January 27, 2021 (view preprint)
  3. Accepted: October 1, 2021
  4. Accepted Manuscript published: October 4, 2021 (version 1)
  5. Version of Record published: October 18, 2021 (version 2)

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

  • 646
    Page views
  • 81
    Downloads
  • 0
    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)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Further reading

    1. Neuroscience
    Zhengchao Xu et al.
    Tools and Resources Updated

    The dorsal raphe nucleus (DR) and median raphe nucleus (MR) contain populations of glutamatergic and GABAergic neurons that regulate diverse behavioral functions. However, their whole-brain input-output circuits remain incompletely elucidated. We used viral tracing combined with fluorescence micro-optical sectioning tomography to generate a comprehensive whole-brain atlas of inputs and outputs of glutamatergic and GABAergic neurons in the DR and MR. We found that these neurons received inputs from similar upstream brain regions. The glutamatergic and GABAergic neurons in the same raphe nucleus had divergent projection patterns with differences in critical brain regions. Specifically, MR glutamatergic neurons projected to the lateral habenula through multiple pathways. Correlation and cluster analysis revealed that glutamatergic and GABAergic neurons in the same raphe nucleus received heterogeneous inputs and sent different collateral projections. This connectivity atlas further elucidates the anatomical architecture of the raphe nuclei, which could facilitate better understanding of their behavioral functions.

    1. Neuroscience
    Shankar Ramachandran et al.
    Research Article Updated

    Neuromodulators promote adaptive behaviors that are often complex and involve concerted activity changes across circuits that are often not physically connected. It is not well understood how neuromodulatory systems accomplish these tasks. Here, we show that the Caenorhabditis elegans NLP-12 neuropeptide system shapes responses to food availability by modulating the activity of head and body wall motor neurons through alternate G-protein coupled receptor (GPCR) targets, CKR-1 and CKR-2. We show ckr-2 deletion reduces body bend depth during movement under basal conditions. We demonstrate CKR-1 is a functional NLP-12 receptor and define its expression in the nervous system. In contrast to basal locomotion, biased CKR-1 GPCR stimulation of head motor neurons promotes turning during local searching. Deletion of ckr-1 reduces head neuron activity and diminishes turning while specific ckr-1 overexpression or head neuron activation promote turning. Thus, our studies suggest locomotor responses to changing food availability are regulated through conditional NLP-12 stimulation of head or body wall motor circuits.