Stability of motor representations after paralysis

  1. Charles Guan  Is a corresponding author
  2. Tyson Aflalo  Is a corresponding author
  3. Carey Y Zhang
  4. Elena Amoruso
  5. Emily R Rosario
  6. Nader Pouratian
  7. Richard A Andersen
  1. California Institute of Technology, United States
  2. University College London, United Kingdom
  3. Casa Colina Hospital and Centers for Healthcare, United States
  4. University of California, Los Angeles, United States

Abstract

Neural plasticity allows us to learn skills and incorporate new experiences. What happens when our lived experiences fundamentally change, such as after a severe injury? To address this question, we analyzed intracortical population activity in the posterior parietal cortex (PPC) of a tetraplegic adult as she controlled a virtual hand through a brain-computer interface (BCI). By attempting to move her fingers, she could accurately drive the corresponding virtual fingers. Neural activity during finger movements exhibited robust representational structure similar to fMRI recordings of able-bodied individuals' motor cortex, which has previously been shown to reflect able-bodied usage patterns. The finger representational structure was consistent throughout multiple sessions, even though the structure contributed to BCI decoding errors. Within individual BCI movements, the representational structure was dynamic, first resembling muscle activation patterns and then resembling the anticipated sensory consequences. Our results reveal that motor representations in PPC reflect able-bodied motor usage patterns even after paralysis, and BCIs can re-engage these representations to restore lost motor functions.

Data availability

Data is available on the BRAIN Initiative DANDI Archive at https://dandiarchive.org/dandiset/000147

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Charles Guan

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    For correspondence
    cguan@caltech.edu
    Competing interests
    The authors declare that no competing interests exist.
  2. Tyson Aflalo

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    For correspondence
    taflalo@caltech.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0101-2455
  3. Carey Y Zhang

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Elena Amoruso

    Institute of Cognitive Neuroscience, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Emily R Rosario

    Casa Colina Hospital and Centers for Healthcare, Pomona, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Nader Pouratian

    5David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Richard A Andersen

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Eye Institute (R01EY015545)

  • Charles Guan
  • Tyson Aflalo
  • Emily R Rosario
  • Nader Pouratian
  • Richard A Andersen

National Eye Institute (UG1EY032039)

  • Charles Guan
  • Tyson Aflalo
  • Emily R Rosario
  • Nader Pouratian
  • Richard A Andersen

Tianqiao and Chrissy Chen Brain-machine Interface Center at Caltech

  • Tyson Aflalo
  • Richard A Andersen

Boswell Foundation

  • Richard A Andersen

Amazon AI4Science Fellowship

  • Charles Guan

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

Ethics

Human subjects: All procedures were approved by the California Institute of Technology, Casa Colina Hospital and Centers for Healthcare, and the University of California, Los Angeles Institutional Review Boards. NS consented to the surgical procedure as well as to the subsequent clinical studies after understanding their nature, objectives, and potential risks.

Copyright

© 2022, Guan 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

  • 1,571
    views
  • 332
    downloads
  • 11
    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. Charles Guan
  2. Tyson Aflalo
  3. Carey Y Zhang
  4. Elena Amoruso
  5. Emily R Rosario
  6. Nader Pouratian
  7. Richard A Andersen
(2022)
Stability of motor representations after paralysis
eLife 11:e74478.
https://doi.org/10.7554/eLife.74478

Share this article

https://doi.org/10.7554/eLife.74478

Further reading

    1. Cell Biology
    2. Neuroscience
    Luis Sánchez-Guardado, Peyman Callejas Razavi ... Carlos Lois
    Research Article

    The assembly and maintenance of neural circuits is crucial for proper brain function. Although the assembly of brain circuits has been extensively studied, much less is understood about the mechanisms controlling their maintenance as animals mature. In the olfactory system, the axons of olfactory sensory neurons (OSNs) expressing the same odor receptor converge into discrete synaptic structures of the olfactory bulb (OB) called glomeruli, forming a stereotypic odor map. The OB projection neurons, called mitral and tufted cells (M/Ts), have a single dendrite that branches into a single glomerulus, where they make synapses with OSNs. We used a genetic method to progressively eliminate the vast majority of M/T cells in early postnatal mice, and observed that the assembly of the OB bulb circuits proceeded normally. However, as the animals became adults the apical dendrite of remaining M/Ts grew multiple branches that innervated several glomeruli, and OSNs expressing single odor receptors projected their axons into multiple glomeruli, disrupting the olfactory sensory map. Moreover, ablating the M/Ts in adult animals also resulted in similar structural changes in the projections of remaining M/Ts and axons from OSNs. Interestingly, the ability of these mice to detect odors was relatively preserved despite only having 1–5% of projection neurons transmitting odorant information to the brain, and having highly disrupted circuits in the OB. These results indicate that a reduced number of projection neurons does not affect the normal assembly of the olfactory circuit, but induces structural instability of the olfactory circuitry of adult animals.

    1. Neuroscience
    GVS Devakinandan, Mark Terasaki, Adish Dani
    Research Article

    Specialized chemosensory signals elicit innate social behaviors in individuals of several vertebrate species, a process that is mediated via the accessory olfactory system (AOS). The AOS comprising the peripheral sensory vomeronasal organ has evolved elaborate molecular and cellular mechanisms to detect chemo signals. To gain insight into the cell types, developmental gene expression patterns, and functional differences amongst neurons, we performed single-cell transcriptomics of the mouse vomeronasal sensory epithelium. Our analysis reveals diverse cell types with gene expression patterns specific to each, which we made available as a searchable web resource accessed from https://www.scvnoexplorer.com. Pseudo-time developmental analysis indicates that neurons originating from common progenitors diverge in their gene expression during maturation with transient and persistent transcription factor expression at critical branch points. Comparative analysis across two of the major neuronal subtypes that express divergent GPCR families and the G-protein subunits Gnai2 or Gnao1, reveals significantly higher expression of endoplasmic reticulum (ER) associated genes within Gnao1 neurons. In addition, differences in ER content and prevalence of cubic membrane ER ultrastructure revealed by electron microscopy, indicate fundamental differences in ER function.