1. Neuroscience

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
https://doi.org/10.7554/eLife.74478
Share this article
Cite this article
  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
  2. Download BibTeX
  3. Download .RIS

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.

Reviewing Editor

  1. Jörn Diedrichsen, Western University, Canada

Publication history

  1. Received: October 6, 2021
  2. Preprint posted: October 9, 2021 (view preprint)
  3. Accepted: August 27, 2022
  4. Accepted Manuscript published: September 20, 2022 (version 1)
  5. Version of Record published: October 12, 2022 (version 2)

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

  • 835
    Page views
  • 215
    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)

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

Categories and tags

Research organism

Further reading

    1. Neuroscience

    Distinct roles of forward and backward alpha-band waves in spatial visual attention

    Andrea Alamia, Lucie Terral ... Rufin VanRullen
    Research Article Updated

    Previous research has associated alpha-band [8–12 Hz] oscillations with inhibitory functions: for instance, several studies showed that visual attention increases alpha-band power in the hemisphere ipsilateral to the attended location. However, other studies demonstrated that alpha oscillations positively correlate with visual perception, hinting at different processes underlying their dynamics. Here, using an approach based on traveling waves, we demonstrate that there are two functionally distinct alpha-band oscillations propagating in different directions. We analyzed EEG recordings from three datasets of human participants performing a covert visual attention task (one new dataset with N = 16, two previously published datasets with N = 16 and N = 31). Participants were instructed to detect a brief target by covertly attending to the screen’s left or right side. Our analysis reveals two distinct processes: allocating attention to one hemifield increases top-down alpha-band waves propagating from frontal to occipital regions ipsilateral to the attended location, both with and without visual stimulation. These top-down oscillatory waves correlate positively with alpha-band power in frontal and occipital regions. Yet, different alpha-band waves propagate from occipital to frontal regions and contralateral to the attended location. Crucially, these forward waves were present only during visual stimulation, suggesting a separate mechanism related to visual processing. Together, these results reveal two distinct processes reflected by different propagation directions, demonstrating the importance of considering oscillations as traveling waves when characterizing their functional role.

    1. Developmental Biology
    2. Neuroscience

    Origin of wiring specificity in an olfactory map revealed by neuron type-specific, time-lapse imaging of dendrite targeting

    Kenneth Kin Lam Wong, Tongchao Li ... Liqun Luo
    Research Article

    How does wiring specificity of neural maps emerge during development? Formation of the adult Drosophila olfactory glomerular map begins with patterning of projection neuron (PN) dendrites at the early pupal stage. To better understand the origin of wiring specificity of this map, we created genetic tools to systematically characterize dendrite patterning across development at PN type-specific resolution. We find that PNs use lineage and birth order combinatorially to build the initial dendritic map. Specifically, birth order directs dendrite targeting in rotating and binary manners for PNs of the anterodorsal and lateral lineages, respectively. Two-photon- and adaptive optical lattice light-sheet microscope-based time-lapse imaging reveals that PN dendrites initiate active targeting with direction-dependent branch stabilization on the timescale of seconds. Moreover, PNs that are used in both the larval and adult olfactory circuits prune their larval-specific dendrites and re-extend new dendrites simultaneously to facilitate timely olfactory map organization. Our work highlights the power and necessity of type-specific neuronal access and time-lapse imaging in identifying wiring mechanisms that underlie complex patterns of functional neural maps.

    1. Neuroscience

    Generative network modeling reveals quantitative definitions of bilateral symmetry exhibited by a whole insect brain connectome

    Benjamin D Pedigo, Mike Powell ... Joshua T Vogelstein
    Research Article

    Comparing connectomes can help explain how neural connectivity is related to genetics, disease, development, learning, and behavior. However, making statistical inferences about the significance and nature of differences between two networks is an open problem, and such analysis has not been extensively applied to nanoscale connectomes. Here, we investigate this problem via a case study on the bilateral symmetry of a larval Drosophila brain connectome. We translate notions of'bilateral symmetry' to generative models of the network structure of the left and right hemispheres, allowing us to test and refine our understanding of symmetry. We find significant differences in connection probabilities both across the entire left and right networks and between specific cell types. By rescaling connection probabilities or removing certain edges based on weight, we also present adjusted definitions of bilateral symmetry exhibited by this connectome. This work shows how statistical inferences from networks can inform the study of connectomes, facilitating future comparisons of neural structures.