Stability of motor representations after paralysis
- California Institute of Technology, United States
- University College London, United Kingdom
- Casa Colina Hospital and Centers for Healthcare, United States
- 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
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PPC_Finger: human posterior parietal cortex recordings during attempted finger movementsDANDI Archive Identifier: 000147.
Article and author information
Author details
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.
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Stability of motor representations after paralysis
eLife 11:e74478.
https://doi.org/10.7554/eLife.74478
Further reading
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- Neuroscience
Experience-based plasticity of the human cortex mediates the influence of individual experience on cognition and behavior. The complete loss of a sensory modality is among the most extreme such experiences. Investigating such a selective, yet extreme change in experience allows for the characterization of experience-based plasticity at its boundaries. Here, we investigated information processing in individuals who lost vision at birth or early in life by probing the processing of braille letter information. We characterized the transformation of braille letter information from sensory representations depending on the reading hand to perceptual representations that are independent of the reading hand. Using a multivariate analysis framework in combination with functional magnetic resonance imaging (fMRI), electroencephalography (EEG), and behavioral assessment, we tracked cortical braille representations in space and time, and probed their behavioral relevance. We located sensory representations in tactile processing areas and perceptual representations in sighted reading areas, with the lateral occipital complex as a connecting ‘hinge’ region. This elucidates the plasticity of the visually deprived brain in terms of information processing. Regarding information processing in time, we found that sensory representations emerge before perceptual representations. This indicates that even extreme cases of brain plasticity adhere to a common temporal scheme in the progression from sensory to perceptual transformations. Ascertaining behavioral relevance through perceived similarity ratings, we found that perceptual representations in sighted reading areas, but not sensory representations in tactile processing areas are suitably formatted to guide behavior. Together, our results reveal a nuanced picture of both the potentials and limits of experience-dependent plasticity in the visually deprived brain.
