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Published May 9, 2022 | Supplemental Material + Published
Journal Article Open

Implicit mechanisms of intention

Abstract

High-level cortical regions encode motor decisions before or even absent awareness, suggesting that neural processes predetermine behavior before conscious choice. Such early neural encoding challenges popular conceptions of human agency. It also raises fundamental questions for brain-machine interfaces (BMIs) that traditionally assume that neural activity reflects the user's conscious intentions. Here, we study the timing of human posterior parietal cortex single-neuron activity recorded from implanted microelectrode arrays relative to the explicit urge to initiate movement. Participants were free to choose when to move, whether to move, and what to move, and they retrospectively reported the time they felt the urge to move. We replicate prior studies by showing that posterior parietal cortex (PPC) neural activity sharply rises hundreds of milliseconds before the reported urge. However, we find that this "preconscious" activity is part of a dynamic neural population response that initiates much earlier, when the participant first chooses to perform the task. Together with details of neural timing, our results suggest that PPC encodes an internal model of the motor planning network that transforms high-level task objectives into appropriate motor behavior. These new data challenge traditional interpretations of early neural activity and offer a more holistic perspective on the interplay between choice, behavior, and their neural underpinnings. Our results have important implications for translating BMIs into more complex real-world environments. We find that early neural dynamics are sufficient to drive BMI movements before the participant intends to initiate movement. Appropriate algorithms ensure that BMI movements align with the subject's awareness of choice.

Additional Information

© 2022 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Received 6 August 2021, Revised 3 February 2022, Accepted 15 March 2022, Available online 6 April 2022. We thank N.S. and E.S. for their bravery and hard work in making this work possible. This work was funded by NIH R01-EY015545, UG1-EY032039, the Della Martin Foundation, and the Boswell Foundation. Author contributions. T.A. designed experiments with assistance from R.A.A., B.R., and C.Z. T.A., B.R., and C.Z. collected data. N.P. performed the surgery on N.S. T.A. analyzed the data. T.A. wrote the paper. T.A. and R.A.A. revised the paper. Data and code availability: • The data that support the findings of this study are available from the lead contact upon reasonable request. • This paper does not report original code, but our custom MATLAB code is available from the authors upon reasonable request. • Any additional information required to reanalyze the data reported in this paper is available from the lead contact upon request. Declaration of interests. N.P. consults for Second Sight Medical Products and Abbott Laboratories. All other authors declare that they have no conflicts of interest.

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Supplemental Material - 1-s2.0-S0960982222004420-mmc1.pdf

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Additional details

Created:
August 22, 2023
Modified:
December 22, 2023