Task-driven neural network models predict neural dynamics of proprioception.

biomechanics cuneate nucleus efference copy goal-driven models neural networks proprioception somatosensory cortex state estimation statistics of movement task-driven models

Journal

Cell
ISSN: 1097-4172
Titre abrégé: Cell
Pays: United States
ID NLM: 0413066

Informations de publication

Date de publication:
18 Mar 2024
Historique:
received: 14 06 2023
revised: 06 12 2023
accepted: 27 02 2024
medline: 23 3 2024
pubmed: 23 3 2024
entrez: 22 3 2024
Statut: aheadofprint

Résumé

Proprioception tells the brain the state of the body based on distributed sensory neurons. Yet, the principles that govern proprioceptive processing are poorly understood. Here, we employ a task-driven modeling approach to investigate the neural code of proprioceptive neurons in cuneate nucleus (CN) and somatosensory cortex area 2 (S1). We simulated muscle spindle signals through musculoskeletal modeling and generated a large-scale movement repertoire to train neural networks based on 16 hypotheses, each representing different computational goals. We found that the emerging, task-optimized internal representations generalize from synthetic data to predict neural dynamics in CN and S1 of primates. Computational tasks that aim to predict the limb position and velocity were the best at predicting the neural activity in both areas. Since task optimization develops representations that better predict neural activity during active than passive movements, we postulate that neural activity in the CN and S1 is top-down modulated during goal-directed movements.

Identifiants

pubmed: 38518772
pii: S0092-8674(24)00239-3
doi: 10.1016/j.cell.2024.02.036
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright © 2024 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Auteurs

Alessandro Marin Vargas (A)

Brain Mind Institute, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne (EPFL), 1015 Lausanne, Switzerland; NeuroX Institute, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne (EPFL), 1015 Lausanne, Switzerland.

Axel Bisi (A)

Brain Mind Institute, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne (EPFL), 1015 Lausanne, Switzerland; NeuroX Institute, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne (EPFL), 1015 Lausanne, Switzerland.

Alberto S Chiappa (AS)

Brain Mind Institute, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne (EPFL), 1015 Lausanne, Switzerland; NeuroX Institute, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne (EPFL), 1015 Lausanne, Switzerland.

Chris Versteeg (C)

Department of Neuroscience, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611, USA; Department of Physical Medicine and Rehabilitation, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611, USA; Department of Biomedical Engineering, McCormick School of Engineering, Northwestern University, Evanston, IL 60208, USA; Shirley Ryan AbilityLab, Chicago, IL 60611, USA.

Lee E Miller (LE)

Department of Neuroscience, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611, USA; Department of Physical Medicine and Rehabilitation, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611, USA; Department of Biomedical Engineering, McCormick School of Engineering, Northwestern University, Evanston, IL 60208, USA; Shirley Ryan AbilityLab, Chicago, IL 60611, USA.

Alexander Mathis (A)

Brain Mind Institute, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne (EPFL), 1015 Lausanne, Switzerland; NeuroX Institute, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne (EPFL), 1015 Lausanne, Switzerland. Electronic address: alexander.mathis@epfl.ch.

Classifications MeSH