Predicting proprioceptive cortical anatomy and neural coding with topographic autoencoders.

Proprioception is one of the least understood senses, yet fundamental for the control of movement. Even basic questions of how limb pose is represented in the somatosensory cortex are unclear. We developed a topographic variational autoencoder with lateral connectivity (topo-VAE) to compute a putati...

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Main Authors: Max Grogan, Kyle P Blum, Yufei Wu, J Alex Harston, Lee E Miller, A Aldo Faisal
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2024-12-01
Series:PLoS Computational Biology
Online Access:https://doi.org/10.1371/journal.pcbi.1012614
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author Max Grogan
Kyle P Blum
Yufei Wu
J Alex Harston
Lee E Miller
A Aldo Faisal
author_facet Max Grogan
Kyle P Blum
Yufei Wu
J Alex Harston
Lee E Miller
A Aldo Faisal
author_sort Max Grogan
collection DOAJ
description Proprioception is one of the least understood senses, yet fundamental for the control of movement. Even basic questions of how limb pose is represented in the somatosensory cortex are unclear. We developed a topographic variational autoencoder with lateral connectivity (topo-VAE) to compute a putative cortical map from a large set of natural movement data. Although not fitted to neural data, our model reproduces two sets of observations from monkey centre-out reaching: 1. The shape and velocity dependence of proprioceptive receptive fields in hand-centered coordinates despite the model having no knowledge of arm kinematics or hand coordinate systems. 2. The distribution of neuronal preferred directions (PDs) recorded from multi-electrode arrays. The model makes several testable predictions: 1. Encoding across the cortex has a blob-and-pinwheel-type geometry of PDs. 2. Few neurons will encode just a single joint. Our model provides a principled basis for understanding of sensorimotor representations, and the theoretical basis of neural manifolds, with applications to the restoration of sensory feedback in brain-computer interfaces and the control of humanoid robots.
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spelling doaj-art-fade427cc19b48c8a770441abdad54ae2025-08-20T02:37:06ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582024-12-012012e101261410.1371/journal.pcbi.1012614Predicting proprioceptive cortical anatomy and neural coding with topographic autoencoders.Max GroganKyle P BlumYufei WuJ Alex HarstonLee E MillerA Aldo FaisalProprioception is one of the least understood senses, yet fundamental for the control of movement. Even basic questions of how limb pose is represented in the somatosensory cortex are unclear. We developed a topographic variational autoencoder with lateral connectivity (topo-VAE) to compute a putative cortical map from a large set of natural movement data. Although not fitted to neural data, our model reproduces two sets of observations from monkey centre-out reaching: 1. The shape and velocity dependence of proprioceptive receptive fields in hand-centered coordinates despite the model having no knowledge of arm kinematics or hand coordinate systems. 2. The distribution of neuronal preferred directions (PDs) recorded from multi-electrode arrays. The model makes several testable predictions: 1. Encoding across the cortex has a blob-and-pinwheel-type geometry of PDs. 2. Few neurons will encode just a single joint. Our model provides a principled basis for understanding of sensorimotor representations, and the theoretical basis of neural manifolds, with applications to the restoration of sensory feedback in brain-computer interfaces and the control of humanoid robots.https://doi.org/10.1371/journal.pcbi.1012614
spellingShingle Max Grogan
Kyle P Blum
Yufei Wu
J Alex Harston
Lee E Miller
A Aldo Faisal
Predicting proprioceptive cortical anatomy and neural coding with topographic autoencoders.
PLoS Computational Biology
title Predicting proprioceptive cortical anatomy and neural coding with topographic autoencoders.
title_full Predicting proprioceptive cortical anatomy and neural coding with topographic autoencoders.
title_fullStr Predicting proprioceptive cortical anatomy and neural coding with topographic autoencoders.
title_full_unstemmed Predicting proprioceptive cortical anatomy and neural coding with topographic autoencoders.
title_short Predicting proprioceptive cortical anatomy and neural coding with topographic autoencoders.
title_sort predicting proprioceptive cortical anatomy and neural coding with topographic autoencoders
url https://doi.org/10.1371/journal.pcbi.1012614
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