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A modular theory of multisensory integration for motor control

To control targeted movements, such as reaching to grasp an object or hammering a nail, the brain can use divers sources of sensory information, such as vision and proprioception. Although a variety of studies have shown that sensory signals are optimally combined according to principles of maximum...

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Autores principales: Tagliabue, Michele, McIntyre, Joseph
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3908447/
https://www.ncbi.nlm.nih.gov/pubmed/24550816
http://dx.doi.org/10.3389/fncom.2014.00001
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author Tagliabue, Michele
McIntyre, Joseph
author_facet Tagliabue, Michele
McIntyre, Joseph
author_sort Tagliabue, Michele
collection PubMed
description To control targeted movements, such as reaching to grasp an object or hammering a nail, the brain can use divers sources of sensory information, such as vision and proprioception. Although a variety of studies have shown that sensory signals are optimally combined according to principles of maximum likelihood, increasing evidence indicates that the CNS does not compute a single, optimal estimation of the target's position to be compared with a single optimal estimation of the hand. Rather, it employs a more modular approach in which the overall behavior is built by computing multiple concurrent comparisons carried out simultaneously in a number of different reference frames. The results of these individual comparisons are then optimally combined in order to drive the hand. In this article we examine at a computational level two formulations of concurrent models for sensory integration and compare this to the more conventional model of converging multi-sensory signals. Through a review of published studies, both our own and those performed by others, we produce evidence favoring the concurrent formulations. We then examine in detail the effects of additive signal noise as information flows through the sensorimotor system. By taking into account the noise added by sensorimotor transformations, one can explain why the CNS may shift its reliance on one sensory modality toward a greater reliance on another and investigate under what conditions those sensory transformations occur. Careful consideration of how transformed signals will co-vary with the original source also provides insight into how the CNS chooses one sensory modality over another. These concepts can be used to explain why the CNS might, for instance, create a visual representation of a task that is otherwise limited to the kinesthetic domain (e.g., pointing with one hand to a finger on the other) and why the CNS might choose to recode sensory information in an external reference frame.
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spelling pubmed-39084472014-02-18 A modular theory of multisensory integration for motor control Tagliabue, Michele McIntyre, Joseph Front Comput Neurosci Neuroscience To control targeted movements, such as reaching to grasp an object or hammering a nail, the brain can use divers sources of sensory information, such as vision and proprioception. Although a variety of studies have shown that sensory signals are optimally combined according to principles of maximum likelihood, increasing evidence indicates that the CNS does not compute a single, optimal estimation of the target's position to be compared with a single optimal estimation of the hand. Rather, it employs a more modular approach in which the overall behavior is built by computing multiple concurrent comparisons carried out simultaneously in a number of different reference frames. The results of these individual comparisons are then optimally combined in order to drive the hand. In this article we examine at a computational level two formulations of concurrent models for sensory integration and compare this to the more conventional model of converging multi-sensory signals. Through a review of published studies, both our own and those performed by others, we produce evidence favoring the concurrent formulations. We then examine in detail the effects of additive signal noise as information flows through the sensorimotor system. By taking into account the noise added by sensorimotor transformations, one can explain why the CNS may shift its reliance on one sensory modality toward a greater reliance on another and investigate under what conditions those sensory transformations occur. Careful consideration of how transformed signals will co-vary with the original source also provides insight into how the CNS chooses one sensory modality over another. These concepts can be used to explain why the CNS might, for instance, create a visual representation of a task that is otherwise limited to the kinesthetic domain (e.g., pointing with one hand to a finger on the other) and why the CNS might choose to recode sensory information in an external reference frame. Frontiers Media S.A. 2014-01-31 /pmc/articles/PMC3908447/ /pubmed/24550816 http://dx.doi.org/10.3389/fncom.2014.00001 Text en Copyright © 2014 Tagliabue and McIntyre. http://creativecommons.org/licenses/by/3.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Tagliabue, Michele
McIntyre, Joseph
A modular theory of multisensory integration for motor control
title A modular theory of multisensory integration for motor control
title_full A modular theory of multisensory integration for motor control
title_fullStr A modular theory of multisensory integration for motor control
title_full_unstemmed A modular theory of multisensory integration for motor control
title_short A modular theory of multisensory integration for motor control
title_sort modular theory of multisensory integration for motor control
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3908447/
https://www.ncbi.nlm.nih.gov/pubmed/24550816
http://dx.doi.org/10.3389/fncom.2014.00001
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