Multisensory Integration in Stroke Patients: A Theoretical Approach to Reinterpret Upper-Limb Proprioceptive Deficits and Visual Compensation

For reaching and grasping, as well as for manipulating objects, optimal hand motor control arises from the integration of multiple sources of sensory information, such as proprioception and vision. For this reason, proprioceptive deficits often observed in stroke patients have a significant impact o...

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Main Authors: Jules Bernard-Espina, Mathieu Beraneck, Marc A. Maier, Michele Tagliabue
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-04-01
Series:Frontiers in Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnins.2021.646698/full
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author Jules Bernard-Espina
Mathieu Beraneck
Marc A. Maier
Michele Tagliabue
author_facet Jules Bernard-Espina
Mathieu Beraneck
Marc A. Maier
Michele Tagliabue
author_sort Jules Bernard-Espina
collection DOAJ
description For reaching and grasping, as well as for manipulating objects, optimal hand motor control arises from the integration of multiple sources of sensory information, such as proprioception and vision. For this reason, proprioceptive deficits often observed in stroke patients have a significant impact on the integrity of motor functions. The present targeted review attempts to reanalyze previous findings about proprioceptive upper-limb deficits in stroke patients, as well as their ability to compensate for these deficits using vision. Our theoretical approach is based on two concepts: first, the description of multi-sensory integration using statistical optimization models; second, on the insight that sensory information is not only encoded in the reference frame of origin (e.g., retinal and joint space for vision and proprioception, respectively), but also in higher-order sensory spaces. Combining these two concepts within a single framework appears to account for the heterogeneity of experimental findings reported in the literature. The present analysis suggests that functional upper limb post-stroke deficits could not only be due to an impairment of the proprioceptive system per se, but also due to deficiencies of cross-references processing; that is of the ability to encode proprioceptive information in a non-joint space. The distinction between purely proprioceptive or cross-reference-related deficits can account for two experimental observations: first, one and the same patient can perform differently depending on specific proprioceptive assessments; and a given behavioral assessment results in large variability across patients. The distinction between sensory and cross-reference deficits is also supported by a targeted literature review on the relation between cerebral structure and proprioceptive function. This theoretical framework has the potential to lead to a new stratification of patients with proprioceptive deficits, and may offer a novel approach to post-stroke rehabilitation.
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spelling doaj.art-93e22f98195740ffb13b03daed4c39872022-12-21T17:17:02ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2021-04-011510.3389/fnins.2021.646698646698Multisensory Integration in Stroke Patients: A Theoretical Approach to Reinterpret Upper-Limb Proprioceptive Deficits and Visual CompensationJules Bernard-EspinaMathieu BeraneckMarc A. MaierMichele TagliabueFor reaching and grasping, as well as for manipulating objects, optimal hand motor control arises from the integration of multiple sources of sensory information, such as proprioception and vision. For this reason, proprioceptive deficits often observed in stroke patients have a significant impact on the integrity of motor functions. The present targeted review attempts to reanalyze previous findings about proprioceptive upper-limb deficits in stroke patients, as well as their ability to compensate for these deficits using vision. Our theoretical approach is based on two concepts: first, the description of multi-sensory integration using statistical optimization models; second, on the insight that sensory information is not only encoded in the reference frame of origin (e.g., retinal and joint space for vision and proprioception, respectively), but also in higher-order sensory spaces. Combining these two concepts within a single framework appears to account for the heterogeneity of experimental findings reported in the literature. The present analysis suggests that functional upper limb post-stroke deficits could not only be due to an impairment of the proprioceptive system per se, but also due to deficiencies of cross-references processing; that is of the ability to encode proprioceptive information in a non-joint space. The distinction between purely proprioceptive or cross-reference-related deficits can account for two experimental observations: first, one and the same patient can perform differently depending on specific proprioceptive assessments; and a given behavioral assessment results in large variability across patients. The distinction between sensory and cross-reference deficits is also supported by a targeted literature review on the relation between cerebral structure and proprioceptive function. This theoretical framework has the potential to lead to a new stratification of patients with proprioceptive deficits, and may offer a novel approach to post-stroke rehabilitation.https://www.frontiersin.org/articles/10.3389/fnins.2021.646698/fullstrokeeye-hand coordinationmaximum likelihood principlevisual compensationproprioception assessmentmultisensory integration
spellingShingle Jules Bernard-Espina
Mathieu Beraneck
Marc A. Maier
Michele Tagliabue
Multisensory Integration in Stroke Patients: A Theoretical Approach to Reinterpret Upper-Limb Proprioceptive Deficits and Visual Compensation
Frontiers in Neuroscience
stroke
eye-hand coordination
maximum likelihood principle
visual compensation
proprioception assessment
multisensory integration
title Multisensory Integration in Stroke Patients: A Theoretical Approach to Reinterpret Upper-Limb Proprioceptive Deficits and Visual Compensation
title_full Multisensory Integration in Stroke Patients: A Theoretical Approach to Reinterpret Upper-Limb Proprioceptive Deficits and Visual Compensation
title_fullStr Multisensory Integration in Stroke Patients: A Theoretical Approach to Reinterpret Upper-Limb Proprioceptive Deficits and Visual Compensation
title_full_unstemmed Multisensory Integration in Stroke Patients: A Theoretical Approach to Reinterpret Upper-Limb Proprioceptive Deficits and Visual Compensation
title_short Multisensory Integration in Stroke Patients: A Theoretical Approach to Reinterpret Upper-Limb Proprioceptive Deficits and Visual Compensation
title_sort multisensory integration in stroke patients a theoretical approach to reinterpret upper limb proprioceptive deficits and visual compensation
topic stroke
eye-hand coordination
maximum likelihood principle
visual compensation
proprioception assessment
multisensory integration
url https://www.frontiersin.org/articles/10.3389/fnins.2021.646698/full
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