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

Abstract

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.

How Tilting the Head Interferes With Eye-Hand Coordination: The Role of Gravity in Visuo-Proprioceptive, Cross-Modal Sensory Transformations

“…To try to formalize and quantify these predictions we applied an optimal theory of multi-sensory integration to the above-described task. This statistical model, in which the task is concurrently represented in the visual and proprioceptive space ( Tagliabue and McIntyre, 2008 , 2011 , 2012 , 2013 , 2014 ; McGuire and Sabes, 2009 ; Tagliabue et al, 2013 ; Arnoux et al, 2017 ; Bernard-Espina et al, 2021 ) allowed to compute the effects of changing posture in terms of subjects’ responses variability and in terms of the relative importance given to the visual and proprioceptive encoding of the information.…”

“…In order to compare the Neck and Gravity Hypotheses predictions with the measured subjects’ precision and sensory weighting, we applied our “ Concurrent Model ” (see below) of multisensory integration ( Tagliabue and McIntyre, 2008 , 2011 , 2012 , 2013 , 2014 ; Tagliabue et al, 2013 ; Arnoux et al, 2017 ; Bernard-Espina et al, 2021 ) to the cross- and uni-modal tasks tested here.…”

Somesthetic, Visual, and Auditory Feedback and Their Interactions Applied to Upper Limb Neurorehabilitation Technology: A Narrative Review to Facilitate Contextualization of Knowledge

“…However, adequately assessing deficits may be challenging. For example, touch and proprioception deficits are often missed due to a lack of consensus in clinical assessment methods, and can lead to errors in diagnosis ( 151 ) and inappropriate care. Vision and proprioception are predominant in the perception of spatial information, while hearing is useful in the perception of temporal information related to the periodicity, regularity, and speed of motion.…”

Efficacy of Multisensory Technology in Post-Stroke Cognitive Rehabilitation: A Systematic Review

“…As a result, brain lesions affecting MSI processing can cause various problems such as feeling hyperactivated by sensory stimuli or having difficulty effectively integrating different sensory information (e.g., visual and auditory). For example, to move hands accurately, information from different sensory systems must be combined (e.g., visual, proprioceptive, and tactile systems) [ 18 ]. Originally, MSI was thought to be a process primarily controlled by bottom-up functions, but several studies have found that the multisensory integration process is also strongly linked to top-down processes, involving memory and attention [ 19 , 20 ].…”