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.
Highlights
Manual dexterity is highly specialized in humans (Lemon, 2008)
If we assume that the cross-reference transformations from the left and right arm joints are characterized by the same variance, the optimal sensory weighting predicted by Maximum Likelihood Principle (MLP) (Figure 4B), consists in encoding the position of the two hands perceived through proprioception in alternative reference frames, including the retinal one, rather than in joint space
Using a theoretical approach, based on statistical models of optimal multi-sensory integration, we have reinterpreted post-stroke proprioceptive deficits, as well as the ability of patients to visually compensate for their deficit
Summary
Manual dexterity is highly specialized in humans (Lemon, 2008). Multimodal information from different sensory systems need to be combined to optimally control hand movements. If we assume that the cross-reference transformations from the left and right arm joints are characterized by the same variance (σJ2l→ExJ = σJ2r→ExJ and σJ2l→R = σJ2r→R), the optimal sensory weighting predicted by MLP (Figure 4B), consists in encoding the position of the two hands perceived through proprioception in alternative reference frames, including the retinal one, rather than in joint space This prediction is consistent with experimental observations on healthy subjects suggesting that retinal and external references contribute to the encoding of asymmetric between-arm tasks (Pouget et al, 2002; McGuire and Sabes, 2009; Jones and Henriques, 2010; Tagliabue and McIntyre, 2013; Arnoux et al, 2017). Within PPC from inferior-lateral to more superior-medial activation with increasing cross-reference processing demands
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