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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.

SUBMITTER: Bernard-Espina J

PROVIDER: S-EPMC8058201 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundThe use of wearable sensor technology (e.g., accelerometers) for tracking human physical activity have allowed for measurement of actual activity performance of the upper limb (UL) in daily life. Data extracted from accelerometers can be used to quantify multiple variables measuring different aspects of UL performance in one or both limbs. A limitation is that several variables are needed to understand the complexity of UL performance in daily life.PurposeTo identify categories of UL performance in daily life in adults with and without neurological UL deficits.MethodsThis study analyzed data extracted from bimanual, wrist-worn triaxial accelerometers from adults from three previous cohorts (N=211), two samples of persons with stroke and one sample from neurologically intact adult controls. Data used in these analyses were UL performance variables calculated from accelerometer data, associated clinical measures, and participant characteristics. A total of twelve cluster solutions (3-, 4- or 5-clusters based with 12, 9, 7, or 5 input variables) were calculated to systematically evaluate the most parsimonious solution. Quality metrics and principal component analysis of each solution were calculated to arrive at a locally-optimal solution with respect to number of input variables and number of clusters.ResultsAcross different numbers of input variables, two principal components consistently explained the most variance. Across the models with differing numbers of UL input performance variables, a 5-cluster solution explained the most overall total variance (79%) and had the best model-fit.ConclusionThe present study identified 5 categories of UL performance formed from 5 UL performance variables in cohorts with and without neurological UL deficits. Further validation of both the number of UL performance variables and categories will be required on a larger, more heterogeneous sample. Following validation, these categories may be used as outcomes in UL stroke research and implemented into rehabilitation clinical practice.

Project description:The brain generally integrates a multitude of sensory signals to form a unified percept. Even in cursor control tasks, such as reaching while looking at rotated visual feedback on a monitor, visual information on cursor position and proprioceptive information on hand position are partially integrated (sensory coupling), resulting in mutual biases of the perceived positions of cursor and hand. Previous studies showed that the strength of sensory coupling (sum of the mutual biases) depends on the experience of kinematic correlations between hand movements and cursor motions, whereas the asymmetry of sensory coupling (difference between the biases) depends on the relative reliabilities (inverse of variability) of hand-position and cursor-position estimates (reliability rule). Furthermore, the precision of movement control and perception of hand position are known to differ between hands (left, right) and workspaces (ipsilateral, contralateral), and so does the experience of kinematic correlations from daily life activities. Thus, in the present study, we tested whether strength and asymmetry of sensory coupling for the endpoints of reaches in a cursor control task differ between the right and left hand and between ipsilateral and contralateral hemispace. No differences were found in the strength of sensory coupling between hands or between hemispaces. However, asymmetry of sensory coupling was less in ipsilateral than in contralateral hemispace: in ipsilateral hemispace, the bias of the perceived hand position was reduced, which was accompanied by a smaller variability of the estimates. The variability of position estimates of the dominant right hand was also less than for the non-dominant left hand, but this difference was not accompanied by a difference in the asymmetry of sensory coupling - a violation of the reliability rule, probably due a stronger influence of visual information on right-hand movements. According to these results, the long-term effects of the experienced kinematic correlation between hand movements and cursor motions on the strength of sensory coupling are generic and not specific for hemispaces or hands, whereas the effects of relative reliabilities on the asymmetry of sensory coupling are specific for hemispaces but not for hands.

Project description:BackgroundProprioception refers to the perception of motion and position of the body or body segments in space. A wide range of proprioceptive tests exists, although tests dynamically evaluating sensorimotor integration during upper limb movement are scarce. We introduce a novel task to evaluate kinesthetic proprioceptive function during complex upper limb movements using a robotic device. We aimed to evaluate the test-retest reliability of this newly developed Dynamic Movement Reproduction (DMR) task. Furthermore, we assessed reliability of the commonly used Joint Reposition (JR) task of the elbow, evaluated the association between both tasks, and explored the influence of visual information (viewing arm movement or not) on performance during both tasks.MethodsDuring the DMR task, participants actively reproduced movement patterns while holding a handle attached to the robotic arm, with the device encoding actual position throughout movement. In the JR task, participants actively reproduced forearm positions; with the final arm position evaluated using an angle measurement tool. The difference between target movement pattern/position and reproduced movement pattern/position served as measures of accuracy. In study 1 (N = 23), pain-free participants performed both tasks at two test sessions, 24-h apart, both with and without visual information available (i.e., vision occluded using a blindfold). In study 2 (N = 64), an independent sample of pain-free participants performed the same tasks in a single session to replicate findings regarding the association between both tasks and the influence of visual information.ResultsThe DMR task accuracy showed good-to-excellent test-retest reliability, while JR task reliability was poor: measurements did not remain sufficiently stable over testing days. The DMR and JR tasks were only weakly associated. Adding visual information (i.e., watching arm movement) had different performance effects on the tasks: it increased JR accuracy but decreased DMR accuracy, though only when the DMR task started with visual information available (i.e., an order effect).DiscussionThe DMR task's highly standardized protocol (i.e., largely automated), precise measurement and involvement of the entire upper limb kinetic chain (i.e., shoulder, elbow and wrist joints) make it a promising tool. Moreover, the poor association between the JR and DMR tasks indicates that they likely capture unique aspects of proprioceptive function. While the former mainly captures position sense, the latter appears to capture sensorimotor integration processes underlying kinesthesia, largely independent of position sense. Finally, our results show that the integration of visual and proprioceptive information is not straightforward: additional visual information of arm movement does not necessarily make active movement reproduction more accurate, on the contrary, when movement is complex, vision appears to make it worse.

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

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