Proprioception and Motor Control in Parkinson's Disease

ABSTRACT

Parkinson's disease (PD) is a neurodegenerative disorder that leads to a progressive decline in motor function. Growing evidence indicates that PD patients also experience an array of sensory problems that negatively impact motor function. This is especially true for proprioceptive deficits, which profoundly degrade motor performance. This review specifically address the relation between proprioception and motor impairments in PD. It is structured around 4 themes: (a) It examines whether the sensitivity of kinaesthetic perception, which is based on proprioceptive inputs, is actually altered in PD. (b) It discusses whether failed processes of proprioceptive-motor integration are central to the motor problems in PD. (c) It presents recent findings focusing on the link between the proprioception and the balance problems in PD. And (d) it discusses the current state of knowledge of how levodopa medication and deep brain stimulation affect proprioceptive and motor function in PD. The authors conclude that a failure to evaluate and to map proprioceptive information onto voluntary and reflexive motor commands is an integral part of the observed motor symptoms in PD.     

The case for proprioception

In formulating a theory of perception that does justice to the embodied and enactive nature of perceptual experience, proprioception can play a valuable role. Since proprioception is necessarily embodied, and since proprioceptive experience is particularly integrated with one’s bodily actions, it seems clear that proprioception, in addition to, e.g., vision or audition, can provide us with valuable insights into the role of an agent’s corporal skills and capacities in constituting or structuring perceptual experience. However, if we are going to have the opportunity to argue from analogy with proprioception to vision, audition, touch, taste, or smell, then it is necessary to eschew any doubts about the legitimacy of proprioception’s inclusion into the category of perceptual modalities. To this end, in this article, I (1) respond to two arguments that Shaun Gallagher (2003) presents in “Bodily self-awareness and objectperception” against proprioception’s ability to meet the criteria of object perception, (2) present a diagnosis of Gallagher’s position by locating a misunderstanding in the distinction between proprioceptive information and proprioceptive awareness, and (3) show that treating proprioception as a perceptual modality allows us to account for the interaction of proprioception with the other sensory modalities, to apply the lessons we learn from proprioception to the other sensory modalities, and to account for proprioceptive learning. Finally, (4) I examine Sydney Shoemaker’s (1994) identification constraint and suggest that a full-fledged notion of object-hood is unnecessary to ground a theory of perception.     

Prism adaptation changes the subjective proprioceptive localization of the hands

Prism adaptation involves a proprioceptive, a visual and a motor component. As the existing paradigms are not able to distinguish between these three components, the contribution of the proprioceptive component remains unclear. In the current study, a proprioceptive judgement task, in the absence of motor responses, was used to investigate how prism adaptation would specifically influences the felt position of the hands in healthy participants. The task was administered before and after adaptation to left and right displacing prisms using either the left or the right hand during the adaptation procedure. The results appeared to suggest that the prisms induced a drift in the felt position of the hands, although the after‐effect depended on the combination of the pointing hand and the visual deviation induced by prisms. The results are interpreted as in line with the hypothesis of an asymmetrical neural architecture of somatosensory processing. Moreover, the passive proprioception of the hand position revealed different effects of proprioceptive re‐alignment compared to active pointing straight ahead: different mechanisms about how visuo‐proprioceptive discrepancy is resolved were hypothesized.     

Feeling darkness: a visually induced somatosensory illusion

Although the five primary senses have traditionally been thought of as separate, examples of their interactions, as well as the neural substrate possibly underlying them, have been identified. Arm position sense, for example, depends on touch, proprioception, and spatial vision of the limb. It is, however, unknown whether position sense is also influenced by more fundamental, nonspatial visual information. Here, we report an illusion that demonstrates that the position sense of the eyelid partly depends on information regarding the relative illumination reported by the two eyes. When only one eye is dark-adapted and both eyes are exposed to a dim environment, the lid of the light-adapted eye feels closed or "droopy." The effect decreases when covering the eye by hand or a patch, thus introducing tactile information congruent with the interocular difference in vision. This reveals that the integration of vision with touch and proprioception is not restricted to higher-level spatial vision, but is instead a more fundamental aspect of sensory processing than has been previously shown.     

Experiencing the Cross-Sensory Error Signal During Movement Leads to Proprioceptive Recalibration

Abstract

Reaching to targets in a virtual reality environment with misaligned visual feedback of the hand results in changes in movements (visuomotor adaptation) and sense of felt hand position (proprioceptive recalibration). We asked if proprioceptive recalibration arises even when the misalignment between visual and proprioceptive estimates of hand position is only experienced during movement. Participants performed a “shooting task” through the targets with a cursor that was rotated 30° clockwise relative to hand motion. Results revealed that, following training on the shooting task, participants adapted their reaches to all targets by approximately 16° and recalibrated their sense of felt hand position by 8°. Thus, experiencing a sensory misalignment between visual and proprioceptive estimates of hand position during movement leads to proprioceptive recalibration.     

Interactions Between Tactile and Proprioceptive Representations in Haptics

ABSTRACT

Neuroprosthetic limbs, regardless of their sophisticated motor control, require sensory feedback to viably interact with the environment. Toward that aim, the authors examined interrelationships between tactile and proprioceptive sensations. Through human psychophysics experiments, they evaluated error patterns of subjects estimating hand location in a horizontal 2-dimensional workspace under 3 tactile conditions. While tactile cues did not significantly affect the structure of the pattern of errors, touching the workspace reduced estimation errors. During neurophysiological experiments, a macaque grasped textured objects using 2 hand postures. Sensory coding showed dependence on both roughness of the manipulandum and posture. In summary, the authors suggest that tactile sensations underlying haptics are processed in a stable spatial reference frame provided by a proprioceptive system, and that tactile and proprioceptive inputs can be encoded simultaneously by individual cells. Such insights will be useful for providing stable, adaptive sensory feedback for neuroprosthetics.     

Vision and proprioception in simple catching

Articular proprioception is normally considered to provide accurate information about limb position, particularly in ball skills in which the eyes are be occupied with tracking the ball. If this is so, then preventing sight of the catching hand without interfering with visual tracking of the ball should affect the accuracy of catching. The experiment reported here indicates that is not the case. Catching is much less accurate if the hand cannot be seen. The errors made are in positioning of the catching hand, which frequently does not contact the ball. In addition, subjects showed larger changes in the felt length arms after catching without sight of the hand than did those who could hand while catching. Visual information about the position of the hand for catching, and this may be because the proprioceptive system is by vision.     

Multisensory Information in the Control of Complex Motor Actions

ABSTRACT— For many of the complex motor actions we perform, perceptual information is available from several different senses including vision, touch, hearing, and the vestibular system. Here I discuss the use of multisensory information for the control of motor action in three particular domains: aviation, sports, and driving. It is shown that performers in these domains use information from multiple senses—frequently with beneficial effects on performance but sometimes with dangerous consequences. Applied psychologists have taken advantage of our natural tendency to integrate sensory information by designing multimodal displays that compensate for situations in which information from one or more of our senses is unreliable or is unattended due to distraction.     

Modality-constrained statistical learning of tactile, visual, and auditory sequences

The authors investigated the extent to which touch, vision, and audition mediate the processing of statistical regularities within sequential input. Few researchers have conducted rigorous comparisons across sensory modalities; in particular, the sense of touch has been virtually ignored. The current data reveal not only commonalities but also modality constraints affecting statistical learning across the senses. To be specific, the authors found that the auditory modality displayed a quantitative learning advantage compared with vision and touch. In addition, they discovered qualitative learning biases among the senses: Primarily, audition afforded better learning for the final part of input sequences. These findings are discussed in terms of whether statistical learning is likely to consist of a single, unitary mechanism or multiple, modality-constrained ones.     

Visual and proprioceptive representations in spatial memory

It has been shown that spatial information can be acquired from both visual and nonvisual modalities. The present study explored how spatial information from vision and proprioception was represented in memory, investigating orientation dependence of spatial memories acquired through visual and proprioceptive spatial learning. Experiment 1 examined whether visual learning alone and proprioceptive learning alone yielded orientation-dependent spatial memory. Results showed that spatial memories from both types of learning were orientation dependent. Experiment 2 explored how different orientations of the same environment were represented when they were learned visually and proprioceptively. Results showed that both visually and proprioceptively learned orientations were represented in spatial memory, suggesting that participants established two different reference systems based on each type of learning experience and interpreted the environment in terms of these two reference systems. The results provide some initial clues to how different modalities make unique contributions to spatial representations.     

Assessing Proprioception in Children: A Review

Proprioception is the subconscious and conscious awareness of the spatial and mechanical status of the musculoskeletal framework. When working with children with motor delays and sensory integrative dysfunction, occupational therapists routinely assess the client's proprioceptive system. However, currently available assessments for occupational therapists are primarily observer-based and concerns have been raised about the reliability of observer-based assessments of sensation. The author's purpose was to review measures of proprioception currently available to occupational therapists and explore direct measures of proprioception from neuroscience and rehabilitation that can be adapted for pediatric clinical use. Observer-based and direct measurements of proprioception assessments complement each other in meeting clinical needs. A better understanding of both types of evaluation will improve proprioceptive evaluation.     

Visual and Proprioceptive Adaptation of Arm Position in a Virtual Environment

The authors examined the resolution of a discrepancy between visual and proprioceptive estimates of arm position in 10 participants. The participants fixed their right shoulder at 0°, 30°, or 60° of transverse adduction while they viewed a video on a head-mounted display that showed their right arm extended in front of the trunk for 30 min. The perceived arm position more closely approached the seen arm position on the display as the difference between the actual and visually displayed arm positions increased. In the extreme case of a 90° discrepancy, the seen arm position on the display was very gradually perceived as approaching the actual arm position. The magnitude of changes in sensory estimates was larger for proprioception (20%) than for vision (< 10%).     

Balance effects of tactile stimulation at the foot

Balance relies on several types of sensory information, including somatosensory senses such as touch and position sense (proprioception). As these senses decline in older adults, there is a question of whether shoes limit somatosensory feedback from the floor. Textured insoles are designed to stimulate the soles of the feet to enhance tactile feedback. Textured insoles have shown balance benefits in some populations, but it is unclear if such tactile stimulation improves a person's balance even in cushioned athletic shoes, which dampen proprioceptive signals. Here we ask whether tactile vs. proprioceptive cues contribute differently to balance control in the healthy somatosensory system. We assessed balance in 20 healthy young adults under four footwear conditions: cushioned shoes with regular insoles, cushioned shoes with textured insoles, barefoot, and minimalist shoes. Each condition was evaluated using the Y-Balance Test (YBT) and the Balance Error Scoring System (BESS), validated tests of dynamic and static balance, respectively. YBT is a dynamic reaching test performed on one leg. The BESS includes various stance conditions with eyes closed. The results showed that footwear influenced dynamic balance only, with textured insoles leading to significantly better performance than barefoot and minimalist shoes did in the YBT. These results suggest that at least for dynamic balance, balance benefits of tactile stimulation from the textured insoles offset any dampening of proprioception caused by the athletic shoes' cushioning. Future research on how these conditions compare in older adults may lead to improved footwear recommendations to reduce fall risk and injuries for that population.     

Sensory conflict in judgments of spatial direction

Artificial discrepancy was created between information about azimuth coming from different sense modalities. The resolution of this discrepancy was examined for the cases of vision and proprioception, proprioception and audition, and vision and audition. Vision biases proprioceptive and auditory judgments. Proprioception biases auditory judgments and has a small effect on visual judgments. The results suggest that the combinations of sense modalities do not behave as an integrated system and the data are interpreted as indicating that different processes are involved in the resolution of discrepant directional information from different pairs of modalities.     

Tactile selective attention and body posture: assessing the multisensory contributions of vision and proprioception

This study addressed the role of proprioceptive and visual cues to body posture during the deployment of tactile spatial attention. Participants made speeded elevation judgments (up vs. down) to vibrotactile targets presented to the finger or thumb of either hand, while attempting to ignore vibrotactile distractors presented to the opposite hand. The first two experiments established the validity of this paradigm and showed that congruency effects were stronger when the target hand was uncertain (Experiment 1) than when it was certain (Experiment 2). Varying the orientation of the hands revealed that these congruency effects were determined by the position of the target and distractor in external space, and not by the particular skin sites stimulated (Experiment 3). Congruency effects increased as the hands were brought closer together in the dark (Experiment 4), demonstrating the role of proprioceptive input in modulating tactile selective attention. This spatial modulation was also demonstrated when a mirror was used to alter the visually perceived separation between the hands (Experiment 5). These results suggest that tactile, spatially selective attention can operate according to an abstract spatial frame of reference, which is significantly modulated by multisensory contributions from both proprioception and vision.     

Accurate reaching after active but not passive movements of the hand: evidence for forward modeling

Converging behavioral findings support recent models of motor control suggesting that estimates of the future positions of a limb as well as the expected sensory consequences of a planned movement may be derived, in part, from efference copies of motor commands. These estimates are referred to as forward models. However, relatively little behavioral evidence has been obtained for proposed forward models that provide on-line estimates of current position. We report data from a patient (JD) who reached accurately to visualized targets with and without vision of her hand despite substantial proprioceptive loss. Additionally, we administered a double-start reaching test to examine the possibility that efference copy information could be used to estimate current limb position. JD reached accurately, without vision, to a final target after actively reaching to a landmark, but exhibited severely impaired reaching after passive movements to the landmark. This finding suggests that forward modeling of efference copy signals may provide relatively accurate estimates of current limb position for the purpose of motor planning. The possibility that such estimates may also contribute to the awareness of body position and to self-recognition is discussed.     

Repetitive pointing to remembered proprioceptive targets improves 3D hand positioning accuracy

Repetitive pointing movements to remembered proprioceptive targets were investigated to determine whether dynamic proprioception could be used to modify the initial sensorimotor conditions associated with an active definition of the target position. Twelve blindfolded subjects used proprioception to reproduce a self-selected target position as accurately as possible. Ten repetitions for each limb were completed using overhead and scapular plane pointing tasks. A 3D optical tracking system determined hand trajectory start and endpoint positions for each repetition. These positions quantified three-dimensional pointing errors relative to the target position and the initial and preceding movement repetitions, as well as changes in movement direction and extent. Target position and cumulative start position errors were significantly greater than the corresponding preceding movement (inter-repetition) errors, and increased as the trial progressed. In contrast, hand trajectory start and endpoint inter-repetition errors decreased significantly with repeated task performance, as did movement extent, although it was consistently underestimated for each repetition. Pointing direction remained constant, except for the angle of elevation for scapular plane pointing, which consistently decreased throughout the trial. The results suggest that the initial conditions prescribed by actively defining a proprioceptive target were subsequently modified by dynamic proprioception, such that movement reproduction capability improved with repeated task performance.     

ATTEMPTS AT MUSCLE CONTROL WITH VISUAL AND AUDITORY IMPULSES AS AUXILIARY STIMULI

The report covers two EMG-experiments designed to show that the results of motor learning based principally on proprioceptive stimulation are less favorable than the corresponding results when visual and/or auditive auxiliary stimulation operate together with proprioception, even when the motor task is as delicate as the one appearing in the main experiment, i.e. single motor unit activity. The second experiment gives grounds for a conclusion that these results seem to hold for more normal working criteria, too.     

Does exercise-induced muscle damage impair subsequent motor skill learning?

Motor skill learning is a fundamental aspect of human behavior based on the calibration of internal models via sensory information such as proprioception. Some conditions, as exercise-induced muscle damage (EIMD), disrupt proprioceptive information, and may cause learning impairment. Such possible relation between EIMD and motor skill learning has not yet been investigated and it is the aim of this study. For this purpose, thirty male university students (19.3 ± 1.8 years) were equally assigned to two groups: EIMD and CON group. The EIMD group received a treatment to induce muscle damage consisting of a weight lifting protocol directed to the agonist muscles related to the task prior to the pretest and to the learning sessions. EIMD was verified and compared between groups and along the process (0–168 h) by means of the degree of delayed onset muscle soreness (DOMS), perceived total quality recovery and maximal isometric strength (MIS). To investigate motor skill learning, both groups practiced a dart throwing task for four sessions with 150 trials in each session. Recovery status and DOMS were recovered at 96 h in the EIMD group, and MIS was not recovered throughout 168 h. In contrast, muscle damage parameters were not altered across 168 h in the CON group. Accuracy and consistency were compared within and between groups in a pretest posttest design. The EIMD group showed less accurate and consistent results on the long term (delayed posttest). Results confirmed our hypothesis that EIMD, a common condition in sports and in rehab practices, may hinder motor skill learning, possibly due to neurological aspects such as proprioceptive information, its relation to central nervous system reorganization and internal model consolidation.     

The use of proprioception and tactile information in haptic search

To investigate how tactile and proprioceptive information are used in haptic object discrimination we conducted a haptic search task in which participants had to search for either a cylinder, a bar or a rotated cube within a grid of aligned cubes. Tactile information from one finger is enough to detect a cylinder amongst the cubes. For detecting a bar or a rotated cube amongst cubes touch alone is not enough. For the rotated cube this is evident because its shape is identical to that of the non-targets, so proprioception must provide information about the orientation of the fingers and hand when touching it. For the bar one either needs proprioceptive information about the distance and direction of a single finger’s movements along the surfaces, or proprioceptive information from several fingers when they touch it simultaneously. When using only one finger, search times for the bar were much longer than those for the other two targets. When the whole hand or both hands were used the search times were similar for all shapes. Most errors were made when searching for the rotated cube, probably due to systematic posture-related biases in judging orientation on the basis of proprioception. The results suggest that tactile and proprioceptive information are readily combined for shape discrimination.