Assessment of postural control in patients with Parkinson’s disease: Sway ratio analysis

Analysis of the postural stability impairments in neurodegenerative diseases is a very demanding task. Age-related declines in posturographic indices are usually superimposed on effects associated with the pathology and its treatment. We present the results of a novel postural sway ratio (SR) analysis in patients with Parkinson’s disease (PD) and age-matched healthy subjects. The sway ratios have been assessed based upon center of foot-pressure (CP) signals recorded in 55 parkinsonians (Hoehn and Yahr: 1-3) and 55 age-matched healthy volunteers while standing quiet with eyes open (EO) and then with eyes closed (EC). Complementing classical sway measure abnormalities, the SR exhibited a high discriminative power for all controlled factors: pathology, vision, and direction of sway. Both the anteroposterior (AP) and mediolateral (ML) sway ratios were significantly increased in PD patients when compared to the control group. An additional SR increase was observed in the response to eyes closure. The sway ratio changes documented here can be attributed to a progressive decline of a postural stability control due to pathology. In fact, a significant correlation between the mediolateral SR under EO conditions and Motor Exam (section III) score of the UPDRS was found. The mediolateral sway ratios computed for EO and EC conditions significantly correlated with the CP path length (r = .87) and the mean anteroposterior CP position within the base of support (r = .38). Both indices reflect postural stability decline and fall tendency # in parkinsonians. The tremor-type PD patients (N = 34) showed more pronounced relationships between the mediolateral SR and selected items from the UPDRS scale, including: falls (Kendall Tau = .47, p < .05), rigidity (.45, p < .05), postural stability (retropulsion) (.52), and the Motor Exam score (.73). The anteroposterior SR correlated only with tremor (Kendal Tau = .77, p < .05). It seems that in force plate posturography the SR can be recommended as a single reliable measure that allows for a better quantitative assessment of postural stability impairments.     

Cathodal tDCS of the Left Posterior Parietal Cortex Increases Proprioceptive Drift

In aiming movements the limb position drifts away from the defined target after some trials without visual feedback, a phenomenon defined as proprioceptive drift (PD). There are no studies investigating the association between the posterior parietal cortex (PPC) and PD in aiming movements. Therefore, cathodal and sham transcranial direct current stimulation (tDCS) were applied to the left PPC concomitantly with the performance of movements with or without vision. Cathodal tDCS applied without vision produced a higher level of PD and higher rates of drift accumulation while it decreased peak velocity and maintained the number of error corrections, not affecting movement amplitude. The proprioceptive information seems to produce an effective reference to movement, but with PPC stimulation it causes a negative impact on position.     

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.     

Origins of the proprioceptive function of vision: visual control of posture in one day old domestic chicks.

Recently hatched domestic chicks control their upright bipedal posture, at least in part, with respect to the flow of visual information at the retina, as do human infants when they first acquire control of the head, of sitting, and of standing. Some implications of the similarity of the proprioceptive function of vision in chicks and in humans for the origins and development of postural control are discussed.     

The adaptation to sensory information in the production of bimanual movement patterns

Bimanual in-phase and anti-phase patterns were performed in the transverse plane under optimal and degraded proprioceptive conditions, i.e., without and with tendon vibration. Moreover, proprioceptive information was changed midway into each trial to examine on-line reorganization. In addition to the proprioceptive perturbation, the availability of visual information was manipulated to study to which degree sensory information from different modalities interact. Movement patterns performed under identical sensory conditions were compared, i.e., the first 15 s (control) and the 15 s following a change in afferent input (transfer). In the control and transfer conditions, movements with vibrations were less accurate than those without vibrations indicating the influence of optimal proprioceptive information in the calibration and recalibration of intrinsic bimanual movement patterns. Furthermore, pattern stability was affected by the nature of the transfer condition. This indicated that the degree of fluctuations in a sensory transfer situation depended upon the quality of the proprioceptive information experienced in the initial conditions. The influence of visual information was not without importance, although the nature of the coordination mode must be taken into account. In the control conditions, in-phase movements were less stable when vision was absent, whereas anti-phase movements were more stable when vision was not present. This observation was made independent of the available proprioceptive information revealing differences in visual guidance between both coordination modes. In the transfer conditions, pattern stability was similar during the vision and no-vision conditions suggesting a limited influence of visual information in the recalibration process.     

Interacting Constraints and the Emergence of Postural Behavior in ACL-Deficient Subjects

In this study, the authors examined how task, informational, and sensorimotor system constraints influence postural control. Postural behavior of subjects with (n = 15) and without (n = 15) a key sensorimotor system constraint, anterior cruciate ligaments (ACLs) in 1 knee, was examined during 1- and 2-legged stance with and without vision. Postural control was assessed on a commonly used postural sway meter and on a dynamic stabilometer. Data on postural sway characteristics were obtained for 30 s under 6 different conditions: standing, with eyes open and closed, on both legs, on the injured leg, and on the noninjured leg. The interaction of task, informational, and sensorimotor constraints was observed only on the dynamic stabilometer and not the postural sway meter. Vision was the most important informational constraint on postural control for subjects on the dynamic stabilometer, particularly for the ACL-deficient group standing on the injured leg. Under more static task constraints, ACL deficiency did not prove a significant disadvantage, because vision was confirmed as a significant source of exproprioceptive information. The results support the functionality of using dynamic tasks such as a stabilometer in assessing postural behavior of subjects with sensorimotor system constraints.     

Interacting Constraints and the Emergence of Postural Behavior in ACL-Deficient Subjects

In this study, the authors examined how task, informational, and sensorimotor system constraints influence postural control. Postural behavior of subjects with (n = 15) and without (n = 15) a key sensorimotor system constraint, anterior cruciate ligaments (ACLs) in 1 knee, was examined during 1 - and 2-legged stance with and without vision. Postural control was assessed on a commonly used postural sway meter and on a dynamic stabilometer. Data on postural sway characteristics were obtained for 30 s under 6 different conditions: standing, with eyes open and closed, on both legs, on the injured leg, and on the noninjured leg. The interaction of task, informational, and sensorimotor constraints was observed only on the dynamic stabilometer and not the postural sway meter. Vision was the most important informational constraint on postural control for subjects on the dynamic stabilometer, particularly for the ACL-deficient group standing on the injured leg. Under more static task constraints, ACL deficiency did not prove a significant disadvantage, because vision was confirmed as a significant source of exproprioceptive information. The results support the functionality of using dynamic tasks such as a stabilometer in assessing postural behavior of subjects with sensorimotor system constraints.     

Effects of disease severity and medication state on postural control asymmetry during challenging postural tasks in individuals with Parkinson’s disease

The aim of this study was to investigate the effects of disease severity and medication state on postural control asymmetry during challenging tasks in individuals with Parkinson’s disease (PD). Nineteen people with PD and 11 neurologically healthy individuals performed three standing task conditions: bipedal standing, tandem and unipedal adapted standing; the individuals with PD performed the tasks in ON and OFF medication state. The participants with PD were distributed into 2 groups according to disease severity: unilateral group (n = 8) and bilateral group (n = 11). The two PD groups performed the evaluations both under and without the medication. Two force plates were used to analyze the posture. The symmetric index was calculated for various of center of pressure. ANOVA one-way (groups) and two-way (PD groups × medication), with repeated measures for medication, were calculated. For main effects of group, the bilateral group was more asymmetric than CG. For main effects of medication, only unipedal adapted standing presented effects of PD medication. There was PD groups × medication interaction. Under the effects of medication, the unilateral group presented lower asymmetry of RMS in anterior–posterior direction and area than the bilateral group in unipedal adapted standing. In addition, the unilateral group presented lower asymmetry of mean velocity, RMS in anterior–posterior direction and area in unipedal standing and area in tandem adapted standing after a medication dose. Postural control asymmetry during challenging postural tasks was dependent on disease severity and medication state in people with PD. The bilateral group presented higher postural control asymmetry than the control and unilateral groups in challenging postural tasks. Finally, the medication dose was able to reduce postural control asymmetry in the unilateral group during challenging postural tasks.     

Upright standing after stroke: How loading-unloading mechanism participates to the postural stabilization

Postural strategies employed by hemiparetic stroke patients need to be better understood to guide rehabilitation. Of the two complementary mechanisms used to stabilize the standing posture, loading-unloading (LU) and pressure distribution (PD), it is hypothesized that the former would be predominantly used. To this aim, posturographic assessments, through a dual force-platform, were performed in 30 Hemiparetics tested 3 months after a unilateral stroke, and 30 matched healthy Controls. Original indices (from 0 to 1) were calculated to assess LU and PD contributions. The results show that along the mediolateral axis, the LU contribution was very high and similar in Hemiparetics and in Controls (0.80 ± 0.07 vs 0.76 ± 0.09 a.u; p > 0.05), indicating a predominant hip involvement. Along the anteroposterior axis, the PD contribution was very close to 1 in controls (0.96 ± 0.03 a.u.) indicating an exclusive ankle involvement. Despite a lower contribution in Hemiparetics (0.88 ± 0.11 a.u.; p < 0.01), the indices were surprisingly always above 0.5, meaning that ankle movements remain predominant for controlling postural sways along the anteroposterior axis in all patients even those with severe clinical deficits. However the PD contribution appeared larger in patients with light or moderate deficits of the sensitivity (r = −0.532; p < 0.01) or the motor command (r = −0.513; p < 0.01). These results indicate that postural stabilization of hemiparetic persons remains controlled by a PD mechanism along the anteroposterior axis, even in those combining poor distal motor command and deep sensory loss. This ankle control, piloted by the more-loaded non-paretic limb, would therefore be preferred to a hip control through lateral trunk motion. This should be considered when defining the objectives of the postural rehabilitation after stroke.     

Visuomotor Adaptation and Proprioceptive Recalibration

ABSTRACT

Motor learning, in particular motor adaptation, is driven by information from multiple senses. For example, when arm control is faulty, vision, touch, and proprioception can all report on the arm's movements and help guide the adjustments necessary for correcting motor error. In recent years we have learned a lot about how the brain integrates information from multiple senses for the purpose of perception. However, less is known about how multisensory data guide motor learning. Most models of, and studies on, motor learning focus almost exclusively on the ensuing changes in motor performance without exploring the implications on sensory plasticity. Nor do they consider how discrepancies in sensory information (e.g., vision and proprioception) related to hand position may affect motor learning. Here, we discuss research from our lab and others that shows how motor learning paradigms affect proprioceptive estimates of hand position, and how even the mere discrepancy between visual and proprioceptive feedback can affect learning and plasticity. Our results suggest that sensorimotor learning mechanisms do not exclusively rely on motor plasticity and motor memory, and that sensory plasticity, in particular proprioceptive recalibration, plays a unique and important role in motor learning.     

Postural control,falls and Parkinson’s disease: Are fallers more asymmetric than non-fallers?

Postural control asymmetry is an important aspect of Parkinson’s disease (PD) that may be associated with falls. The aim of this study was to compare the postural control asymmetry during postural tasks between fallers and non-fallers in people with PD and neurological healthy age-matched controls (CG). Individuals with idiopathic PD (n = 24) and CG (n = 24) were sub-divided into groups of fallers and non-fallers based on their fall history over the past year. Participants performed blocks of three 30-s trials of quiet standing with feet in a side-by-side and semi-tandem stance position. The center of pressure parameters for each limb were measured and used to calculate the symmetry index. Fallers compared to non-fallers had decreased asymmetry of vertical force in the side-by-side condition. During the tandem-front leg condition, PD non-fallers increased asymmetry of the medial-lateral velocity of sway compared to CG non-fallers. In addition, for the tandem–back leg condition, PD non-fallers increased asymmetry of total displacement and medial-lateral root mean square and mean velocity of sway compared to PD fallers. The results of the study did not support the hypothesis that PD fallers are more asymmetric than PD non-fallers. On the contrary, our results indicated that PD non-fallers had higher postural control asymmetry, especially during the more challenging (semi-tandem standing) postural task.     

Attention Demands in Balance Recovery following Lower Limb Amputation

The attention demands in balance control after damage to the peripheral sensorimotor system were studied in 12 persons with a recent lower limb amputation. The interference of an arithmetic task with two postural tasks of different complexity (quiet standing and active weight shifting) was examined several times during their rehabilitation while the subjects stood on a force platform. Control data were obtained from healthy subjects. For both postural tasks, persons with amputation performed worse than controls. Quiet standing, a relatively simple task, revealed clear dual-task interference only in the amputation group. Evidence was found for a reduction in dual-task interference as rehabilitation progressed. In contrast, voluntary (feedback-controlled) weight shifting, a more complex task, revealed an equal amount of dual-task interference in persons with amputation and in controls, without changes in interference over the period of rehabilitation. The results indicate that attentional mechanisms may be involved in postural control, depending on both the novelty and complexity of the task. Moreover, a reduction in attention demands of quiet standing may reflect a central adaptation of the postural organization to the peripheral sensorimotor impairments caused by lower limb amputation.     

Attention demands in balance recovery following lower limb amputation

The attention demands in balance control after damage to the peripheral sensorimotor system were studied in 12 persons with a recent lower limb amputation. The interference of an arithmetic task with two postural tasks of different complexity (quiet standing and active weight shifting) was examined several times during their rehabilitation while the subjects stood on a force platform. Control data were obtained from healthy subjects. For both postural tasks, persons with amputation performed worse than controls. Quiet standing, a relatively simple task, revealed clear dual-task interference only in the amputation group. Evidence was found for a reduction in dual-task interference as rehabilitation progressed. In contrast, voluntary (feedback-controlled) weight shifting, a more complex task, revealed an equal amount of dual-task interference in persons with amputation and in controls, without changes in interference over the period of rehabilitation. The results indicate that attentional mechanisms may be involved in postural control, depending on both the novelty and complexity of the task. Moreover a reduction in attention demands of quiet standing may reflect a central adaptation of the postural organization to the peripheral sensorimotor impairments caused by lower limb amputation.     

Sensorimotor Impairment of Speech and Hand Movement Timing Processing in Parkinson’s Disease

Models of motor control have highlighted the role of temporal predictive mechanisms in sensorimotor processing of speech and limb movement timing. We investigated how these mechanisms are affected in Parkinson’s disease (PD) while patients performed speech and hand motor reaction time tasks in response to sensory stimuli with predictable and unpredictable temporal dynamics. Results showed slower motor reaction times in PD vs. control in response to temporally predictable, but not unpredictable stimuli. This effect was driven by faster motor responses to predictable stimuli in control subjects; however, no such effect was observed in the PD group. These findings indicated the relationship between PD pathology and sensorimotor deficits in temporal predictive mechanisms of timing processing during speech production and hand movement.     

Ideational action impairments in Alzheimer's disease

We report data from a group of patients with mild Alzheimer's disease on a range of tasks requiring either stored semantic knowledge about objects (e.g., naming object use) or the execution of action to objects (e.g., miming and using objects). We found that the patients were impaired at miming in response to objects, even when they could describe the object's function. On the other hand, copying gestures was not impaired relative to naming gestures, indicating that an ideomotor deficit in action execution, per se, was unlikely to explain the impairments in object use. We suggest instead that the patients had an impairment in stored motor programmes for action, over and above their deficits in semantic knowledge. Despite this, the patients were better at using than at miming to objects, consistent with the view that proprioceptive input (when using objects) can directly constrain selection of the appropriate motor programme for action.     

Coupling of postural and manual tasks in expert performers

The purpose of this study was to investigate the integration of bimanual rhythmic movements and posture in expert marching percussionists. Participants (N = 11) performed three rhythmic manual tasks [1:1, 2:3, and 2:3-F (2:3 rhythm played faster at a self-selected tempo)] in one of three postures: sitting, standing on one foot, and standing on two feet. Discrete relative phase, postural time-to-contact, and coherence analysis were used to analyze the performance of the manual task, postural control, and the integration between postural and manual performance. Across all three rhythms, discrete relative phase mean and variability results showed no effects of posture on rhythmic performance. The complexity of the manual task (1:1 vs. 2:3) had no effect on postural time-to-contact. However, increasing the tempo of the manual task (2:3 vs. 2:3-F) did result in a decreased postural time-to-contact in the two-footed posture. Coherence analysis revealed that the coupling between the postural and manual task significantly decreased as a function of postural difficulty (going from a two-footed to a one-footed posture) and rhythmic complexity (1:1 vs. 2:3). Taken together, these results demonstrate that expert marching percussionists systematically decouple postural and manual fluctuations in order to preserve the performance of the rhythmic movement task.     

Speech motor programming in hypokinetic and ataxic dysarthria

It is widely accepted that the cerebellar and basal ganglia control circuits contribute to the programming of movement. Converging evidence from neuroimaging, limb control, and neuropsychological studies suggests that (1) people with cerebellar disease have reduced ability to program movement sequences in advance of movement onset and (2) people with Parkinson's disease are unable to maintain a programmed response or to rapidly switch between responses. Despite a substantial supporting literature, no studies have addressed these potential areas of speech programming disruption for speakers with ataxic and hypokinetic dysarthria. Control participants and adults with dysarthria completed speech reaction time protocols designed to capture these aspects of utterance preparation. Results provided initial support for processing deficits in speakers with ataxic and hypokinetic dysarthria that are separable from motor execution impairments.     

Review of first trial responses in balance control: influence of vestibular loss and Parkinson's disease

The reaction to an unexpected balance disturbance is unpractised, often startling and frequently associated with falls. This everyday situation can be reproduced in an experimental setting by exposing standing humans to sudden, unexpected and controlled movements of a support surface. In this review, we focus on the responses to the very first balance perturbation, the so-called first trial reactions (FTRs). Detailed analysis of FTRs may have important implications, both for clinical practice (providing new insights into the pathophysiological mechanisms underlying accidental falls in real life) and for understanding human physiology (what triggers and mediates these FTRs, and what is the relation to startle responses?). Several aspects of the FTRs have become clear. FTRs are characterized by an exaggerated postural reaction, with large EMG responses and co-contracting muscles in multiple body segments. This balance reaction is associated with marked postural instability (greater body sway to the perturbation). When the same perturbation is repeated, the size of the postural response habituates and the instability disappears. Other issues about FTRs remain largely unresolved, and these are addressed here. First, the functional role of FTRs is discussed. It appears that FTRs produce primarily increased trunk flexion during the multi-segmental response to postural perturbations, thus producing instability. Second, we consider which sensory signals trigger and modulate FTRs, placing specific emphasis on the role of vestibular signals. Surprisingly, vestibular signals appear to have no triggering role, but vestibular loss leads to excessive upper body FTRs due to loss of the normal modulatory influence. Third, we address the question whether startle-like responses are contributing to FTRs triggered by proprioceptive signals. We explain why this issue is still unresolved, mainly because of methodological difficulties involved in separating FTRs from ‘pure’ startle responses. Fourth, we review new work about the influence of perturbation direction on FTRs. Recent work from our group shows that the largest FTRs are obtained for toe-up support surface rotations which perturb the COM in the posterior direction. This direction corresponds to the directional preponderance for falls seen both in the balance laboratory and in daily life. Finally, we briefly touch upon clinical diagnostic issues, addressing whether FTRs (as opposed to habituated responses) could provide a more ecologically valid perspective of postural instability in patients compared to healthy subjects. We conclude that FTRs are an important source of information about human balance performance, both in health and disease. Future studies should no longer discard FTRs, but routinely include these in their analyses. Particular emphasis should be placed on the link between FTRs and everyday balance performance (including falls), and on the possible role played by startle reactions in triggering or modulating FTRs.     

Everyday cognitive failures and memory problems in Parkinson's patients without dementia

There is growing evidence that Parkinson’s disease patients without dementia exhibit cognitive deficits in some executive, memory and selective attention tasks. However, the impact of these deficits on their everyday cognitive functioning remains largely unknown. This issue was explored using self-report questionnaires. Twenty-four Parkinson’s patients and 24 age-matched controls rated how frequently they make particular cognitive errors, such as forgetting what they were about to say. In addition, a partner or significant other also rated each participant’s propensity for making cognitive errors. Rather than simply rating themselves as making more of all types of errors, these results indicate that PD patients make more of specific types of error. Further analysis suggests that some of these errors are related to attentional processes (being more distractible) whereas others are related to retrieval processes (being unable to recall important details from the previous day).     

The postural control can be optimized by the first movement initiation condition encountered when submitted to muscle fatigue

We investigated whether and how the movement initiation condition (IC) encountered during the early movements performed following focal muscle fatigue affects the postural control of discrete ballistic movements. For this purpose, subjects performed shoulder flexions in a standing posture at maximal velocity under two movement IC, i.e., in self-paced conditions and submitted to a Stroop-like task in which participants had to trigger fast shoulder flexions at the presentation of incongruent colors. Shoulder flexion kinematics, surface muscle activity of focal and postural muscles as well as center-of-pressure kinematics were recorded. The initial IC and the order in which subjects were submitted to these two conditions were varied within two separate experimental sessions. IC schedule was repeated before and after fatigue protocols involving shoulder flexors. The aim of this fatigue procedure was to affect acceleration-generating capacities of focal muscles. In such conditions, the postural muscle activity preceding and accompanying movement execution is expected to decrease. Following fatigue, when subjects initially moved in self-paced conditions, postural muscle activity decreased and scaled to the lower focal peak acceleration. This postural strategy then transferred to the Stroop-like task. In contrast, when subjects initially moved submitted to the Stroop-like task, postural muscle activity did not decrease and this transferred to self-paced movements. Regarding the center-of-pressure peak velocity, which is indicative of the efficiency of the postural actions generated in stabilizing posture, no difference appeared between the two sessions post-fatigue. This highlights an optimization of the postural actions when subjects first moved in self-paced conditions, smaller postural muscle activation levels resulting in similar postural consequences. In conclusion, the level of neuromuscular activity associated with the postural control is affected and can be optimized by the initial movement IC experienced post-fatigue. Beyond the fundamental contributions arising from these results, we point out potential applications for trainers and sports instructors.