Proprioceptive impairment and postural orientation control in Parkinson's disease

Impairment of postural control is a common consequence of Parkinson’s disease (PD). Increasing evidences demonstrate that the pathophysiology of postural disorders in PD includes deficits in proprioceptive processing and integration. However, the nature of these deficits has not been thoroughly examined. We propose to establish a link between proprioceptive impairments and postural deficits in PD using two different experimental approaches manipulating proprioceptive information. In the first one, the subjects stood on a platform that tilted slowly with oscillatory angular movements in the frontal or sagittal planes. The amplitude and frequency of these movements were kept below the semicircular canal perception threshold. Subjects were asked to maintain vertical body posture with and without vision. The orientations of body segments were analyzed. In the second one, the postural control was tested using the tendon-vibration method, which is known to generate illusory movement sensations and postural reactions. Vibrations were applied to ankle muscles. The subject’s whole-body motor responses were analyzed from center of pressure displacements.In the first experiment, the parkinsonian patients (PP) were unable to maintain the vertical trunk orientation without vision. Their performances with vision improved, without fully reaching the level of control subjects (CS). In the second experiment, the postural reactions of the PP were similar to those of the CS at the beginning of the perturbation and increased drastically at the end of the perturbation’s period as compared to those of CS and could induce fall.These results will bring new concepts to the sensorimotor postural control, to the physiopathology of posture, equilibrium and falls in PD and to the role of basal ganglia pathways in proprioception integration. Nevertheless, in order to assess precisely the role played by sensorimotor integration deficits in postural impairments in PD, further studies establishing the links between clinical features and abnormalities are now required.     

Does transcranial direct current stimulation during writing alleviate upper limb freezing in people with Parkinson’s disease? A pilot study

Transcranial direct current stimulation (tDCS) over the primary motor cortex (M1) can boost motor performance in Parkinson’s disease (PD) when it is applied at rest. However, the potential supplementary therapeutic effect of the concurrent application of tDCS during the training of motor tasks is largely unknown. The present study examined the effects of tDCS on upper limb motor blocks during a freezing-provoking writing task (the funnel task) requiring up- and down-stroke movements at alternating amplitudes. Ten PD patients and 10 age-matched controls underwent two sessions of writing combined with 20 min of anodal or sham tDCS on the left M1 in a randomized cross-over design. The primary outcome was the number of upper limb freezing episodes during five trials of the funnel task on a touch-sensitive tablet. PD patients showed a significant reduction in freezing episodes during tDCS compared to sham. No effects of tDCS were found for the amplitude, variability and speed of the strokes outside the freezing episodes. However, patients who reported freezing episodes in daily life (N = 6) showed a beneficial effect of tDCS on stroke characteristics. These results indicate a subgroup-dependent variability in response to non-invasive brain stimulation applied during the performance of motor tasks in PD. This warrants future studies to examine tDCS as an adjuvant tool for training programs aimed to reduce motor deficits related to freezing.     

Having a body versus moving your body: How agency structures body-ownership

We investigated how motor agency in the voluntary control of body movement influences body awareness. In the Rubber Hand Illusion (RHI), synchronous tactile stimulation of a rubber hand and the participant's hand leads to a feeling of the rubber hand being incorporated in the participant's own body. One quantifiable behavioural correlate of the illusion is an induced shift in the perceived location of the participant's hand towards the rubber hand. Previous studies showed that the induced changes in body awareness are local and fragmented: the proprioceptive drift is largely restricted to the stimulated finger. In the present study, we investigated whether active and passive movements, rather than tactile stimulation, would lead to similarly fragmented body awareness. Participants watched a projected image of their hand under three conditions: active finger movement, passive finger movement, and tactile stimulation. Visual feedback was either synchronous or asynchronous with respect to stimulation of the hand. A significant overall RHI, defined as greater drifts following synchronous than asynchronous stimulation, was found in all cases. However, the distribution of the RHI across stimulated and non-stimulated fingers depended on the kind of stimulation. Localised proprioceptive drifts, specific to the stimulated finger, were found for tactile and passive stimulation. Conversely, during active movement of a single digit, the proprioceptive drifts were not localised to that digit, but were spread across the whole hand. Whereas a purely proprioceptive sense of body-ownership is local and fragmented, the motor sense of agency integrates distinct body-parts into a coherent, unified awareness of the body.     

Age-related differences in the integration of sensory information during the execution of a bimanual coordination task

Young (n = 7) and elderly (n = 7) subjects performed bimanual coordination patterns in the transverse plane according to the in-phase or antiphase mode. Sensory information was manipulated through visual (with or without vision of the limbs) and proprioceptive input (with or without vibratory stimuli on one limb). Movement patterns with vibrations showed higher deviations from the intended relative phase than did those without vibrations. This finding suggests that the proprioceptive information induced by the vibrations and the movement interfered, leading to a disruption of the coordination patterns. In addition, as compared with the elderly, the young subjects performed more stable movements under normal circumstances but were more strongly affected by vibratory stimuli during the performance of in-phase movements. During antiphase movements, both age groups experienced a decrease of pattern stability. Furthermore, the absence or presence of visual feedback influenced the performance of the young subjects more than that of the elderly. The presence of vision led to stable in-phase movements, whereas a decrease of pattern stability was observed for antiphase movements. In general, these results demonstrate that manipulation of feedback sources affects young subjects more than elderly ones, and this can be related to a reduced sensory sensitivity as a function of aging.     

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.     

Proprioceptive control of goal-directed movements in man, studied by means of vibratory muscle tendon stimulation

The purpose of this study was to investigate the role of propriomuscular feedback in the control of pluriarticular pointing movements, performed without visual feedback toward visual targets. The proprioceptive inputs were distorted during movements by applying vibration to the distal tendon of the biceps muscle. Various movement and vibration durations were imposed. The results show that vibration affects the spatial outcome of the movements. The effects of vibration were movement time-independent when the durations were shorter than 450 ms and became movement time-dependent with longer durations. Moreover, the effects of vibration became more marked when a short vibration was applied at the end rather than at the beginning of a slow movement. These studies suggest that at least two types of proprioceptive control loops may be involved in correcting this kind of movement, depending on the execution time. In slow movements, the final phase might be a privileged period for on-line, propriomuscular-based corrections. Lastly, it emerged that the regulation of a goal-directed movement on the basis of proprioceptive feedback processing can take place within at most 200 ms.     

Role of proprioceptive information in movement programming and control in 5 to 11-year old children

The role of proprioceptive inputs in the control of goal-directed movements was examined, by means of the tendon vibration technique, in 5 to 11-year old children performing a serial pointing task. Children pointed, with movements of various amplitudes and at various positions, by alternating wrist flexions and extensions. Tendon vibration was applied to both agonist and antagonist muscles to perturb relevant muscular proprioceptive inputs during the static or dynamic phase of the task, i.e., during stops on targets or during movement execution. Constant and variable amplitude errors as well as constant position error were evaluated. Vibratory perturbation applied during movement execution resulted in a similar reduction in movement amplitude, yielding an increased constant error in all age groups and a systematic position error in the direction of the movement starting point. Perturbing proprioception during static phases preceding movement resulted in an age-related increase in the variable amplitude error, which was maximal in 5-year old children performing extension movements. The results were interpreted in terms of the use of proprioceptive information in the feedforward and feedback based components of movement control in children. In particular, the results indicated (1) developmental changes in the relative weighting of each component, (2) an increased capacity to move from one strategy to the other, depending on the availability of information, and (3) developmental changes from an alternated to an integrated control of amplitude and position in serial pointing.     

An examination of the relationship between visual capture and prism adaptation

The phenomena of prismatically induced “visual capture” and adaptation of the hand were compared. In Experiment 1, it was demonstrated that when the subject’s hand was transported for him by the experimenter (passive movement) immediately preceding the measure of visual capture, the magnitude of the immediate shift in felt limb position (visual capture) was enhanced relative to when the subject moved the hand himself (active movement). In Experiment 2, where the dependent measure was adaptation of the prism-exposed hand, the opposite effect was produced by the active/passive manipulation. It appears, then, that different processes operate to produce visual capture and adaptation. It was speculated that visual capture represents an immediate weighting of visual over proprioceptive input as a result of the greater precision of vision and/or the subject’s tendency to direct his attention more heavily to this modality. In contrast, prism adaptation is probably a recalibration of felt limb position in the direction of vision, induced by the presence of a registered discordance between visual and proprioceptive inputs.     

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.     

Visual guidance for hand advance but not hand withdrawal in a reach-to-eat task in adult humans: reaching is a composite movement

Many animal species use reaching for food to place in the mouth (reach-to-eat) with a hand, and it may be a primitive movement. Although researchers (I. Q. Whishaw, 2005; A. N. Iwaniuk & I. Q. Whishaw, 2000; M. Gentiluci, I. Toni, S. Chieffi, & G. Pavesi, 1994) have described visual guidance of reaching in both normal and brain-injured human and nonhuman primates, researchers have not described the contribution of vision during advance of the limb to grasp food and during withdrawal of the limb with food to the mouth. To evaluate visual contributions, the authors monitored eye movements in young adults as they reached for food with and without vision. Participants visually engaged the target prior to the 1st hand movement and disengaged it as the food was grasped. Visual occlusion slowed limb advance and altered digit shaping but did not affect withdrawal. The dependence on visual control of advance but not withdrawal suggests that the reach-to-eat movement is a composite of 2 basic movements under visual and tactile/proprioceptive guidance, respectively.     

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.     

Visual information: The control of aiming movements

The study examined the contribution of various sources of visual information utilised in the control of discrete aiming movements. Subjects produced movements, 15.24 cm in amplitude, to a 1.27 cm target in a movement time of 330 ms. Responses were carried out at five vision-manipulation conditions which allowed the subject complete vision, no vision, vision of only the target or stylus, and a combination of stylus and target. Response accuracy scores indicated that a decrement in performance occurred when movements were completed in the absence of visual information or when only the target was visible during the response. The stylus and the target plus stylus visual conditions led to response accuracy which was comparable to movements produced with complete vision. These results suggest that the critical visual information for aiming accuracy is that of the stylus. These findings are consistent with a control model based on a visual representation of the discrepancy between the position of the hand and the location of the target.     

The utilization of visual information in the control of reciprocal aiming movements

Two experiments examined on-line processing during the execution of reciprocal aiming movements. In Experiment 1, participants used a stylus to make movements between two targets of equal size. Three vision conditions were used: full vision, vision during flight and vision only on contact with the target. Participants had significantly longer movement times and spent more time in contact with the targets when vision was available only on contact with the target. Additionally, the proportion of time to peak velocity revealed that movement trajectories became more symmetric when vision was not available during flight. The data indicate that participants used vision not only to 'home-in' on the current target, but also to prepare subsequent movements. In Experiment 2, liquid crystal goggles provided a single visual sample every 40 ms of a 500 ms duty cycle. Of interest was how participants timed their reciprocal aiming to take advantage of these brief visual samples. Although across participants no particular portion of the movement trajectory was favored, individual performers did time their movements consistently with the onset and offset of vision. Once again, performance and kinematic data indicated that movement segments were not independent of each other.     

Discrimination of amount of spinal flexion for movements made with and without vision after lumbar disc replacement

Discrimination of differences between small lumbar flexion movements made when standing may differ depending on whether vision is available. Dependence on general vision during trunk movements may be increased following surgery, in which an intervertebral disc is replaced with a prosthetic disc. This study investigated whether the availability of vision changed discrimination of small differences in lumbar forward flexion movement when standing for patients with lumbar disc replacement and healthy peers. 20 volunteers without a history of back pain and 20 with disc replacement undertook a 100-trial sequence of forward flexion movements to a set of physical stops, making an absolute judgement as to the position after each movement. General (nontarget) vision during the movement was available or removed randomly trial by trial. Availability of vision did not affect discrimination of flexion movements of the lumbar spine either in normal healthy individuals or those with disc replacement.     

Specificity of practice, visual information, and intersegmental dynamics in rapid-aiming limb movements

The authors tested the specificity of practice hypothesis on intersegmental dynamics of rapid-aiming limb movements. During acquisition, 20 participants performed an aiming task as quickly and accurately as possible either with or without vision. Following moderate (140 trials) and extensive (560 trials) practice, participants completed 20 transfer test trials in a no-vision condition. Overall, the acquisition-phase findings revealed that vision improved aiming accuracy performance but had only a slight impact on movement time and intersegmental dynamics. After 560 trials of practice, however, withdrawal of vision resulted in specificity of practice effects on intersegmental dynamics at the shoulder as well as on aiming accuracy. Taken together, those findings support and extend the specificity of practice hypothesis     

Gaze-dependent deviation in pointing induced by transcranial magnetic stimulation over the human posterior parietal cortex

Signals arising from the saccadic system influence the planning and generation of pointing movements, and the posterior parietal cortex (PPC) appears to play a vital role in that interaction. The authors demonstrate in the present study that during visual fixation, eye-position signals can dominate pointing responses when the activity in the PPC contralateral to the moving limb is disrupted with transcranial magnetic stimulation (TMS). In particular, when presented with targets in peripheral vision, participants (N=5) exposed to TMS over the PPC failed to show the normal pattern of responses in which pointing movements end up farther away from the goal target. Instead, they tended to point more toward the current point of visual fixation. Those results suggest that the PPC is involved in integrating eye-position and visual information to affect reaching in the contralateral arm.     

Eye-hand coordination in goal-directed aiming.

In a number of studies, we have demonstrated that the spatial-temporal coupling of eye and hand movements is optimal for the pickup of visual information about the position of the hand and the target late in the hand's trajectory. Several experiments designed to examine temporal coupling have shown that the eyes arrive at the target area concurrently with the hand achieving peak acceleration. Between the time the hand reached peak velocity and the end of the movement, increased variability in the position of the shoulder and the elbow was accompanied by a decreased spatial variability in the hand. Presumably, this reduction in variability was due to the use of retinal and extra-retinal information about the relative positions of the eye, hand and target. However, the hand does not appear to be a slave to the eye. For example, we have been able to decouple eye movements and hand movements using Müller-Lyer configurations as targets. Predictable bias, found in primary and corrective saccadic eye movements, was not found for hand movements, if on-line visual information about the target was available during aiming. That is, the hand remained accurate even when the eye had a tendency to undershoot or overshoot the target position. However, biases of the hand were evident, at least in the initial portion of an aiming movement, when vision of the target was removed and vision of the hand remained. These findings accent the versatility of human motor control and have implications for current models of visual processing and limb control.     

Optimal control strategies under different feedback schedules: kinematic evidence

Two experiments were conducted in which participants (N = 12, Experiment 1; N = 12, Experiment 2) performed rapid aiming movements with and without visual feedback under blocked, random, and alternating feedback schedules. Prior knowledge of whether vision would be available had a significant impact on the strategies that participants adopted. When they knew that vision would be available, less time was spent preparing movements before movement initiation. Participants also reached peak deceleration sooner but spent more time after peak deceleration adjusting limb trajectories. Consistent with those findings, analysis of spatial variability at different points in the trajectory indicated that variability increased up to peak deceleration but then decreased from peak deceleration to the end of the movement.     

Visual regulation of manual aiming: A comparison of methods

Visual regulation of upper limb movements occurs throughout the trajectory and is not confined to discrete control in the target area. Early control is based on the dynamic relationship between the limb, the target, and the environment. Despite robust outcome differences between protocols involving visual manipulations, it remains difficult to identify the kinematic events that characterize these differences. In this study, participants performed manual aiming movements with and without vision. We compared several traditional approaches to movement analysis with two new methods of quantifying online limb regulation. As expected, participants undershot the target and their movement endpoints were more variable when vision was not available. Although traditional measures such as reaction time, time after peak velocity, and the presence of discontinuities in acceleration were sensitive to the visual manipulation, measures quantifying the trial-to-trial spatial variability throughout the trajectory were the most effective in isolating the time course of online regulation.     

Eye-hand coordination asymmetries in manual aiming

The authors investigated whether movement-planning and feedback-processing abilities associated with the 2 hand-hemisphere systems mediate illusion-induced biases in manual aiming and saccadic eye movements. Although participants' (N = 23) eye movements were biased in the direction expected on the basis of a typical Müller-Lyer configuration, hand movements were unaffected. Most interesting, both left- and right-handers' eye fixation onset and time to hand peak velocity were earlier when they aimed with the left hand than they were when they aimed with the right hand, regardless of the availability of vision for online movement control. They thus adapted their eye-hand coordination pattern to accommodate functional asymmetries. The authors suggest that individuals apply different movement strategies according to the abilities of the hand and the hemisphere system used to produce the same outcome.