Coordination deficits during trunk-assisted reach-to-grasp movements in Parkinson's disease.

The present study investigated how Parkinson's disease (PD) affects temporal coordination among the trunk, arm, and fingers during trunk-assisted reach-to-grasp movements. Seated participants with PD and healthy controls made prehensile movements. During the reach to the object, the involvement of the trunk was altered based on the instruction; the trunk was not involved, moved forward (flexion), or moved backward (extension) in the sagittal plane. Each of the trunk movements was combined with an extension or flexion motion of the arm during the reach. For the transport component, the individuals with PD substantially delayed the onset of trunk motion relative to that of arm motion in conditions where the trunk was moved in the direction opposite from the arm reaching toward the object. At the same time, variability of intervals between the onsets and intervals between the velocity peaks of the trunk and wrist movements was increased. The magnitudes of the variability measures were significantly correlated with the severity of PD. Regarding the grasp component, the individuals with PD delayed the onset of finger movements during reaching. These results imply that PD impairs temporal coordination between the axial and distal body segments during goal-directed skilled actions. When there is a directional discrepancy between the trunk and wrist motions, individuals with PD appear to prioritize wrist motion that is tied to the task goal over the trunk motion. An increase in disease severity magnifies the coordination deficits.

Control of aperture closure initiation during trunk-assisted reach-to-grasp movements.

The present study investigated how the involvement and direction of trunk movement during reach-to-grasp movements affect the coordination between the transport and grasping components. Seated young adults made prehensile movements in which the involvement of the trunk was varied; the trunk was not involved, moved forward (flexion), or moved backward (extension) in the sagittal plane during the reach to the object. Each of the trunk movements was combined with an extension or flexion motion of the arm during the reach. Regarding the relationship between the trunk and arm motion for arm transport, the onset of wrist motion relative to that of the trunk was delayed to a greater extent for the trunk extension than for the trunk flexion. The variability of the time period from the peak of wrist velocity to the peak of trunk velocity was also significantly greater for trunk extension compared to trunk flexion. These findings indicate that trunk flexion was better integrated into the control of wrist transport than trunk extension. In terms of the temporal relationship between wrist transport and grip aperture, the relationship between the time of peak wrist velocity and the time of peak grip aperture did not change or become less steady across conditions. Therefore, the stability of temporal coordination between wrist transport and grip aperture was maintained despite the variation of the pattern of intersegmental coordination between the arm and the trunk during arm transport. The transport-aperture coordination was further assessed in terms of the control law according to which the initiation of aperture closure during the reach occurs when the hand crosses a hand-to-target distance threshold for grasp initiation, which is a function of peak aperture, wrist velocity and acceleration, trunk velocity and acceleration, and trunk-to-target distance at the time of aperture closure initiation. The participants increased the hand-to-target distance threshold for grasp initiation in the conditions where the trunk was involved compared to the conditions where the trunk was not involved. An increase also occurred when the trunk was extended compared to when it was flexed. The increased distance threshold implies an increase in the hand-to-target distance-related safety margin for grasping when the trunk is involved, especially when it is extended. These results suggest that the CNS significantly utilizes the parameters of trunk movement together with movement parameters related to the arm and the hand for controlling grasp initiation.

Age and Not the Preferred Limb Influences the Kinematic Structure of Pointing Movements.

In goal-directed movements, effective open-loop control reduces the need for feedback-based corrective submovements. The purpose of this study was to determine the influence of hand preference and aging on submovements during single- and two-joint pointing movements. A total of 12 young and 12 older right-handed participants performed pointing movements that involved either elbow extension or a combination of elbow extension and horizontal shoulder flexion with their right and left arms to a target. Kinematics were used to separate the movements into their primary and secondary submovements. The older adults exhibited slower movements, used secondary submovements more often, and produced relatively shorter primary submovements. However, there were no interlimb differences for either age group or for the single- and two-joint movements. These findings indicate that open-loop control is similar between arms but compromised in older compared to younger adults.

Effects of hand termination and accuracy constraint on eye-hand coordination during sequential two-segment movements.

The purpose of this study was to examine the effects of accuracy constraints and termination requirements of hand movement on eye-hand coordination. Healthy adults performed two-segment eye and hand aiming movements to predetermined stationary targets. While two-segment eye movements were made to the first and second targets for all conditions, hand movements were varied across conditions. The first segment had two target sizes to alter accuracy constraints. There were three hand movement types with different termination requirements: (1) stop both at the first and at the second targets, (2) stop at the first target and discontinue, and (3) move through the first target and discontinue. The results showed that the initiation of saccades was moderately correlated with the initiation of hand movements, and both initiations changed in a similar fashion depending on various hand termination requirements. Amplitude of primary saccades and frequency of corrective saccades during the first segment were affected by the combined effects of accuracy constraints and hand termination requirements. These results suggest that the planning and execution of saccades are based in part on global task constraints related to the accuracy and termination demands of hand movements over the two segments. During the transition from the first to the second segment, the gaze was held on the first target until shortly after the pointing to that target was terminated, showing gaze anchoring. The gaze anchoring was prolonged due to the increased accuracy constraint of that target or by including pointing to the second target. However, the gaze anchoring was broken prior to the completion of pointing when the accuracy constraint was reduced and pointing to the second target was excluded. The observed modifications of gaze anchoring imply that the oculomotor system is functionally obligated to fixate a gaze to a pointing target only to the extent that successful completion of a pointing task is ensured by the actual completion or by a predictive assessment of pointing termination.

Control of aperture closure initiation during reach-to-grasp movements under manipulations of visual feedback and trunk involvement in Parkinson's disease.

The present project was aimed at investigating how two distinct and important difficulties (coordination difficulty and pronounced dependency on visual feedback) in Parkinson's disease (PD) affect each other for the coordination between hand transport toward an object and the initiation of finger closure during reach-to-grasp movement. Subjects with PD and age-matched healthy subjects made reach-to-grasp movements to a dowel under conditions in which the target object and/or the hand were either visible or not visible. The involvement of the trunk in task performance was manipulated by positioning the target object within or beyond the participant's outstretched arm to evaluate the effects of increasing the complexity of intersegmental coordination under different conditions related to the availability of visual feedback in subjects with PD. General kinematic characteristics of the reach-to-grasp movements of the subjects with PD were altered substantially by the removal of target object visibility. Compared with the controls, the subjects with PD considerably lengthened transport time, especially during the aperture closure period, and decreased peak velocity of wrist and trunk movement without target object visibility. Most of these differences were accentuated when the trunk was involved. In contrast, these kinematic parameters did not change depending on the visibility of the hand for both groups. The transport-aperture coordination was assessed in terms of the control law according to which the initiation of aperture closure during the reach occurred when the hand distance-to-target crossed a hand-target distance threshold for grasp initiation that is a function of peak aperture, hand velocity and acceleration, trunk velocity and acceleration, and trunk-target distance at the time of aperture closure initiation. When the hand or the target object was not visible, both groups increased the hand-target distance threshold for grasp initiation compared to its value under full visibility, implying an increase in the hand-target distance-related safety margin for grasping. The increase in the safety margin due to the absence of target object vision or the absence of hand vision was accentuated in the subjects with PD compared to that in the controls. The pronounced increase in the safety margin due to absence of target object vision for the subjects with PD was further accentuated when the trunk was involved compared to when it was not involved. The results imply that individuals with PD have significant limitations regarding neural computations required for efficient utilization of internal representations of target object location and hand motion as well as proprioceptive information about the hand to compensate for the lack of visual information during the performance of complex multisegment movements.

Phase dependence of transport-aperture coordination variability reveals control strategy of reach-to-grasp movements.

Based on an assumption of movement control optimality in reach-to-grasp movements, we have recently developed a mathematical model of transport-aperture coordination (TAC), according to which the hand-target distance is a function of hand velocity and acceleration, aperture magnitude, and aperture velocity and acceleration (Rand et al. in Exp Brain Res 188:263-274, 2008). Reach-to-grasp movements were performed by young adults under four different reaching speeds and two different transport distances. The residual error magnitude of fitting the above model to data across different trials and subjects was minimal for the aperture-closure phase, but relatively much greater for the aperture-opening phase, indicating considerable difference in TAC variability between those phases. This study's goal is to identify the main reasons for that difference and obtain insights into the control strategy of reach-to-grasp movements. TAC variability within the aperture-opening phase of a single trial was found minimal, indicating that TAC variability between trials was not due to execution noise, but rather a result of inter-trial and inter-subject variability of motor plan. At the same time, the dependence of the extent of trial-to-trial variability of TAC in that phase on the speed of hand transport was sharply inconsistent with the concept of speed-accuracy trade-off: the lower the speed, the larger the variability. Conversely, the dependence of the extent of TAC variability in the aperture-closure phase on hand transport speed was consistent with that concept. Taking into account recent evidence that the cost of neural information processing is substantial for movement planning, the dependence of TAC variability in the aperture-opening phase on task performance conditions suggests that it is not the movement time that the CNS saves in that phase, but the cost of neuro-computational resources and metabolic energy required for TAC regulation in that phase. Thus, the CNS performs a trade-off between that cost and TAC regulation accuracy. It is further discussed that such trade-off is possible because, due to a special control law that governs optimal switching from aperture opening to aperture closure, the inter-trial variability of the end of aperture opening does not affect the high accuracy of TAC regulation in the subsequent aperture-closure phase.

Joint-specific disruption of control during arm movements in Parkinson's disease.

The leading joint hypothesis (LJH) suggests distinct types of control (leading and subordinate) at different joints during multi-joint movements. Taking into account specific features of movements in Parkinson's disease (PD), the LJH predicts distinct effect of PD on control of leading and subordinate joints: impaired interaction torque (INT) regulation should be emphasized at the subordinate joints, and impaired generation of muscle torque (MUS) magnitude should be more pronounced at the leading joint. This prediction was tested by studying three tasks of horizontal shoulder-elbow movements in PD patients and age-matched controls: cyclic line drawing, cyclic point-to-point, and discrete pointing movements. Each task included movements in different directions, providing both shoulder-lead and elbow-lead control patterns. Torque analysis supported the prediction, specifically for Tasks 2 and 3 in which movement targets were chosen to emphasize the shoulder- and elbow-lead control patterns. Patients did not exploit INT for motion generation as successfully as controls did, but only at the subordinate joint. Underproduction of MUS by PD patients was more apparent at the leading than subordinate joint. The results support joint-specific effect of PD on movement control. They also suggest that dyscoordination of joint motions in PD stems predominantly from impaired control of subordinate joints, while bradykinesia is associated more with control of the leading than subordinate joint. Possible contribution of the revealed impairments in joint control to some other movement features in PD is discussed. The study demonstrates the efficiency of the LJH application for revealing changes in joint control caused by motor disorders.

Hypometria and bradykinesia during drawing movements in individuals with Parkinson's disease.

To address the hypothesis that Parkinson's disease (PD) patients have deficits in controlling acceleration, a drawing task was used in which target size, frequency, and weight of pen were manipulated. In accordance with previous results, it was found that, relative to controls, PD patients produced movements at the required frequency, but moved significantly slower, produced less acceleration, and drew smaller-than-required stroke sizes. This resulted in smaller-than-required movement amplitudes, suggesting that hypometria and bradykinesia in drawing and/or handwriting are related. Patients were found to perform similarly to controls when the target size was 1 cm. However, their performance became more dissimilar at greater stroke lengths. In addition to the aforementioned effects it was found that movement amplitude error was less when the pen was 20 times heavier than the normal pen and that the increased load may dampen abnormal limb-stiffness characteristics induced by PD.

Movement structure in young and elderly adults during goal-directed movements of the left and right arm.

Elderly adults often exhibit performance deficits during goal-directed movements of the dominant arm compared with young adults. Recent studies involving hemispheric lateralization have provided evidence that the dominant and non-dominant hemisphere-arm systems are specialized for controlling different movement parameters and that hemispheric specialization may be reduced during normal aging. The purpose was to examine age-related differences in the movement structure for the dominant (right) and non-dominant (left) during goal-directed movements. Young and elderly adults performed 72 aiming movements as fast and as accurately as possible to visual targets with both arms. The findings suggest that previous research utilizing the dominant arm can be generalized to the non-dominant arm because performance was similar for the two arms. However, as expected, the elderly adults showed shorter relative primary submovement lengths and longer relative primary submovement durations, reaction times, movement durations, and normalized jerk scores compared to the young adults.

Quantitative model of transport-aperture coordination during reach-to-grasp movements.

It has been found in our previous studies that the initiation of aperture closure during reach-to-grasp movements occurs when the hand distance to target crosses a threshold that is a function of peak aperture amplitude, hand velocity, and hand acceleration. Thus, a stable relationship between those four movement parameters is observed at the moment of aperture closure initiation. Based on the concept of optimal control of movements (Naslin 1969) and its application for reach-to-grasp movement regulation (Hoff and Arbib 1993), it was hypothesized that the mathematical equation expressing that relationship can be generalized to describe coordination between hand transport and finger aperture during the entire reach-to-grasp movement by adding aperture velocity and acceleration to the above four movement parameters. The present study examines whether this hypothesis is supported by the data obtained in experiments in which young adults performed reach-to-grasp movements in eight combinations of two reach-amplitude conditions and four movement-speed conditions. It was found that linear approximation of the mathematical model described the relationship among the six movement parameters for the entire aperture-closure phase with very high precision for each condition, thus supporting the hypothesis for that phase. Testing whether one mathematical model could approximate the data across all the experimental conditions revealed that it was possible to achieve the same high level of data-fitting precision only by including in the model two additional, condition-encoding parameters and using a nonlinear, artificial neural network-based approximator with two hidden layers comprising three and two neurons, respectively. This result indicates that transport-aperture coordination, as a specific relationship between the parameters of hand transport and finger aperture, significantly depends on the condition-encoding variables. The data from the aperture-opening phase also fit a linear model, whose coefficients were substantially different from those identified for the aperture-closure phase. This result supports the above hypothesis for the aperture-opening phase, and consequently, for the entire reach-to-grasp movement. However, the fitting precision was considerably lower than that for the aperture-closure phase, indicating significant trial-to-trial variability of transport-aperture coordination during the aperture-opening phase. Implications for understanding the neural mechanisms employed by the CNS for controlling reach-to-grasp movements and utilization of the mathematical model of transport-aperture coordination for data analysis are discussed.