Changes in Timing and kinematics of goal directed eye-hand movements in early-stage Parkinson's disease

Abstract

Objective: Many daily activities involve intrinsic or extrinsic goal-directed eye and hand movements. An extensive visuomotor coordination network including nigro-striatal pathways is required for efficient timing and positioning of eyes and hands. The aim of this study was to investigate how Parkinson's disease (PD) affects eye-hand coordination in tasks with different cognitive complexity.

Methods: We used a touch screen, an eye-tracking device and a motion capturing system to quantify changes in eye-hand coordination in early-stage PD patients (H&Y < 2.5) and age-matched controls. Timing and kinematics of eye and hand were quantified in four eye-hand coordination tasks (pro-tapping, dual planning, anti-tapping and spatial memory task).

Results: In the pro-tapping task, saccade initiation towards extrinsic goals was not impaired. However, in the dual planning and anti-tapping task initiation of saccades towards intrinsic goals was faster in PD patients. Hand movements were differently affected: initiation of the hand movement was only delayed in the pro-tapping and dual planning task. Overall, hand movements in PD patients were slower executed compared to controls.

Interpretation: Whereas initiation of saccades in an extrinsic goal-directed task (pro-tapping task) is not affected, early stage PD patients have difficulty in suppressing reflexive saccades towards extrinsic goals in tasks where the endpoint is an intrinsic goal (e.g. dual planning and anti-tapping task). This is specific for eye movements, as hand movements have delayed responses in the pro-tapping and dual planning task. This suggests that reported impairment of the dorsolateral prefrontal cortex in early-stage PD patients affects only inhibition of eye movements. We conclude that timing and kinematics of eye and hand movements in visuomotor tasks are affected in PD patients. This result may have clinical significance by providing a behavioral marker for the early diagnosis of PD.

Figure 1

Overview of the touch screen representations of the starting position and each eye-hand coordination task. A: starting position. The background color of the touch screen was set to grey (RGB value [0.6 0.6 0.6]) and remained this color during all tasks. The participant fixated the eyes on the white central dot and placed the index finger on the blue bar on the bottom of the screen. B: pro-tapping task. A blue dot appeared that had to be touched as fast and accurate as possible. C: in the dual planning task, the eyes had to be fixated on the red dot while simultaneously the blue dot had to be touched. D: the anti-tapping task required participants to touch the screen on the side opposite of the location of the red dot, mirrored in the y-axis. E: In the spatial memory task, a green dot briefly flashed on the screen while participants were in starting position (E1-3). The instruction was to touch the remembered location of the flashed dot as soon as the starting position disappeared.

Figure 2

Quantification of timing variables from eye and hand movement signals. Traces of eye (solid line) and hand movements (dashed line) during the performance of a pro-tapping task trial. At time 0 ms, the blue dot which is the target location for both eye and hand movement, is displayed at a position of +15 degrees with respect to the central dot. The triangle (▲) represents the moment the finger is released from the touch screen, whereas the reversed triangle (▼) represents the moment the target dot is touched. Eye latency (EL) was defined as the time between presentation of the target and the start of the saccade towards it. Hand latency (HL) is the time between presentation of the target and the release of the finger from the screen (▲). Hand execution time (HET) is the time between the release of the finger from the screen and the touch of the target (▲ to ▼). The kinematic variable hand maximal velocity (HMV) is determined from the peak velocity of the hand between start and end of a hand movement.

Figure 3

Representative eye and hand movement traces performed during the four different tasks. Each panel labeled A, B, C and D consists of two subpanels. The upper subpanel shows the eye movements, the lower subpanel those of the hand. Solid lines: PD patient data, dashed line: control subject data. Panel A: pro-tapping task. At time 0 ms the target for the eyes is displayed at a position of 15 degrees from the central dot. Note that in this situation PD patients are able to initiate a saccade towards the target as fast as controls and that PD patients initiated the hand movement significantly slower (HL), as the release of the finger from the screen (▲) was delayed compared to controls (Δ). This panel also shows that the time between the release of the finger from the screen and the touch of the target was significantly increased in PD patients (▲ to ▼) compared to controls (Δ to ∇). Panel B: dual planning task. PD patients initiated the saccade towards the target dot significantly faster compared to controls. Note that for the PD patient the release of the finger from the screen (▲) was significantly delayed compared to controls (Δ). The example also shows that the time between the release of the finger from the screen and the touch of the target was significantly increased in PD patients (▲ to ▼) compared to controls (Δ to ∇). Panel C: anti-tapping task. The PD patient was significantly faster to initiate an eye movement towards the opposite direction of the displayed dot than the control. The PD patient was able to initiate the hand movement (▲) as fast as controls (Δ). The example also shows that HET was significantly increased in PD patients (▲ to ▼) compared to controls (Δ to ∇). Panel D: spatial memory task. The PD patient initiated a saccade towards the remembered target location about as fast as the control. PD patients were also able to initiate the hand movement (▲) as fast as controls (Δ). The time between the release of the finger from the screen and the touch of the target was significantly increased in PD patients (▲ to ▼) compared to controls (Δ to ∇).