Prehension synergies and hand function in early-stage Parkinson's disease

Abstract

We explored the multi-digit synergies and hand performance in object manipulations and pressing tasks in patients with early-stage Parkinson's disease (PD) and healthy controls. Synergies were defined as inter-trials co-variation patterns among forces/moments produced by individual digits that stabilized a resultant mechanical variable. The subjects performed three main tasks: pressing (steady-state force production followed by a force pulse into the target), prehension (manipulation of a handheld instrumented handle imitating the action of taking a sip from a glass), and functional object manipulation (moving a glass with water as quickly and accurately as possible along a chain of targets). The PD patients were slower compared to controls in all three tasks. Patients showed smaller synergy indices in the pressing and prehension tasks. In the prehension tasks, patients showed elevated grip force at steady states with smaller grip force modulation during the handle motion. PD patients showed smaller feed-forward synergy adjustments in preparation to the quick action in the pressing and (to a smaller degree) prehension tasks. Synergy indices correlated with the time index of performance in the functional glass-with-water task, whereas none of the indices correlated with the Unified PD Rating Scale part III-motor scores. We interpret the results as pointing at an important role of subcortical structures in motor synergies and their feed-forward adjustments to action.

Figure 1

The prehension setup included the customized handle with five force/moment sensors, a magnetic tracking sensor, and a level.

Figure 2

Time profiles of movement velocity, sum of tangential forces (Ft TOT) in phase 1, and resultant force (Fn RES) in phase 2. Averaged values across subjects for the PD and CS groups are presented with standard error shades from the initiation (t_START) to the termination (t_END) of movement in each phase. The data between t_START and t_END were re-sampled to 100 points.

Figure 3

Peak-to-peak grip force during the movement (ΔF_G) for phases 1 and 2 in control (CS, white bars) and Parkinson’s disease (PD, black bars) groups. Group means are shown with standard errors.

Figure 4

The relationship between the changes in the grip force (ΔF_G) and thumb tangential force (ΔF^T) during phase 1 for the two groups, control (CS) and Parkinson’s disease (PD). Each point represents the averaged value across trials within each subject. Linear regression equations are shown for the PD and CS groups separately, along with the coefficients of determination (R²).

Figure 5

Safety margin for the thumb plotted against time for the control (CS) and Parkinson’s disease (PD) groups. Averaged values across subjects within each group are presented with standard error shades over the first steady state (SS1), between the initiation of movement (t_START) and the termination of movement (t_END) re-sampled to 100 points, and over the second steady state (SS2). Note the higher SM values and smaller magnitude of modulation in the PD group.

Figure 6

The synergy index (ΔV_Z) during the steady states averaged across subjects within each group (CS – control subjects; PD – Parkinson’s disease) at each of the two levels of hierarchy, the VF-TH level and IF level, for three performance variables: normal force (F^N), tangential force (F^T), and total moment of force (M_TOT and M_VF). Group means with standard error bars are shown.

Figure 7

The correlations between normalized movement time during the “glass-and-water” test (MT_water) and movement time during phase 1 (MT_P1) in the prehension task (panel A, r = 0.80, p < 0.001), and also with the synergy index at the steady state (ΔV_SS) in the pressing task (r = −0.74, p < 0.05). The correlations were computed over all subjects from both groups, controls (CS) and Parkinson’s disease (PD).