Hypokinesia without decrement distinguishes progressive supranuclear palsy from Parkinson's disease

Abstract

Repetitive finger tapping is commonly used to assess bradykinesia in Parkinson's disease. The Queen Square Brain Bank diagnostic criterion of Parkinson's disease defines bradykinesia as 'slowness of initiation with progressive reduction in speed and amplitude of repetitive action'. Although progressive supranuclear palsy is considered an atypical parkinsonian syndrome, it is not known whether patients with progressive supranuclear palsy have criteria-defined bradykinesia. This study objectively assessed repetitive finger tap performance and handwriting in patients with Parkinson's disease (n = 15), progressive supranuclear palsy (n = 9) and healthy age- and gender-matched controls (n = 16). The motion of the hand and digits was recorded in 3D during 15-s repetitive index finger-to-thumb tapping trials. The main finding was hypokinesia without decrement in patients with progressive supranuclear palsy, which differed from the finger tap pattern in Parkinson's disease. Average finger separation amplitude in progressive supranuclear palsy was less than half of that in controls and Parkinson's disease (P < 0.001 in both cases). Change in tap amplitude over consecutive taps was computed by linear regression. The average amplitude slope in progressive supranuclear palsy was nearly zero (0.01°/cycle) indicating a lack of decrement, which differed from the negative slope in patients with Parkinson's disease OFF levodopa (-0.20°/cycle, P = 0.002). 'Hypokinesia', defined as <50% of control group's mean amplitude, combined with 'absence of decrement', defined as mean positive amplitude slope, were identified in 87% of finger tap trials in the progressive supranuclear palsy group and only 12% in the Parkinson's disease OFF levodopa group. In progressive supranuclear palsy, the mean amplitude was not correlated with disease duration or other clinimetric scores. In Parkinson's disease, finger tap pattern was compatible with criteria-defined bradykinesia, characterized by slowness with progressive reduction in amplitude and speed and increased variability in speed throughout the tap trial. In Parkinson's disease, smaller amplitude, slower speed and greater speed variability were all associated with a more severe Unified Parkinson's Disease Rating Scale motor score. Analyses of handwriting showed that micrographia, defined as smaller than 50% of the control group's mean script size, was present in 75% of patients with progressive supranuclear palsy and 15% of patients with Parkinson's disease (P = 0.022). Most scripts performed by patients with progressive supranuclear palsy did not exhibit decrements in script size. In conclusion, patients with progressive supranuclear palsy have a specific finger tap pattern of 'hypokinesia without decrement' and they do not have criteria-defined limb bradykinesia. Similarly, 'micrographia' and 'lack of decrement in script size' are also more common in progressive supranuclear palsy than in Parkinson's disease.

Figure 1

Infrared-emitting diodes fixed to eight designated regions. Motion was recorded in 3D (Coda) and key parameters were measured for each cycle of finger tap.

Figure 2

Handwriting performed by a healthy 65-year-old female (mean script size = 0.86 cm², slope 1 = 0.28, slope 2 = −0.06).

Figure 3

Kinematic parameters during the first 15-s right finger tap trial in a Parkinson's disease patient during the ‘OFF’ condition represented by red circle plots (UPDRSIII-OFF = 32) and a patient with PSP represented by blue triangle plots (UPDRSIII = 69; Frontal Assessment Battery = 14). The slopes (S) for amplitude, duration and speed, and coefficient of variation (CV) for speed are shown. Lack of decrement and fatigue in the patient with PSP is reflected by the positive amplitude slope and speed slope. The speed coefficient of variation in the patient with Parkinson's disease is three times greater than PSP, suggesting high irregularity in speed.

Figure 4

(A) Mean amplitude, duration and speed of control, PSP and PD-OFF groups and P-values by post hoc analysis. Error bars represent 95% confidence intervals. *P < 0.05 indicates statistical significance and #P = 0.05–0.10 indicates borderline significance by Tukey HSD post hoc analysis. (B) Mean slope values for amplitude, duration and speed of control, PSP and PD-OFF groups and P-values by post hoc analysis. Error bars represent 95% confidence intervals. Dotted reference lines represent zero, values below which represent progressive downward negative slope across the 15-s finger tap trial. *P < 0.05 indicates statistical significance and #P = 0.05–0.10 indicates borderline significance by Tukey HSD post hoc analysis.

Figure 5

Among PD-OFF subgroup, a more severe UPDRSIII-OFF score was correlated with smaller mean amplitude, slower mean speed and greater variability in speed.

Figure 6

(A) Handwriting performed by a 58-year-old right-handed patient when in the ‘OFF’ condition (UPDRS = 18, mean script size = 0.66 cm², slope 1 = −0.01, slope 2 = −0.16). (B) Handwriting by the same patient with Parkinson's disease when in the ‘ON’ condition (UPDRS = 13, mean script size = 1.14 cm², slope 1 = −0.08, slope 2 = −0.46).

Figure 7

An example of micrographia from a patient with advanced PSP who had the smallest script size in the PSP group (UPDRSIII = 69, mean script size = 0.14 cm², slope 1 = 0.23, slope 2 = −0.01).