Abstract
The rhythm of the internal clock is considered to be determined by the basal ganglia, with some studies suggesting slower internal clock in Parkinson’s disease (PD). However, patients may also show motor hastening when they walk (festination) or are engaged in repetitive tapping, indicating faster ticking of the internal clock. Is the internal clock slower or faster in PD? The purpose of this study was to answer this question, i.e., how fast and slow a rhythm they can synchronize with, especially with reference to the limit of sensorimotor synchronization or temporal integration, representing the threshold of slower pace they can entrain into their motor actions, which is known to lie between 2 and 3 s in normal subjects but not yet studied in PD. We employed a synchronized tapping task that required subjects to tap the key in synchrony with repetitive tones at fixed interstimulus intervals (ISI) between 200 and 4800 ms. Twenty normal subjects and sixteen PD patients were enrolled, who were classified into early and advanced PD groups by UPDRS-III (early: 15 or less, advanced: more than 15). The ISI at which the response changes from synchronizing with the tones to lagging behind them was considered to be the limit of temporal integration. Early PD patients responded ahead of the tones (negative asynchrony), which became more apparent with repeated tapping. This suggested “faster” ticking clock even in the presence of the pacing tones. In normal subjects, the limit of temporal integration was around 2–3 s: below this, subjects could synchronize with the tones, while above it they had difficulty in synchronization. In early PD patients, the limit of temporal integration was significantly longer than in normal subjects, pointing to their enhanced ability to synchronize also with slower paces of tones, but advanced PD patients had significantly shortened limits, suggesting that advanced patients lost this ability. In conclusion, the limit of temporal integration is initially longer but gets shorter as the disease progresses. It can be explained by the hastening of the internal clock at the earlier stages of PD, followed by the loss of temporal integration.
Highlights
Animal and human neuroimaging studies over the last 10– 20 years have made it clear that the neural structures responsible for temporal processing are those closely associated with the motor system such as the basal ganglia and the cerebellum
The normal subject was able to tap approximately in synchrony with the tones presented at interstimulus interval (ISI) of up to 2400–3600 ms, the tapping became more variable around the time of the tones as ISI increased
Our study demonstrated that early Parkinson’s disease (PD) patients (UPDRS-III ≤ 15) show a tendency toward negative asynchrony as well as a prolonged limit of temporal integration compared to normal subjects
Summary
Animal and human neuroimaging studies over the last 10– 20 years have made it clear that the neural structures responsible for temporal processing are those closely associated with the motor system such as the basal ganglia and the cerebellum. There is as yet no evidence for the neural substrate of a dedicated pacemaker within the central nervous system, SET has been successful in explaining many behavioral aspects of temporal processing as studied by tasks addressing time perception and production (Buhusi and Meck, 2005). By this account, if the internal clock ticks faster, the interval of time is perceived as longer, because more beats of pacemaker would tick during the same interval, whereas when the subjects are required to produce a verbally dictated time interval (e.g., 3 s), the duration produced will be shorter, since the ticks are faster. The notion of slower internal clock is consistent with the findings of studies in which animals treated with dopamine blockers performed the temporal generation task (Pastor et al, 1992; Lange et al, 1995; Koch et al, 2008)
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