Parkinson's disease patients showed delayed awareness of motor intention
Introduction
In everyday life, we experience “free will” when we act voluntarily with prior decision and intention to perform a certain action. However, in the light of recent progress in human neuroscience this apparent link between the intention and action is not as straightforward as it appears. Significant temporal gap between them and the possible existence of subconscious or automatic intention urged some investigators to cast serious doubts on the concept of “free will” (Libet et al., 1982).
Libet's classic experiment using a rotating clock (Libet et al., 1983) revealed that the awareness of the intention to move occurs 200 ms before the actual action and that the electroencephalographic activity precedes this intention by 300 ms. Neurophysiologic studies consistently showed that the implicit motor preparation measured by cortical slow potentials or change in neural oscillations can start more than 1 s earlier than the movement onset (Kornhuber and Deecke, 1965, Shibasaki, 2012, Shibasaki and Hallett, 2006). Moreover, one recent functional MRI study reported the time delay of 10 s or more between the subconscious brain activation and actual overt movement (Soon et al., 2008). As for the brain representation of intention, human neuroimaging and lesion studies implicated the medial frontal areas (pre-SMA/SMA proper) and prefrontal-parietal networks for relevant cortical regions (Cunnington et al., 2002, Lau et al., 2004, Nachev et al., 2005, Sirigu et al., 2004, Soon et al., 2008).
Although the functional importance of the motor loop of the basal ganglia-thalamo-cortical network for controlling volitional movements has been suggested (Alexander et al., 1986, Rouiller et al., 1994, Sakai et al., 1999, Schell and Strick, 1984, Wiesendanger and Wiesendanger, 1985) and dopamine plays an essential role in motor control as well as motivation and modulates the prefrontal and frontal function via basal ganglia thalamo-cortical loop (Tinaz et al., 2010, Zgaljardic et al., 2003), behavioral studies in patients with dopamine depletion investigating the timing of motor intention have never been conducted. Striatal dopamine depletion due to degeneration of the nigrostriatal dopaminergic neuron causes motor disturbance of Parkinson's disease (PD), where the self-willed movement initiation without external cues is most severely disrupted. To test whether the perceived times of actions and intentions are abnormal in PD patients without medication, we applied Libet's clock paradigm (Libet et al., 1983) to patients and age-matched controls.
Since previous studies showed the deficits of timing discrimination in PD patients (Artieda et al., 1992, Fiorio et al., 2007), the use of Libet's task in those patients has some methodological limitations. Thus, we used the control condition of the somatosensory timing detection task to account for this disturbance in timing perception.
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Subjects
Participants consisted of 13 patients with PD (5 males, 8 females) and 13 healthy adults (6 males, 7 females) whose ages were matched (PD group: 67.4 ± 7.1 years old, healthy group: 70.2 ± 2.2 years old).
Patients with PD were diagnosed according to the UK Parkinson's Disease Society Brain Bank criteria (Hughes et al., 1992). They were mildly impaired (Hoehn and Yahr 1: 4 patients, 2: 5 patients, 3: 4 patients). Unified Parkinson's Disease Rating Scale (UPDRS) part 3 for off period was 16.6 ± 7.2. The
Results
In the healthy subjects, awareness of the motor intention (W-time) occurred at −400.6 ± 38.7 ms (mean ± SEM), while awareness of the motor action (M-time) occurred at −136.6 ± 20.1 ms. In PD-off patients, W-time was −249.3 ± 16.3 ms, while M-time was −141.4 ± 22.1 ms. The average S-time was around 100 ms for both groups; healthy: 87.7 ± 13.8 ms and PD-off: 90.1 ± 12.4 ms.
Two-way repeated measure ANOVA comparing healthy subjects and PD-off patients showed the significant effects of Task (F(2, 48) = 82.7, p < 0.001) and
Discussion
The perceived timing of motor intention but not action was significantly delayed in the PD patients than in the age-matched healthy controls. Since the simple timing perception itself measured by S and M judgment tasks was not disturbed, the shortened W-time of the present study may be associated with the delayed and disrupted generation of motor intention in PD patients.
Previous studies on the motor intention suggested the importance of the fronto-parietal network (Cunnington et al., 2002, Lau
Acknowledgement
This study was partly supported by Grant-in-Aid for Scientific Research (B) 24300192 (to T.M.) from the Japan Society for the Promotion of Science.
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