Attention to Automatic Movements in Parkinson's Disease: Modified Automatic Mode in the Striatum

Abstract

We investigated neural correlates when attending to a movement that could be made automatically in healthy subjects and Parkinson's disease (PD) patients. Subjects practiced a visuomotor association task until they could perform it automatically, and then directed their attention back to the automated task. Functional MRI was obtained during the early-learning, automatic stage, and when re-attending. In controls, attention to automatic movement induced more activation in the dorsolateral prefrontal cortex (DLPFC), anterior cingulate cortex, and rostral supplementary motor area. The motor cortex received more influence from the cortical motor association regions. In contrast, the pattern of the activity and connectivity of the striatum remained at the level of the automatic stage. In PD patients, attention enhanced activity in the DLPFC, premotor cortex, and cerebellum, but the connectivity from the putamen to the motor cortex decreased. Our findings demonstrate that, in controls, when a movement achieves the automatic stage, attention can influence the attentional networks and cortical motor association areas, but has no apparent effect on the striatum. In PD patients, attention induces a shift from the automatic mode back to the controlled pattern within the striatum. The shifting between controlled and automatic behaviors relies in part on striatal function.

Keywords: attentional networks; controlled pattern; dopamine depletion; neural correlates; putamen.

Figure 1.

Brain activity during the process of developing automatic movements and in the attention stage. Brain regions activated in early-learning (A), automatic (B), and attention (C) stages in healthy subjects (left column), and Parkinson's disease patients (right column) while performing a visuomotor association task (one-sample t-test, P < 0.05, FWE corrected). L, left; R, right.

Figure 2.

The interaction between group and experimental conditions on brain activation. The activations show the interaction between experimental conditions (early-learning, automatic, and attention) and group (patients and controls); repeated-measures ANOVA, P < 0.05, FWE corrected, Table 3). L, left; R, right; APu, anterior putamen; CB, cerebellum; DLPFC, dorsolateral prefrontal cortex; PG, precentral gyrus; PMC, premotor cortex; PPu, posterior putamen; PreC, precuneus; pre-SMA, rostral supplementary motor area.

Figure 3.

Differences of brain activation between automatic and early-learning stages in controls. Brain regions more activated in the early-learning than in the automatic stage (A), and more activated in the automatic than in the early-learning stage (B) while performing the visuomotor association task (post hoc t-test, P < 0.05, FWE corrected, Supplementary Table 1). L, left; R, right; ACC, anterior cingulate cortex; APu, anterior putamen; CB, cerebellum; CN, caudate nucleus; DLPFC, dorsolateral prefrontal cortex; IPL, inferior parietal lobule; PMC, premotor cortex; PPu, posterior putamen; pre-SMA, rostral supplementary motor area; SPL, superior parietal lobule.

Figure 4.

Differences of brain activation between 2 groups at the automatic stage. Brain regions more activated in the Parkinson's disease patients than in controls (A), and more activated in control than in patients (B) at the automatic stage (post hoc t-test, P < 0.05, FWE corrected, Supplementary Table 2). L, left; R, right; APu, anterior putamen; CB, cerebellum; DLPFC, dorsolateral prefrontal cortex; PG, precentral gyrus; PMC, premotor cortex; PPu, posterior putamen; pre-SMA, rostral supplementary motor area.

Figure 5.

Brain regions more activated when attending to an automatic movement. Brain regions more activated in attention than in automatic stage in controls (A), and Parkinson's disease patients (B) when performing the visuomotor association task (post hoc t-test, P < 0.05, FWE corrected). Attention to the automatic task increased activations in the right DLPFC (MNI coordinates 34, 43, 32), right ACC (6, 46, 11), and left pre-SMA (−10, 6, 55) in controls, and enhanced activity in the right DLPFC (42, 25, 34), bilateral PMC (−32, 2, 52, and 32, −6, 55), and right cerebellum (40, −55, −35) in patients compared with the automatic stage (Table 4). L, left; R, right; ACC, anterior cingulate cortex; CB, cerebellum; DLPFC, dorsolateral prefrontal cortex; PMC, premotor cortex; pre-SMA, rostral supplementary motor area.

Figure 6.

The effective connections in the DLPFC in each stage in each group. The influences from the right DLPFC on other task-related areas in the early-learning, automatic, and attention stages in controls (A) and Parkinson's disease patients (B). The results shown are the path coefficients between the ROIs and other regions that are significantly different from zero (two-sample t-test, P < 0.001, Table 5). The red lines indicate that the DLPFC had positive influences on other task-related areas. The thicker lines indicate stronger connections. L, left; R, right; ACC, anterior cingulate cortex; APu, anterior putamen; CB, cerebellum; CN, caudate nucleus; DLPFC, dorsolateral prefrontal cortex; IPL, inferior parietal lobule; M1, primary motor cortex; PMC, premotor cortex; PPu, posterior putamen; pre-SMA, rostral supplementary motor area; SMA, caudal supplementary motor area; SPL, superior parietal lobule.

Figure 7.

The effective connections in the M1 in each stage in each group. The influences the left M1 received from other task-related areas in the early-learning, automatic, and attention stages in controls (A) and Parkinson's disease patients (B). The results shown are the path coefficients between the ROIs and other regions that are significantly different from zero (two-sample t-test, P < 0.001, Table 6). The red lines indicate that the M1 received positive influences from other task-related areas. The blue lines indicate that the ACC had negative influence on M1. The thicker lines indicate stronger connections. L, left; R, right; ACC, anterior cingulate cortex; APu, anterior putamen; CB, cerebellum; CN, caudate nucleus; DLPFC, dorsolateral prefrontal cortex; IPL, inferior parietal lobule; M1, primary motor cortex; PMC, premotor cortex; PPu, posterior putamen; pre-SMA, rostral supplementary motor area; SMA, caudal supplementary motor area; SPL, superior parietal lobule.