Compensatory activity in the extrastriate body area of Parkinson's disease patients

Abstract

Compensatory mechanisms are a crucial component of the cerebral changes triggered by neurodegenerative disorders. Identifying such compensatory mechanisms requires at least two complementary approaches: localizing candidate areas using functional imaging, and showing that interference with these areas has behavioral consequences. Building on recent imaging evidence, we use this approach to test whether a visual region in the human occipito-temporal cortex-the extrastriate body area-compensates for altered dorsal premotor activity in Parkinson's disease (PD) during motor-related processes. We separately inhibited the extrastriate body area and dorsal premotor cortex in 11 PD patients and 12 healthy subjects, using continuous theta burst stimulation. Our goal was to test whether these areas are involved in motor compensatory processes. We used motor imagery to isolate a fundamental element of motor planning, namely subjects' ability to incorporate the current state of their body into a motor plan (mental hand rotation). We quantified this ability through a posture congruency effect (i.e., the improvement in subjects' performance when their current body posture is congruent to the imagined movement). Following inhibition of the right extrastriate body area, the posture congruency effect was lost in PD patients, but not in healthy subjects. In contrast, inhibition of the left dorsal premotor cortex reduced the posture congruency effect in healthy subjects, but not in PD patients. These findings suggest that the right extrastriate body area plays a compensatory role in PD by supporting a function that is no longer performed by the dorsal premotor cortex.

Figures

Figure 1.

Task setup. A, Time line of the experimental procedures. MEP measurements were collected before and after performance of a motor imagery task. The task was performed before and after delivery of cTBS over PMd or EBA (on 2 different days). The MEP measurements taken before and after the first motor imagery task were combined into a single measure (“cTBS baseline”) for each experimental session. B, Motor imagery task. Participants had to judge whether the stimulus presented on a computer screen was a left or right hand, pressing one of two buttons with the corresponding left or right foot. Every 12 trials, subjects were instructed to assume a particular posture with their left and right hands. This manipulation of spatial congruency between the hand drawing and the current posture of the subject lead was coded as “matching” (left panel) when the side of the hand (palm or back) and the laterality (left or right) of the hand drawing corresponded with the hand position of the subject.

Figure 2.

Behavioral performance. A, Response times (mean ± SEM) during the baseline sessions as a function of group (healthy subjects or Parkinson's disease patients) and stimulus rotation (as illustrated by the hand drawings). Response times changed as a function of stimulus rotation for both groups. B, Response times (mean ± SEM) as a function of group (healthy subjects or Parkinson patients) and experimental session (baseline, after cTBS over EBA, and after cTBS over PMd). Response times decreased after either cTBS interventions, similarly for both groups. C, Response times (mean ± SEM) as a function of hand posture (healthy subjects or Parkinson patients) and experimental session (baseline, after cTBS over EBA, and after cTBS over PMd).

Figure 3.

Behavioral performance: effects of cTBS. Differences in RTs (mean in milliseconds ± SEM) between trials with nonmatching and matching configurations between subjects' own hands and hand drawings on display (posture congruency effect). Data are shown as a function of group and experimental session. cTBS over PMd reduced the posture congruency effect in the healthy subject group. cTBS over EBA reduced the posture congruency effect in the PD group.

Figure 4.

MEPs. Relative change in mean peak-to-peak amplitude of the MEPs, normalized to MEP amplitude measured at baseline. The first post-cTBS measurement (cTBS1) was performed 7 min after the end of cTBS, and before the onset of the motor imagery task. The second post-cTBS measurement (cTBS2) was performed after the end of the motor imagery task.