Compensatory stepping in Parkinson's disease is still a problem after deep brain stimulation randomized to STN or GPi

Abstract

The effects of deep brain stimulation (DBS) on balance in people with Parkinson's disease (PD) are not well established. This study examined whether DBS randomized to the subthalamic nucleus (STN; n = 11) or globus pallidus interna (GPi; n = 10) improved compensatory stepping to recover balance after a perturbation. The standing surface translated backward, forcing subjects to take compensatory steps forward. Kinematic and kinetic responses were recorded. PD-DBS subjects were tested off and on their levodopa medication before bilateral DBS surgery and retested 6 mo later off and on DBS, combined with off and on levodopa medication. Responses were compared with PD-control subjects (n = 8) tested over the same timescale and 17 healthy control subjects. Neither DBS nor levodopa improved the stepping response. Compensatory stepping in the best-treated state after surgery (DBS+DOPA) was similar to the best-treated state before surgery (DOPA) for the PD-GPi group and the PD-control group. For the PD-STN group, there were more lateral weight shifts, a delayed foot-off, and a greater number of steps required to recover balance in DBS+DOPA after surgery compared with DOPA before surgery. Within the STN group five subjects who did not fall during the experiment before surgery fell at least once after surgery, whereas the number of falls in the GPi and PD-control groups were unchanged. DBS did not improve the compensatory step response needed to recover from balance perturbations in the GPi group and caused delays in the preparation phase of the step in the STN group.

Keywords: Parkinson's disease; balance; compensatory stepping; deep brain stimulation.

Fig. 1.

A: the subject stood quietly with arms folded (Ai) when the standing surface unexpectedly moved backward with a step velocity that forced the subject to make a compensatory step forward (Aii). B: examples of vertical force distribution changes under the feet during the perturbation and the categorization of anticipatory postural adjustments (APAs).

Fig. 2.

Preparation for compensatory stepping. A: % of trials categorized by their APA behavior for each of the groups. B and C: mean ± SE of the latency to foot-off (B) and forward displacement of center of mass (CoM) at the time of foot-off (C) for each condition. In B and C, the Parkinson's disease (PD) control group is shown in black, the PD-globus pallidus interna (GPi) group is white, the PD-subthalamic nucleus (STN) group is dark gray, and the healthy control (HC) group is light gray.

Fig. 3.

Execution phase of compensatory stepping: mean ± SE anterior-posterior (AP) length of the first step (A), average velocity of the first step (B), and total number of steps required to regain balance for the PD-control subjects (C). The PD-control group is shown in black, the PD-GPi group is white, the PD-STN group is dark gray, and the HC group is light gray.