Subliminal gait initiation deficits in rapid eye movement sleep behavior disorder: A harbinger of freezing of gait?

Abstract

Background: Muscle activity during rapid eye movement sleep is markedly increased in people with rapid eye movement sleep behavior disorder and people with Parkinson's disease (PD) who have freezing of gait. This study examined whether individuals with rapid eye movement sleep behavior disorder who do not have a diagnosis of PD show abnormalities in gait initiation that resemble the impairments observed in PD and whether there is a relationship between these deficits and the level of rapid eye movement sleep without atonia.

Methods: Gait initiation and polysomnography studies were conducted in 4 groups of 10 participants: rapid eye movement sleep behavior disorder, PD with and without freezing of gait, and controls.

Results: Significant reductions were seen in the posterior shift of the center of pressure during the propulsive phase of gait initiation in the groups with rapid eye movement sleep behavior disorder and PD with freezing of gait when compared with controls and PD nonfreezers. These reductions negatively correlated with the amount of rapid eye movement sleep without atonia. The duration of the initial dorsiflexor muscle burst during gait initiation was significantly reduced in both PD groups and the rapid eye movement sleep behavior disorder cohort.

Conclusions: These results provide evidence that people with rapid eye movement sleep behavior disorder, prior to a diagnosis of a degenerative neurologic disorder, show alterations in the coupling of posture and gait similar to those seen in PD. The correlation between increased rapid eye movement sleep without atonia and deficits in forward propulsion during the push-off phase of gait initiation suggests that abnormities in the regulation of muscle tone during rapid eye movement sleep may be related to the pathogenesis of freezing of gait. © 2016 International Parkinson and Movement Disorder Society.

Keywords: PD; RBD; freezing; gait; sleep.

Figure 1. Example of the primary outcome variables measured during gait initiation in a control subject

A. Vertical ground reaction forces (GRFs) generated by the stepping (right leg, solid line) and stance leg (left, dashed line). B. Center of pressure excursion (CoP) in the anterior-posterior (solid line) and rightward-leftward (dashed line) directions. Note there are often two distinct peaks in the posterior excursion. The first peak usually coincides with the peak loading and unloading of the step and stance legs respectively, and the second peak usually occurs near step leg toe-off. C. Example of the initial burst of EMG activity in the tibialis anterior (TA) muscle. RTO = right toe off.

Figure 2

A. Examples of five consecutive trials of self-initiated gait in a representative subject from each group. The top row shows right (step leg) and left (stance leg) vertical ground reaction forces (GRFs). Each trial has been aligned to the onset of the initial increase in the right GRF at 1000ms. Note the consistency and smoothness of the profiles in the control subject compared with the presence of multiple inflections, hesitations and reduced magnitude of the profiles in the PD-FOG, PD+FOG and RBD subjects. The bottom row shows the anterior-posterior and medial-lateral excursions of the net CoP. The red line with an arrow highlights the initial trajectory of the CoP during the APA phase for one trial. B. Changes in the magnitude of the vertical GRFs and the net center of pressure (CoP) excursion across groups. Summary of the mean peak amplitudes of the dependent variables across groups during self-initiated gait: (A) stepping leg loading force, (B) stance leg unloading force, (C) peak rightward excursion of the center of pressure, (D) first and second peaks of the posterior excursion of the CoP. * = significantly different from controls at the p<0.05 level, § = significantly different from the PD-FOG group at the p<0.05 level. Error bars are one standard error. (CON = control subjects, PD-FOG = PD without FOG, PD+FOG = PD with FOG, RBD = REM sleep behavior disorder).

Figure 3

A. Muscle activation patterns in the tibialis anterior (TA) muscle during gait initiation. Representative examples of vertical ground reaction forces (left column) on the stepping (solid line) and stance (dashed line) legs and TA EMG (right column) in a control, PD-FOG, PD+FOG and RBD subject. Plots have been aligned to the start of the APA at time = 0 ms. Note the fused and prolonged first burst of activity in the TA muscle in the control subject compared to an initial short duration burst, followed by addition bursts in all other groups. RTO = right toe-off, LTO = left toe-off. B. Group averages of the mean duration of the first burst in the TA muscle. The first burst duration was significantly reduced in the PD-FOG, PD+FOG and RBD groups compared with controls, and both PD groups compared with the RBD group. * = significantly different from controls at the p<0.05 level, + = significantly different from the RBD group at the p<0.05 level. Error bars are one standard error. (CON = control subjects, PD-FOG = PD without FOG, PD+FOG = PD with FOG, RBD = REM sleep behavior disorder)