Abstract
Freezing of gait (FOG) is often experienced in advanced stages of Parkinson's disease (PD) and can lead to an increased risk of falls. Although spatiotemporal characteristics of FOG are well-described, their underlying neuromuscular mechanisms remain poorly understood. Several studies have demonstrated an abnormal activation of distal muscles of the lower limb and coordination impairments during gait in people with PD (pwPD). However, few have investigated how various characteristics of electromyograms (EMGs) change before, during and after a freezing episode (FE). Our objective was to quantify changes in proximal and distal leg muscle activity associated with FEs. In this study, 12 pwPD, confirmed as freezers, performed a repetitive stepping-in-place task used to elicit FE. Surface EMGs were collected from proximal [rectus femoris and biceps femoris (BF)] and distal [tibialis anterior (TA) and gastrocnemius medialis (GM)] muscles. Data epochs of 500 ms were extracted from EMG time series at four different periods: baseline, 2 s before a FE, during a FE, and 2 s after a FE. For each epoch, EMG amplitude [root-mean-square (RMS)], variability [coefficient of variation (CoV)], and inter-muscle functional connectivity (mutual information) were quantified. Results from the analysis of 21 FEs show a significant main effect of Period for EMG amplitude in bilateral TA and in the least affected GM (p < 0.01), with decreased activation before freezing that remained low during and after the FE. On the other hand, a main effect of Period was also found in bilateral BF muscles (p < 0.01) but with increased activation before freezing that was generally sustained during and after FE. Main effects of Period were also found for all measures of variability, except for the least affected GM, showing reduced variability during the FE that returned to baseline in all muscles except both TA. Moreover, an increase in functional connectivity between the least affected distal muscles was seen before the FE. Our findings confirm that many characteristics of EMG patterns of both distal and proximal leg muscles change throughout periods of a FE, suggesting both impairment and adaptive strategies from proximal muscles.
Highlights
Parkinson’s disease (PD) is a degenerative, progressive motor system disorder caused by the loss of nigro-striatal neurons
Schlenstedt et al [24] recently observed a higher hip co-contraction between left and right tensor fasciae latae in a group of people with PD (pwPD) with freezing compared to a group of pwPD who did not experience freezing during anticipatory postural adjustments prior gait initiation. They reported higher gastrocnemius medialis (GM) activity in pwPD with freezing compared to a healthy control group. All these findings indicate that gait initiation deficits seen in PD are a consequence of impaired anticipatory postural adjustments that are characterized by abnormal timing and amplitude activation of postural muscles, including tibialis anterior (TA) and GM
Our results of EMG amplitude suggest that the decrease in the activation of both TA muscles before the freezing episode (FE) may reduce stability, which is consistent with previous results showing that deficits in gait initiation in PD are a consequence of an abnormal activation timing and decrease activation of TA muscles [22,23,24] and that poor balance and falls in elderly are related to a loss of capabilities of strength and power of the ankle dorsiflexors [38, 39]
Summary
Parkinson’s disease (PD) is a degenerative, progressive motor system disorder caused by the loss of nigro-striatal neurons. PD is associated to various impairments in motor function. Present in the latest stages of the disease, FOG has been described as the inability to complete a step regardless of the intention to move [4]. It is one of the most disabling symptoms of PD [5,6,7,8]. Some characteristics of FOG such as high-frequency, decreased step amplitudes, trembling-like leg movements, and gait festination, have been well-described [4, 7, 9], the causes of FOG remain unknown
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