Antagonist muscle activity during reactive balance responses is elevated in Parkinson's disease and in balance impairment

Abstract

Background: Abnormal antagonist leg muscle activity could indicate increased muscle co-contraction and clarify mechanisms of balance impairments in Parkinson's disease (PD). Prior studies in carefully selected patients showed PD patients demonstrate earlier, longer, and larger antagonist muscle activation during reactive balance responses to perturbations.

Research question: Here, we tested whether antagonist leg muscle activity was abnormal in a group of PD patients who were not selected for phenotype and most of whom had volunteered for exercise-based rehabilitation.

Methods: We compared antagonist activation during reactive balance responses to multidirectional support-surface translation perturbations in 31 patients with mild-moderate PD (age 68±9; H&Y 1-3; UPDRS-III 32±10) and 13 matched individuals (age 65±9). We quantified modulation of muscle activity (i.e., the ability to activate and inhibit muscles appropriately according to the perturbation direction) using modulation indices (MI) derived from minimum and maximum EMG activation levels observed across perturbation directions.

Results: Antagonist leg muscle activity was abnormal in unselected PD patients compared to controls. Linear mixed models identified significant associations between impaired modulation and PD (P<0.05) and PD severity (P<0.01); models assessing the entire sample without referencing PD status identified associations with balance ability (P<0.05), but not age (P = 0.10).

Significance: Antagonist activity is increased during reactive balance responses in PD patients who are not selected on phenotype and are candidates for exercise-based rehabilitation. This activity may be a mechanism of balance impairment in PD and a potential rehabilitation target or outcome measure.

Fig 1. Translation perturbation paradigm and EMG tuning curves.

A: Schematic depiction of multidirectional support surface translation perturbations. Green and red perturbation directions correspond to those for which maximum values were observed most frequently for MGAS-R and those directly opposite (see D). B: Tuning curves from the nonPD and PD groups depicting mean EMG activity during the APRX time bin (70–450 ms after perturbation onset). Horizontal bars indicate perturbation direction ranges θ_max and θ₁₈₀ used for calculation of modulation index MI180. C. Examples of calculation of MI (Eq 1) and MI180 (Eq 2) for TA from two different participants.

Fig 2

Associations between PD (A) and Age (B) and impaired modulation in analyses of individual muscles. Associations are described as Odds Ratios (OR) calculated separately using both MI and MI180 modulation indices derived from both APR1 and APRX time bins. Solid lines and dots represent the OR and 95% confidence limits for modulation index MI; dashed lines and open dots represent modulation index MI180. Odds ratios > 1 (shaded area) indicate that the presence of the risk factor (PD or Age) is strongly associated with the presence of impaired modulation for that muscle.