Emotional auditory stimuli influence step initiation in Parkinson's disease with freezing of gait

Abstract

Freezing of gait (FOG) in Parkinson's disease (PD) can be triggered by sensomotor, cognitive or limbic factors. The limbic system's impact on FOG is attributed to elevated limbic load, characterized by aversive stimuli, potentially depleting cognitive resources for movement control, resulting in FOG episodes. However, to date, PD patients with and without FOG have not shown alterations of anticipatory postural adjustments during gait initiation after exposure to emotional images, possibly because visual stimuli are less immediately disruptive than auditory stimuli, which can more directly affect attention and the limbic system. This study aims to determine if step initiation is influenced by ecological auditory stimuli with emotional content in patients with FOG compared to those without. Forty-five participants, divided into 3 groups (15 PD with FOG, 15 PD without FOG in ON state, and 15 healthy subjects), stood on a force platform and were asked to step forward in response to neutral, pleasant, or unpleasant ecological auditory stimuli. Anticipatory postural adjustments were investigated in imbalance and unloading phases, while spatio-temporal parameters, including center of pressure (CoP) displacements, were computed for step initiation. PD with FOG showed a reduction of CoP displacements after listening to unpleasant stimuli. Conversely, pleasant stimuli facilitated CoP displacements in these subjects. No influence of affective stimuli on CoP displacements was found in the other two groups. Multiple regression analysis revealed that the behavioral pattern in PD with FOG, modulated by stimuli with affective valence, was mainly associated with the limbic area (i.e., depression). The findings showed that the emotional network plays a crucial role in the pathophysiology of freezing, generating probably interference with attentional reserves that trigger FOG.

Keywords: Auditory stimuli; Center of pressure; Emotions; Freezing of gait; Gait initiation.

Fig. 1

(A) Cartoon of experimental task. (B) Center of Pressure (COP) displacement. The COP trace from APA onset to APA end (i.e., toe off) is reported. Unloading phase is represented by the red line and the imbalance phase by the green line. Swing phase is depicted by the light blue line.

Fig. 2

Center of Pressure (COP) displacements during emotional gait initiation task for the imbalance (Panels A, B) and unloading (Panels C, D) phases. COP data [Median values and IQR] are reported on Y axes. Group values are shown in the left panel (1), and the experimental conditions (B, N, P, U) are displayed in the remaining panels on the X-axes (HC: (2), PD: (3), PD-FOG: (4)). HC healthy control, PD Parkinson’s Disease, FOG freezing of gait, AP antero-posterior, ML medio-lateral. Asterisks indicate significant difference (*p < 0.05, **p < 0.01).

Fig. 3

The graphs show the differential behavior of the Center Of Pressure (COP) displacements during gait initiation task in response to unpleasant and pleasant, and for each group. AP (Panels A, C) and ML (Panels B, D). CoP displacements [Median values and IQR] are reported on Y axes. FOG freezing of gait, AP antero-posterior, ML medio-lateral. Asterisks indicate significant difference (*p < 0.05, **p < 0.01).