Basal ganglia signal dynamics during continuous emotional stimulation in Parkinson’s disease

Introduction: The intrinsic response to emotions plays an important role in Parkinson’s disease (PD), shaping not only the non-motor but also the motor profile of the patient. Emotional stimuli are typically characterized by valence (positive or negative) and arousal (relative strength of the emotion). While many studies investigated the neurophysiological processing of emotions at the cortical level, the role of the basal ganglia is not well understood. Objective: To study the impact of prolonged exposure to different emotional stimuli on basal ganglia oscillatory activity in patients with PD. Methods: Eight PD patients chronically implanted with a sensing-enabled Deep Brain Stimulation (DBS) system in the Subthalamic nucleus (STN) were enrolled. Patients on their usual dopaminergic medication underwent multiple iterations of 2-minutes video-based emotional stimulation using a validated dataset of emotions with different valence and arousal content (joy, sadness, fear, erotic, neutral), as well as a white-screen/white-noise control condition. Local field potentials (LFP) were recorded in parallel from the STN in bipolar mode. Spectral data ranging from the theta (4-7 Hz) to the high-beta band (21-30 Hz) were analyzed in the context of the various emotional stimuli. Patients also underwent a complete neuropsychological evaluation to assess cognitive decline, anxiety, apathy, and empathy. Results: STN alpha band (8-13 Hz) activity was modulated by the emotional arousal level, with high-arousal stimuli reducing the alpha power compared to low-arousal stimuli. This effect was evident both for positive and negative valence stimuli, as well as in both hemispheres. Importantly, beta band activity was largely unaffected by the different emotional stimuli. Conclusion: Our findings expand on the important role of alpha oscillations in emotion processing at the subcortical level in PD and highlight its modulation by different emotional arousal levels. Importantly, our results are suggestive that the accuracy of beta-driven adaptive DBS might not be affected by various emotional stimuli in PD.