Different effects of levodopa and subthalamic stimulation on emotional conflict in Parkinson's disease

Abstract

Parkinson's disease impairs the decoding of emotional stimuli reflecting alterations of the limbic cortico‐subcortical network. The objective of this study was to assess and compare the behavioral and electrophysiological effects of both levodopa and subthalamic stimulation on emotional processing in Parkinson's disease. Operated patients (n =16) and matched healthy subjects performed an emotional Stroop task, in which the emotion expressed by a face must be recognized while ignoring an emotional distractive word and that includes a neutral control sub‐task. Patients were tested in the four possible treatment conditions (off stim/off med; on stim/off med; off stim/on med; and on stim/on med). High‐resolution electroencephalography was recorded while performing the task. Patients made significantly more mistakes in facial emotion recognition than healthy subjects (p < .005). Untreated patients performed worse in the emotional trials than in the control sub‐task (p < .05). Fearful faces induced significantly slower reaction times than happy faces in patients (p = .0002), but not in the healthy subjects. The emotional Stroop effect with levodopa was significantly higher than with subthalamic stimulation when fearful faces were assessed (p = .0243). Conversely, treatments did not modulate the Stroop effect of the control sub‐task. EEG demonstrated that, compared with the untreated state, levodopa but not subthalamic stimulation significantly increases the amplitude of the event‐related potential N170 (p = .002 vs. p = .1, respectively), an electrophysiological biomarker of early aspects of facial processing. The activity of the N170 cortical sources within the right fusiform gyrus was increased by levodopa (p < .05) but not by stimulation. While levodopa normalizes the recognition of emotional facial expression and early EEG markers of emotional processing, subthalamic stimulation does not. Thus, operated patients require dopaminergic medication in addition to stimulation to treat emotional symptoms of Parkinson's disease.

Emotional Processing Impairments in Apathetic Patients with Parkinson’s Disease: An ERP Study in Early Time Windows

“…The N170 amplitude in PD patients can be increased by levodopa treatment, indicating an association of dopaminergic depletion and the early stages of emotional processing [47] and may support the poorer N170 indexes in apathetic patients in this study. Notably, the nonapathetic PD and HC groups showed larger N170 amplitudes in the right hemisphere than in the left hemisphere, while the amplitude showed no hemispheric difference in the apathetic PD group.…”

Effects of Subthalamic Nucleus Deep Brain Stimulation on Facial Emotion Recognition in Parkinson’s Disease: A Critical Literature Review

“…On the other hand, Mondillon et al [ 62 ] showed a greater benefit in FER performance when the two therapies (DBS and L-Dopa) were combined. Moreover, another study [ 121 ] found that levodopa reduced the reaction time in both the facial emotional and control Stroop subtasks in PD patients postoperatively. Another study [ 122 ], using an emotional valence-dependent categorization task a few days after surgery with the stimulator not yet turned on, showed that dopamine enhanced processing of pleasant information.…”

“…The majority of studies did not assess reaction times for FER tasks. A study [ 121 ] using an emotional Stroop task showed that stimulation (ON condition) significantly reduced reaction times, whereas another [ 45 ] showed longer reaction times specifically for disgust recognition irrespective of stimulation condition. The potential involvement of anxiety, depression, or apathy in FER impairment after DBS is another issue not widely addressed among studies possibly because patients with major affective disturbances were excluded preoperatively.…”

“…Emotional auditory stimuli evoked activity in the right ventral STN in an electrophysiological study [ 147 ]. Another study [ 121 ] reached the conclusion that STN DBS induced hypoactivation of the right fusiform gyrus. Moreover, an imaging study [ 66 ] showed that the inhibition of the activity of the lateral fusiform face area was the result of the stimulation of the right STN.…”

Deep Brain Stimulation of the Subthalamic Nucleus Influences Facial Emotion Recognition in Patients With Parkinson’s Disease: A Review

“…In all presented studies, patients received additional dopaminergic medication, which was applied supplementary to DBS (except for single patients). Some publications, however, tried to filter out L-Dopa-associated effects on facial recognition performance under DBS and deployed an experimental setting with alternating testing conditions for medication and DBS: (1) Med OFF/DBS OFF; (2) Med OFF/DBS ON; (3) Med ON/DBS OFF; (4) Med ON/DBS ON (Berney et al, 2007; Mondillon et al, 2012; Aiello et al, 2014; Mermillod et al, 2014; Martínez-Fernández et al, 2018). Two other studies reported data for facial recognition in three different conditions: for DBS ON and OFF and for medicated patients only (Schneider et al, 2003; McIntosh et al, 2015).…”