An fMRI study into emotional processing in Parkinson's disease: Does increased medial prefrontal activation compensate for striatal dysfunction?

Abstract

Background: Apart from a progressive decline of motor functions, Parkinson's disease (PD) is also characterized by non-motor symptoms, including disturbed processing of emotions. This study aims at assessing emotional processing and its neurobiological correlates in PD with the focus on how medicated Parkinson patients may achieve normal emotional responsiveness despite basal ganglia dysfunction.

Methods: Nineteen medicated patients with mild to moderate PD (without dementia or depression) and 19 matched healthy controls passively viewed positive, negative, and neutral pictures in an event-related blood oxygen level-dependent functional magnetic resonance imaging study (BOLD-fMRI). Individual subjective ratings of valence and arousal levels for these pictures were obtained right after the scanning.

Results: Parkinson patients showed similar valence and arousal ratings as controls, denoting intact emotional processing at the behavioral level. Yet, Parkinson patients showed decreased bilateral putaminal activation and increased activation in the right dorsomedial prefrontal cortex (PFC), compared to controls, both most pronounced for highly arousing emotional stimuli.

Conclusions: Our findings revealed for the first time a possible compensatory neural mechanism in Parkinson patients during emotional processing. The increased medial PFC activity may have modulated emotional responsiveness in patients via top-down cognitive control, therewith restoring emotional processing at the behavioral level, despite striatal dysfunction. These results may impact upon current treatment strategies of affective disorders in PD as patients may benefit from this intact or even compensatory influence of prefrontal areas when therapeutic strategies are applied that rely on cognitive control to modulate disturbed processing of emotions.

Fig 1. Experimental design of the event-related emotional processing task.

Each trial started with a black screen with a white fixation cross, followed by a picture or null-event (fixation cross). After an inter-stimulus interval (fixation cross) a prompt appeared on the screen asking the participants whether the pictured contained a (part of a) human or not. The onsets of both the pictures and prompt were jittered in order to achieve optimal sampling of the hemodynamic response. Note that the pictures depicted in Fig 1 are not from the IAPS. In the actual experiment the words human/non-human were placed next to each other.

Fig 2. Results of the ROI analysis on the processing of low and high arousing stimuli in Parkinson patients and controls.

Contrasting healthy controls (HCs) with Parkinson patients (PD) showed a differential increase of BOLD signal for HCs in the left (posterior) putamen for low arousal (A) and bilaterally in the putamen for high arousal (B, all P_SVC<0.05). Contrasting Parkinson patients with healthy controls revealed an increased BOLD signal for Parkinson patients in the right dorsomedial prefrontal cortex (dmPFC) for low (C) arousal and high arousal (D, all P_SVC<0.05).