Motor symptom asymmetry in Parkinson's disease predicts emotional outcome following subthalamic nucleus deep brain stimulation

Abstract

The objective of this study was to explore the brain modifications associated with vocal emotion (i.e., emotional prosody) processing deficits in patients with Parkinson's disease after deep brain stimulation of the subthalamic nucleus, and the impact of motor asymmetry on these deficits. We therefore conducted 18-fluorodeoxyglucose positron emission tomography scans of 29 patients with left-or right-sided motor symptoms of Parkinson's disease before and after surgery, and correlated changes in their glucose metabolism with modified performances on the recognition of emotional prosody. Results were also compared with those of a matched healthy control group. Patients with more left-sided motor symptoms exhibited a deficit in vocal emotion recognition for neutral, anger, happiness and sadness in the preoperative condition that was normalized postoperatively. Patients with more right-sided motor symptoms performed comparably to controls in the preoperative condition, but differed significantly on fear postoperatively. At the metabolic level, the improvement observed among patients with left-sided motor symptoms was correlated with metabolic modifications in a right-lateralized network known to be involved in emotional prosody, while the behavioral worsening observed among patients with right-sided motor symptoms was correlated with metabolic modifications in the left parahippocampal gyrus and right cerebellum. We suggest that surgery has a differential impact on emotional processing according to motor symptom lateralization, and interpret these results as reflecting the (de)synchronization of the limbic loop in the postoperative condition.

Motor Symptom Asymmetry Predicts Non-motor Outcome and Quality of Life Following STN DBS in Parkinson's Disease

“…Third, from the results of Drapier, et al 7 , we predicted that DBS would bring about an improvement in quality of life and that this improvement would be driven by the physical quality-of-life subscore. This improvement would be signi cant only in RPD patients, driven by a signi cant improvement in their motor symptoms, as observed by Voruz, et al 15 .…”

“…The aim of the present study was to investigate the cognitive, neuropsychiatric, and quality-of-life pro les of patients with PD 12 months after STN DBS as a function of motor symptom asymmetry. According to recent research 15 , motor symptom asymmetry could be a meaningful predictor of non-motor performance following surgery. The present results seem to indicate that, at 12 months, DBS does not have a detrimental effect on cognitive measures for RPD patients (with inferred left cerebral pathology), whereas we did observe a harmful effect for LPD patients compared with HCs.…”

“…Given STN functional anatomy, these results suggest that DBS has a dissociative effect in the cognitive and affective domains, depending on motor symptom lateralization. Based on the integrative model of STN function put forward by Péron, et al 10 , the study by Voruz, et al 15 supports the notion that although STN DBS typically restores motor functions, the surgery/stimulation can unintentionally impair non-motor functions. In this study, RPD patients (with inferred left cerebral pathology) did not exhibit any emotional impairment prior to surgery (probably owing to right hemispheric specialization of the basal ganglia for vocal emotion processing 16 ), but developed emotional impairment in the wake of DBS.…”

“…From overall ndings in the literature, we made several predictions about the expected effects of motor symptom asymmetry on cognition, neuropsychiatric symptoms, and quality of life following DBS. First, on the basis of Voruz, et al 15 results in the neuropsychological domain, we expected to observe poorer performance on cognitive function tests post-DBS, but only for the LPD subgroup, with performance levels unchanged in the RPD subgroup. Second, we predicted that RPD patients would exhibit greater vulnerability to neuropsychiatric symptoms than would LPD patients and that DBS would have a bene cial effect on these symptoms in the RPD subgroup 15 .…”

“…Despite these indications of laterality effects in pre-DBS conditions, little research has been done on the non-motor impact of motor symptom asymmetry in patients post-DBS. In one recent study 15 , the authors found that LPD patients had impaired vocal emotion recognition for neutral, angry, happy, and sad voices before DBS that normalized after DBS, whereas RPD patients performed comparably to controls before DBS, but differed signi cantly on fear recognition after DBS. Although no signi cant difference was found between the RPD and LPD subgroups on any of the neuropsychological background tests in either the pre-or postoperative conditions, comparisons with healthy controls (HCs) suggested a potentially greater post-DBS deterioration in cognitive performance in LPD patients than in RPD patients.…”