Abstract

BackgroundThere appears to be an overlap between the limbic system, which is modulated by subthalamic nucleus (STN) deep brain stimulation (DBS) in Parkinson's disease (PD), and the brain network that mediates theory of mind (ToM). Accordingly, the aim of the present study was to investigate the effects of STN DBS on ToM of PD patients and to correlate ToM modifications with changes in glucose metabolism.Methodology/Principal FindingsTo this end, we conducted 18FDG-PET scans in 13 PD patients in pre- and post-STN DBS conditions and correlated changes in their glucose metabolism with modified performances on the Eyes test, a visual ToM task requiring them to describe thoughts or feelings conveyed by photographs of the eye region. Postoperative PD performances on this emotion recognition task were significantly worse than either preoperative PD performances or those of healthy controls (HC), whereas there was no significant difference between preoperative PD and HC. Conversely, PD patients in the postoperative condition performed within the normal range on the gender attribution task included in the Eyes test. As far as the metabolic results are concerned, there were correlations between decreased cerebral glucose metabolism and impaired ToM in several cortical areas: the bilateral cingulate gyrus (BA 31), right middle frontal gyrus (BA 8, 9 and 10), left middle frontal gyrus (BA 6), temporal lobe (fusiform gyrus, BA 20), bilateral parietal lobe (right BA 3 and right and left BA 7) and bilateral occipital lobe (BA 19). There were also correlations between increased cerebral glucose metabolism and impaired ToM in the left superior temporal gyrus (BA 22), left inferior frontal gyrus (BA 13 and BA 47) and right inferior frontal gyrus (BA 47). All these structures overlap with the brain network that mediates ToM.Conclusion/SignificanceThese results seem to confirm that STN DBS hinders the ability to infer the mental states of others and modulates a distributed network known to subtend ToM.

Highlights

  • High-frequency deep brain stimulation (DBS) of the subthalamic nucleus (STN) constitutes a therapeutic advance for severely disabled patients with Parkinson’s disease (PD) in whom long-term pharmacological treatment has failed

  • We hypothesized that STN DBS would impair theory of mind (ToM), because of the overlap between the limbic system, which is modulated by STN DBS in PD, and the brain network that mediates ToM

  • The aim of the present study was to investigate the effects of STN DBS on the ToM abilities of PD patients

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Summary

Introduction

High-frequency deep brain stimulation (DBS) of the subthalamic nucleus (STN) constitutes a therapeutic advance for severely disabled patients with Parkinson’s disease (PD) in whom long-term pharmacological treatment has failed. A number of positron emission tomography (PET) studies of humans have confirmed these hypotheses, demonstrating modifications in cerebral activation and associating them with changes in cognitive function [9,10,11,12] and emotional impairment following STN DBS [13,14] These results suggest that the STN may be part of a broadly distributed neural network involved in associative and emotional processing, either via computation within the STN itself or by virtue of its impact on other associative/limbic territories. This network seems to encompass cortical regions, including the orbitofrontal cortex (OFC), temporal sulcus, temporal poles, cingulate gyrus and prefrontal cortex, and several subcortical regions, such as the amygdala and ventral striatum. The aim of the present study was to investigate the effects of STN DBS on ToM of PD patients and to correlate ToM modifications with changes in glucose metabolism

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