Elsevier

Neuropsychologia

Volume 48, Issue 4, March 2010, Pages 1053-1062
Neuropsychologia

Recognition of emotional prosody is altered after subthalamic nucleus deep brain stimulation in Parkinson's disease

https://doi.org/10.1016/j.neuropsychologia.2009.12.003Get rights and content

Abstract

The recognition of facial emotions is impaired following subthalamic nucleus (STN) deep brain stimulation (DBS) in Parkinson's disease (PD). These changes have been linked to a disturbance in the STN's limbic territory, which is thought to be involved in emotional processing. This was confirmed by a recent PET study where these emotional modifications were correlated with changes in glucose metabolism in different brain regions, including the amygdala and the orbitofrontal regions that are well known for their involvement in emotional processing. Nevertheless, the question as to whether these emotional changes induced by STN DBS in PD are modality-specific has yet to be answered. The objective of this study was therefore to examine the effects of STN DBS in PD on the recognition of emotional prosody.

An original emotional prosody paradigm was administered to twenty-one post-operative PD patients, twenty-one pre-operative PD patients and twenty-one matched controls. Results showed that both the pre- and post-operative groups differed from the healthy controls. There was also a significant difference between the pre and post groups. More specifically, an analysis of their continuous judgments revealed that the performance of the post-operative group compared with that of the other two groups was characterized by a systematic emotional bias whereby they perceived emotions more strongly.

These results suggest that the impaired recognition of emotions may not be specific to the visual modality but may also be present when emotions are expressed through the human voice, implying the involvement of the STN in the brain network underlying the recognition of emotional prosody.

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. Although there is growing evidence of the beneficial effects of chronic DBS on PD motor symptoms, several clinical studies have reported cognitive (For a review, see Parsons, Rogers, Braaten, Woods, & Troster, 2006), behavioural and emotional impairments (For a review, see Temel et al., 2006) associated with STN DBS in PD.

Clinical studies have revealed that the recognition of facial expressions of emotions is impaired following STN DBS in PD (Biseul et al., 2005, Drapier et al., 2008, Dujardin et al., 2004, Le Jeune et al., 2008, Péron et al., in press, Schroeder et al., 2004). Although the materials and procedure differed across studies, it has been argued that one consistent finding is that the impairment seems to selectively concern negative emotions. Anger recognition was found to be selectively impaired in Schroeder et al.’s study (2004), recognition of three negative emotions (anger, disgust, sadness) was impaired in Dujardin et al.’s study (Dujardin et al., 2004), fear recognition was selectively impaired in Biseul et al.’s study (Biseul et al., 2005), and fear and sadness were impaired in Drapier et al. and Péron et al.’s studies (Drapier et al., 2008, Péron et al., in press). Nevertheless, the selective nature of the disruption of negative emotions following STN DBS in PD remains under debate. For instance, the design of the above-mentioned studies appears to have been biased towards negative emotions. While they always had several negative stimuli, they only had one positive stimulus (happiness), so there was a greater likelihood of misusing a negative scale. Another important finding is that the impairment cannot be attributed to secondary variables, such as anxiety or depression, a visuospatial deficit or general cognitive decline. These results suggest that the STN may be part of a broadly distributed neural network involved in the recognition of facial expressions, either via computation within the STN itself or by virtue of its impact on other brain regions involved in emotional processing, such as the orbitofrontal cortices and the amygdala (for a review, see for e.g., Adolphs, Damasio, Tranel, & Damasio, 1996).

STN involvement in emotional processing has also been suggested by intraoperative studies, such as that conducted by Kuhn et al. (2005), which showed a differential and dynamic modulation of STN potentials in response to the presentation of affective pictures. However, Kühn et al.’s result should be viewed with caution, as some parameters, such as the visual stimulus features, were not properly controlled in the study and could therefore account for this result (Delplanque, N’Diaye, Scherer, & Grandjean, 2007).

PET studies have also been conducted in order to test the hypothesis of the involvement of the STN in the recognition of facial expressions (Geday et al., 2006, Le Jeune et al., 2008). In one of them (Le Jeune et al., 2008), our group recently obtained a positive correlation between a reduction in the recognition of fearful facial expressions following STN DBS and changes in glucose metabolism, especially in the right orbitofrontal cortex, using 18FDG-PET. These results suggest that the STN is a key basal ganglia structure in brain circuits involved in emotional processing.

Nevertheless, this research has left several questions unanswered and it has yet to be determined whether these emotional changes induced by STN DBS in PD are modality-specific or supramodal. Whereas previous studies have focused on the influence of STN stimulation on the recognition of emotional facial expressions, the present study examined the effects of STN stimulation on the recognition of emotional expressions conveyed by the human voice i.e., the recognition of emotional prosody.

Emotional prosody is defined as modifications in segmental and supra-segmental speech parameters during an emotional episode (Grandjean, Banziger, & Scherer, 2006). Physiological modifications in the vocal tract and vocal folds during an emotional episode, such as modifications in the tension of the vocal folds related to vagus nerve activity or in the tension of the soft palate, induce modulations in different acoustic components of the human voice (Ghazanfar and Rendall, 2008, Grandjean et al., 2006). These voice modulations can be studied and described in terms of modifications in acoustic parameters such as fundamental frequency, amplitude and distribution of energy across different frequency bands. These objective acoustic measures correspond, at the level of perception, to the modulations in intonation (i.e. pitch), loudness and voice quality perceived by the listener. Investigations of the perception of emotional prosody through fMRI and patient studies have allowed researchers to delineate a distributed neural network involved in the identification and recognition of emotional prosody. In addition to primary and secondary auditory regions, modulation of neuronal activity within the superior temporal sulcus and gyrus has also been reported in response to exposure to emotional prosodic stimuli (Ethofer et al., 2006b, Grandjean et al., 2005, Sander et al., 2005). An increase in activity within the amygdala has also been observed, not only in response to emotional prosody (Grandjean et al., 2005, Sander et al., 2005) but also in response to emotional animal vocalizations (Fecteau, Belin, Joanette, & Armony, 2007). Modulations in activity within anterior regions, such as the orbitofrontal cortex and inferior frontal areas, have been described, especially when participants pay attention to an auditory stimulus or are asked to identify emotional prosody (Ethofer et al., 2006a, Sander et al., 2005, Wildgruber et al., 2004). Recently, a study of neglect patients confirmed that these regions – the superior temporal sulcus and gyrus and the orbitofrontal cortex – are important for detecting emotional voices in the environment (Grandjean, Sander, Lucas, Scherer, & Vuilleumier, 2008). In addition to these regions, the involvement of the basal ganglia in the processing of emotional prosody, particularly the caudate nucleus and putamen, has also been revealed by fMRI and patient studies (Bach et al., 2008, Grandjean et al., 2005, Kotz et al., 2003, Morris et al., 1999).

These findings highlight the overlap between the neuroanatomical substrates of the recognition of emotional prosody and the neuroanatomical circuit that STN DBS is thought to modify, particularly the amygdala and the orbitofrontal cortex regions (Le Jeune et al., 2008). Accordingly, in the present study, we hypothesized that the impaired recognition of emotions in PD patients following STN DBS is not specific to the visual sensory modality but is also present when emotions are expressed through the human voice.

To test this hypothesis, we explored the recognition of emotions in the vocal modality, using an original emotional prosody paradigm, in twenty-one PD patients in a pre-operative condition, twenty-one PD patients in a post-operative condition, and twenty-one matched healthy controls (HC).

Section snippets

Participants (Table 1)

Two groups of patients with PD (pre-operative and post-operative groups) and a HC group took part in the study.

All patients met the clinical criteria of the United Kingdom Parkinson's Disease Society Brain Bank for Idiopathic PD (Hughes, Daniel, Kilford, & Lees, 1992). The first patient group included 21 patients (10 men, 11 women) with advanced PD who were candidates for STN DBS (pre-operative group), while the second included 21 patients (10 men, 11 women) who had already undergone bilateral

Motor, neuropsychological and psychiatric assessments (Tables 1 and 3)

The analysis failed to reveal any significant difference between the two PD patient groups for any of the variables of the motor assessment, except for the Schwab & England score in the “On” condition, and there was no significant difference between the three groups for any of the variables of the neuropsychological background assessment. Interestingly, there was a significant difference between the UPDRS III ‘off-dopa–off-stim’ and ‘off-dopa–on-stim’ scores in the post-operative PD patient

Discussion

The aim of the present study was to explore the recognition of emotions in the vocal modality (i.e. emotional prosody) in PD following STN DBS, in order to measure the extent to which the disruption in emotion recognition observed after this type of neurosurgery are specific to the visual modality or are also present in the auditory modality. We explored performances on the recognition of emotions from voices by comparing the ratings given by a pre-operative, a post-operative and an HC group (n =

Conflict of interest

The authors report no conflicts of interest.

Acknowledgements

We would like to thank the patients and normal controls for contributing their time to this study, Mme Wiles-Portier for preparing the manuscript, and the Ear, Nose and Throat Department of Rennes University Hospital for conducting the hearing tests.

This study was funded by the Neurology Unit of Pontchaillou University Hospital in Rennes, France (Prof. G. Edan) and the Swiss Centre for Affective Sciences in Geneva, Switzerland.

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