Emotion recognition impairment and apathy after subthalamic nucleus stimulation in Parkinson's disease have separate neural substrates

Abstract

Objective

To test the hypothesis that emotion recognition and apathy share the same functional circuit involving the subthalamic nucleus (STN).

Methods

A consecutive series of 17 patients with advanced Parkinson's disease (PD) was assessed 3 months before (M − 3) and 3 months (M + 3) after STN deep brain stimulation (DBS). Mean (±S.D.) age at surgery was 56.9 (8.7) years. Mean disease duration at surgery was 11.8 (2.6) years. Apathy was measured using the Apathy Evaluation Scale (AES) at both M−3 and M3. Patients were also assessed using a computerised paradigm of facial emotion recognition [Ekman, P., & Friesen, W. V. (1976). Pictures of facial affect. Palo Alto: Consulting Psychologist Press] before and after STN DBS. Prior to this, the Benton Facial Recognition Test was used to check that the ability to perceive faces was intact.

Results

Apathy had significantly worsened at M3 (42.5 ± 8.9, p = 0.006) after STN-DBS, in relation to the preoperative assessment (37.2 ± 5.5). There was also a significant reduction in recognition percentages for facial expressions of fear (43.1% ± 22.9 vs. 61.6% ± 21.4, p = 0.022) and sadness (52.7% ± 19.1 vs. 67.6% ± 22.8, p = 0.031) after STN DBS. However, the postoperative worsening of apathy and emotion recognition impairment were not correlated.

Conclusions

Our results confirm that the STN is involved in both the apathy and emotion recognition networks. However, the absence of any correlation between apathy and emotion recognition impairment suggests that the worsening of apathy following surgery could not be explained by a lack of facial emotion recognition and that its behavioural and cognitive components should therefore also be taken into consideration.

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 (Parsons, Rogers, Braaten, Woods, & Troster, 2006), behavioural and emotional impairments (Temel et al., 2005) associated with STN DBS in PD.

One of the major concerns in this area is the occurrence of apathy after STN DBS in PD. Most previous studies dealing with apathy have had methodological limitations, either due to a lack of specific tools to assess apathy (Saint-Cyr, Trepanier, Kumar, Lozano, & Lang, 2000; Trepanier, Kumar, Lozano, Lang, & Saint-Cyr, 2000) or because of a failure to include a control group in the experimental design (Funkiewiez et al., 2004, Volkmann et al., 2001). Our group, however, reported that apathy could be induced by STN DBS (Drapier et al., 2006) in PD after comparing the patient group with a control group of Parkinsonian patients who met the surgical criteria but were still on the waiting list for surgery.

Apathy is clinically defined as a decrease in or lack of motivation, interest or emotions, which cannot be ascribed to any impairment of consciousness or any emotional or cognitive disorder (Marin, 1991). This led Marin (1990) to define three main domains for characterising apathy: behaviour, emotion and cognition, as reflected in the Apathy Evaluation Scale. According to the multicomponential view, emotions are defined as “episodes of massive, synchronized recruitment of mental and somatic resources allowing to adapt to or cope with a stimulus event subjectively appraised as being highly pertinent to the needs, goals, and values of the individuals” (Scherer, Schorr, & Johnstone, 2001). Our group has demonstrated that, when it comes to facial expressions of emotions, fear recognition is impaired by STN DBS in PD (Biseul et al., 2005, Le Jeune et al., 2008), implying that the STN could be involved in the fear recognition circuit, either via computation within the STN or by virtue of its impact on other limbic territories.

The STN's involvement in emotional processing has been suggested by other prospective studies, which have reported a selective reduction in the recognition of negative emotion following STN DBS in PD (Dujardin et al., 2006, Schroeder et al., 2004) but also by perioperative studies, such as that conducted by Kühn et al. (2005), which showed a differential and dynamic modulation of STN potential in response to the presentation of affective pictures. However, Kühn et al.'s result has to 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.

Apathy is an important psychiatric component of PD (Aarsland et al., 1999, Cummings et al., 1994) which can be defined clinically as a lack of reaction to emotional stimuli. Thus, apathy appears to take the form of a complex emotional withdrawal with emotional, behavioural and cognitive dimensions (Marin, 1991), which may be aggravated by STN DBS. Emotion recognition is also impaired after STN DBS. In the light of our previous findings (Biseul et al., 2005, Drapier et al., 2006, Le Jeune et al., 2008) the aim of this study was to examine whether apathy/emotional withdrawal can be explained by a facial emotion recognition impairment. This would imply that apathy emotional withdrawal and facial expression recognition networks at least share some common circuits passing through the STN. Furthermore, we wanted to test whether the emotional dimension is actually the major disorder in apathy and whether it influences the other – cognitive and behavioural – dimensions of apathy.