Subthalamic nucleus oscillations during vocal emotion processing are dependent of the motor asymmetry of Parkinson's disease.

The subthalamic nucleus (STN) is involved in different aspects of emotional processes and more specifically in emotional prosody recognition. Recent studies on the behavioral effects of deep brain stimulation (DBS) in patients with Parkinson's disease (PD) have uncovered an asymmetry in vocal emotion decoding in PD, with left-onset PD patients showing deficits for the processing of happy voices. Whether and how PD asymmetry affects STN electrophysiological responses to emotional prosody, however, remains unknown. In the current study, local field potential activity was recorded from eight left- and six right-lateralized motor-onset PD patients (LOPD/ROPD) undergoing DBS electrodes implantation, while they listened to angry, happy and neutral voices. Time-frequency decomposition revealed that theta (2-6 Hz), alpha (6-12 Hz) and gamma (60-150 Hz) band responses to emotion were mostly bilateral with a differential pattern of response according to patient's sides-of onset. Conversely, beta-band (12-20 Hz and 20-30 Hz) emotional responses were mostly lateralized in the left STN for both patient groups. Furthermore, STN theta, alpha and gamma band responses to happiness were either absent (theta band) or reduced (alpha and gamma band) in the most affected STN hemisphere (contralateral to the side-of onset), while a late low-beta band left STN happiness-specific response was present in ROPD patients and did not occur in LOPD patients. Altogether, in this study, we demonstrate a complex pattern of oscillatory activity in the human STN in response to emotional voices and reveal a crucial influence of disease laterality on STN low-frequency oscillatory activity.

Vocal emotion decoding in the subthalamic nucleus: An intracranial ERP study in Parkinson's disease.

Using intracranial local field potential (LFP) recordings in patients with Parkinson's disease (PD) undergoing deep brain stimulation (DBS), we explored the electrophysiological activity of the subthalamic nucleus (STN) in response to emotional stimuli in the auditory modality. Previous studies focused on the influence of visual stimuli. To this end, we recorded LFPs within the STN in response to angry, happy, and neutral prosodies in 13 patients with PD who had just undergone implantation of DBS electrodes. We observed specific modulation of the right STN in response to anger and happiness, as opposed to neutral prosody, occurring at around 200-300ms post-onset, and later at around 850-950ms post-onset for anger and at around 3250-3350ms post-onset for happiness. Taken together with previous reports of modulated STN activity in response to emotional visual stimuli, the present results appear to confirm that the STN is involved in emotion processing irrespective of stimulus valence and sensory modality.

Multimodal emotion perception after anterior temporal lobectomy (ATL).

In the context of emotion information processing, several studies have demonstrated the involvement of the amygdala in emotion perception, for unimodal and multimodal stimuli. However, it seems that not only the amygdala, but several regions around it, may also play a major role in multimodal emotional integration. In order to investigate the contribution of these regions to multimodal emotion perception, five patients who had undergone unilateral anterior temporal lobe resection were exposed to both unimodal (vocal or visual) and audiovisual emotional and neutral stimuli. In a classic paradigm, participants were asked to rate the emotional intensity of angry, fearful, joyful, and neutral stimuli on visual analog scales. Compared with matched controls, patients exhibited impaired categorization of joyful expressions, whether the stimuli were auditory, visual, or audiovisual. Patients confused joyful faces with neutral faces, and joyful prosody with surprise. In the case of fear, unlike matched controls, patients provided lower intensity ratings for visual stimuli than for vocal and audiovisual ones. Fearful faces were frequently confused with surprised ones. When we controlled for lesion size, we no longer observed any overall difference between patients and controls in their ratings of emotional intensity on the target scales. Lesion size had the greatest effect on intensity perceptions and accuracy in the visual modality, irrespective of the type of emotion. These new findings suggest that a damaged amygdala, or a disrupted bundle between the amygdala and the ventral part of the occipital lobe, has a greater impact on emotion perception in the visual modality than it does in either the vocal or audiovisual one. We can surmise that patients are able to use the auditory information contained in multimodal stimuli to compensate for difficulty processing visually conveyed emotion.