نقش حسی برای نقص احساسات صوتی در بیماری پارکینسون پس از تحریک تالاموس فرعی

Subthalamic nucleus (STN) deep brain stimulation in Parkinson's disease induces modifications in the recognition of emotion from voices (or emotional prosody). Nevertheless, the underlying mechanisms are still only poorly understood, and the role of acoustic features in these deficits has yet to be elucidated. Our aim was to identify the influence of acoustic features on changes in emotional prosody recognition following STN stimulation in Parkinson's disease. To this end, we analysed the performances of patients on vocal emotion recognition in pre-versus post-operative groups, as well as of matched controls, entering the acoustic features of the stimuli into our statistical models. Analyses revealed that the post-operative biased ratings on the Fear scale when patients listened to happy stimuli were correlated with loudness, while the biased ratings on the Sadness scale when they listened to happiness were correlated with fundamental frequency (F0). Furthermore, disturbed ratings on the Happiness scale when the post-operative patients listened to sadness were found to be correlated with F0. These results suggest that inadequate use of acoustic features following subthalamic stimulation has a significant impact on emotional prosody recognition in patients with Parkinson's disease, affecting the extraction and integration of acoustic cues during emotion perception.

By demonstrating that subthalamic nucleus (STN) deep brain stimulation (DBS) in Parkinson's disease induces modifications in emotion processing, previous research has made it possible to infer the functional involvement of the STN in this domain (see, Péron, Frühholz, Vérin, & Grandjean, 2013 for a review). STN DBS in Parkinson's disease has been reported to induce modifications in all the emotional components studied so far (subjective feeling, motor expression of emotion, arousal, action tendencies, cognitive processes, and emotion recognition), irrespective of stimulus valence (positive or negative) and sensory-input modality. In emotion recognition, for instance, these patients exhibit deficits or impairments both for facial emotion (Biseul et al., 2005, Drapier et al., 2008, Dujardin et al., 2004, Le Jeune et al., 2008, Péron et al., 2010a and Schroeder et al., 2004) and for vocal emotion: so-called emotional prosody ( Bruck, Wildgruber, et al., 2011 and Péron et al., 2010b). Emotional prosody refers to the suprasegmental and segmental changes that take place in the course of a spoken utterance, affecting physical properties such as amplitude, timing, and fundamental frequency (F0), the last of these being perceived as pitch (Grandjean, Banziger, & Scherer, 2006). An additional cue to emotion is voice quality, the percept derived from the energy distribution of a speaker's frequency spectrum, which can be described using adjectives such as shrill or soft, and can have an impact at both the segmental and the suprasegmental levels ( Schirmer & Kotz, 2006). Emotional prosody recognition has been shown to correlate with perceived modulations of these different acoustic features during an emotional episode experienced by the speaker. In the prototypical example illustrated in Fig. 1, taken from Schirmer and Kotz (2006), happiness is characterized by a rapid speech rate, by high intensity, and by mean F0 and F0 variability, making vocalizations sound both melodic and energetic. By contrast, sad vocalizations are characterized by a slow speech rate, by low intensity, and by mean F0 and F0 variability, but have high spectral noise, resulting in the impression of a broken voice ( Banse & Scherer, 1996). Thus, understanding a vocal emotional message requires the analysis and integration of a variety of acoustic cues. Full-size image (35 K) Fig. 1. Oscillograms (top panels) and spectrograms (bottom panels) of the German sentence “Die ganze Zeit hatte ich ein Ziel” (“During all this time I had one goal”). The sentence is shorter when produced with a happy prosody (2 sec) than with a sad one (2.2 sec). The speech is also louder, as can be seen by comparing the sound envelopes illustrated in the oscillograms. This envelope is larger (i.e., it deviates more from baseline) for happy than for sad prosody. Spectral differences between happy and sad prosody are illustrated in the spectrograms. The dark shading indicates the energy of frequencies up to 5000 Hz. The superimposed blue lines represent the fundamental frequency (F0) contour, which is perceived as speech melody. This contour shows greater variability and a higher mean for happy than for sad prosody. Reproduced with permission (N°3277470398909) from Schirmer and Kotz (2006). Figure options The perception and decoding of emotional prosody has been studied in functional magnetic resonance imaging (fMRI) and patient studies, allowing researchers to delineate a distributed neural network involved in the identification and recognition of emotional prosody (Ethofer, Anders, Erb, Droll, et al., 2006, Ethofer, Anders, Erb, Herbert, et al., 2006, Ethofer et al., 2011, Frühholz et al., 2012, Grandjean et al., 2008, Grandjean et al., 2005, Sander et al., 2005, Schirmer and Kotz, 2006 and Wildgruber et al., 2009). Accordingly, models of emotional prosody processing have long postulated that information is processed in multiple successive stages related to different levels of representations (see Witteman, Van Heuven, & Schiller, 2012 for a review). Following the processing of auditory information in the primary and secondary auditory cortices (Bruck, Kreifelts, et al., 2011 and Wildgruber et al., 2009), with the activation of predominantly right-hemispheric regions (Banse and Scherer, 1996 and Grandjean et al., 2006) (Stage 1), two successive stages of prosody decoding have been identified. The second stage, related to the representation of meaningful suprasegmental acoustic sequences, is thought to involve projections from the superior temporal gyrus (STG) to the anterior superior temporal sulcus (STS). These cortical structures have been identified as forming the so-called temporal voice-sensitive area ( Belin and Zatorre, 2000 and Grandjean et al., 2005) made up of voice-sensitive neuronal populations. In the third stage, emotional information is made available by the STS for higher order cognitive processes mediated by the right inferior frontal gyrus (IFG) ( Frühholz & Grandjean, 2013b) and orbitofrontal cortex (OFC) ( Ethofer, Anders, Erb, Herbert, et al., 2006, Grandjean et al., 2008, Sander et al., 2005 and Wildgruber et al., 2004). This stage appears to be related to the explicit evaluation of vocally expressed emotions. In addition to this frontotemporal network, increased activity has also been observed within the amygdaloid nuclei in response to emotional prosody (Frühholz et al., 2012, Frühholz and Grandjean, 2013a, Grandjean et al., 2005 and Sander et al., 2005). Although it was not their focus, these studies have also reported the involvement of subcortical regions (other than the amygdaloid nuclei) in the processing of emotional prosody, such as the thalamus (Wildgruber et al., 2004) and the basal ganglia (BG). The involvement of the caudate and putamen has repeatedly been observed in fMRI, patient, and electroencephalography studies (Bach et al., 2008, Frühholz et al., 2012, Grandjean et al., 2005, Kotz et al., 2003, Morris et al., 1999, Paulmann et al., 2008, Paulmann et al., 2009 and Sidtis and Van Lancker Sidtis, 2003). More recently, the studies exploring the emotional effects of STN DBS in Parkinson's disease have highlighted the potential involvement of the STN in the brain network subtending emotional prosody processing (Bruck, Wildgruber, et al., 2011; see also, Péron et al., 2013 for a review; Péron, Grandjean, et al., 2010). In the study by Péron, Grandjean, et al. (2010), an original emotional prosody paradigm was administered to post-operative Parkinson's patients, preoperative Parkinson's patients, and matched controls. Results showed that, compared with the other two groups, the post-operative group exhibited a systematic emotional bias, with emotions being perceived more strongly. More specifically, contrasts notably revealed that, compared with preoperative patients and healthy matched controls, the post-operative group rated “happiness” more intensely when they listened to fearful stimuli, and they rated “surprise” significantly more intensely when they listened to angry or fearful utterances. Interestingly, a recent high-resolution fMRI study in healthy participants reinforced the hypothesis that the STN plays a functional role in emotional prosody processing, reporting left STN activity during a gender task that compared angry voices with neutral stimuli (Frühholz et al., 2012 and Péron et al., 2013). It is worth noting that, while these results seem to confirm the involvement of the BG, with further supporting evidence coming from numerous sources (for a review, see Gray & Tickle-Degnen, 2010; see also Péron, Dondaine, Le Jeune, Grandjean, & Verin, 2012), most models of emotional prosody processing fail to specify the functional role of either the BG in general or the STN in particular, although some authors have attempted to do so. Paulmann et al. (2009), for instance, suggested that the BG are involved in integrating emotional information from different sources. Among other things, they are thought to play a functional role in matching acoustic speech characteristics such as perceived pitch, duration, and loudness (i.e., prosodic information) with semantic emotional information. Kotz and Schwartze (2010) elaborated on this suggestion by underlining the functional role of the BG in decoding emotional prosody. They postulated that these deep structures are involved in the rhythmic aspects of speech decoding. The BG therefore seem to be involved in the early stage, and above all, the second stage of emotional prosody processing (see earlier for a description of the multistage models of emotional prosody processing). From the emotional effects of STN DBS reported in the Parkinson's disease literature, Péron et al. (2013) have posited that the BG and, more specifically, the STN, coordinate neural patterns, either synchronizing or desynchronizing the activity of the different neuronal populations involved in specific emotion components. They claim that the STN plays “the role of neural rhythm organizer at the cortical and subcortical levels in emotional processing, thus explaining why the BG are sensitive to both the temporal and the structural organization of events” (Péron et al., 2013). Their model incorporates the proposal put forward by Paulmann et al. (2009) and elaborated on by Kotz and Schwartze (2010), but goes one step further by suggesting that the BG and, more specifically, the STN, are sensitive to rhythm because of their intrinsic, functional role as rhythm organizer or coordinator of neural patterns. In this context, the exact contribution of the STN and, more generally, the BG, to emotional prosody decoding remains to be clarified. More specifically, the questions of the interaction between the effects of STN DBS per se and the nature of the auditory emotional material (e.g., its acoustic features), as well as the impact that DBS might have on the construction of the acoustic object/auditory percept, has yet to be resolved. The influence of acoustic features on emotional prosody recognition in patients with Parkinson's disease undergoing STN DBS has not been adequately accounted for to date, even though this question is of crucial interest since, as explained earlier, evidence gathered from fMRI and lesion models have led to the hypothesis that the BG play a critical and potentially direct role in the integration of the acoustic features of speech, especially in rhythm perception (Kotz and Schwartze, 2010 and Pell and Leonard, 2003). From the results of an 18fludeoxyglucose-positron emission tomography (18FDG-PET) study comparing resting-state glucose metabolism before and after STN DBS in Parkinson's disease (Le Jeune et al., 2010), we postulated that acoustic features have an impact on the emotional prosody disturbances observed following STN DBS. This study indeed showed that STN DBS modifies metabolic activity across a large and distributed network encompassing areas known to be involved in the different stages of emotional prosody decoding (notably the second and third stages in Schirmer and Kotz's 2006, with clusters found in the STG and STS regions) (Le Jeune et al., 2010). In this context, the aim of the present study was to pinpoint the influence of acoustic features on changes in emotional prosody recognition following STN DBS in Parkinson's disease. To this end, we analysed the vocal emotion recognition performances of 21 Parkinson's patients in a preoperative condition, 21 Parkinson's patients in a post-operative condition, and 21 matched healthy controls (HC), derived from the data published in a previous study (Péron, Grandjean, et al., 2010), by entering the acoustic features of the stimuli into our statistical models as dependent variables of interest. This validated emotional prosody recognition task (Péron et al., 2011, Péron et al., 2014 and Péron et al., 2010b) has proven to be relevant for studying the affective effects of STN DBS in PD patients, notably because of its sensitivity (Péron, 2014). The use of visual (continuous) analogue scales is indeed far more sensitive to emotional effects than are categorization and forced-choice tasks (naming of emotional faces and emotional prosody), chiefly because visual analogue scales do not induce categorization biases (K.R. Scherer & Ekman, 2008).