Emotional motor resonance and its role in anomalous subjective experience in schizophrenia

Abstract

In recent years, worldwide explosion of interest in early, prodromal detection and prevention of schizophrenia, has acknowledged the nonpsychotic anomalous subjective experience as essential in clinical features of schizophrenia. Ongoing contemporary psychopathological research strongly enhance the importance of subtle, nonpsychotic qualitative changes of subjective experiences, among which foremost anomalies of the sense of the self have been considered as core subjective clinical manifestations of schizophrenia. Noteworthy, qualitative and empirical studies consistently indicate that certain anomalous subjective experiences antedate the onset of full-blown psychosis. Moreover, recent years’ growing experimental evidence, documented that anomalous subjective experiences occur in various schizophrenia-related conditions (i.e., full-blown schizophrenia, prodromal conditions, schizotypy, and among genetically high-risk individuals). Particularly, phenomenological psychopathological research exploring self-disorders (SDs) highlights that SDs form an important phenotype for the characterization of Schizophrenia Spectrum (SzSp) disorders, both in clinical and in genetically high-risk populations. Interestingly, a recent study tested the distribution of SDs in a sample of nonpsychotic, genetically high-risk individuals found a gradient-like pattern of SDs, corroborating the concept of SDs as valuable, quantitatively tractable, trait phenotype for indexing genetic liability to SzSp. Nevertheless, until now, nobody has ever found a direct association between phenomenological experience (i.e., the mind level) and neurophysiology (i.e., the body level) in schizophrenia disorder. The need to find such a linkage is gaining growing significance, particularly in light of an existing marked gap between patients’ complaints, that principally entail disturbing experiences, and what are the most preeminent schizophrenia theories and therapies, stemming and proceeding largely at a brain level of description and analysis (e.g., mainly employing pharmacological interventions). The purpose of the first experiment, is to explore whether a possible multisensory disintegration would occur in patients with schizophrenia. To this aim, we tested a novel paradigm to investigate the evaluation of the emotional content of perceived emotions presented through dynamic expressive stimuli, facial mimicry evoked by the same stimuli, and their functional relation. Emotional facial expression, indeed, is an important low-level mechanism contributing to the experience of empathy. Noteworthy, schizophrenia is associated with pervasive social cognitive impairments, including altered emotional processing of facial expressions. Fifteen healthy controls and 15 patients diagnosed with schizophrenia were presented with stimuli portraying positive (laugh), negative (cry) and neutral (control) emotional stimuli in visual, auditory modalities in isolation, and congruently or incongruently associated. Participants where requested to recognize and quantitatively rate the emotional value of the perceived stimuli, while electromyographic activity of Corrugator and Zygomaticus muscles was recorded. Results showed that all participants correctly judged the perceived emotional stimuli and prioritized the visual over the auditory modality in identifying the emotion when they were incongruently associated (Audio-Video Incongruent condition). The neutral emotional stimuli did not evoke any muscle responses and were judged by all participants as emotionally neutral. Control group responded with rapid and congruent mimicry to emotional stimuli, and in Incongruent condition muscle responses were driven by what participants saw rather than by what they heard. Patient group showed a similar pattern only with respect to negative stimuli, whereas showed a lack of or a non-specific Zygomaticus response when positive stimuli were presented. Finally, we found that only patients with reduced facial mimicry (Internalizers) judged both positive and negative emotions as significantly more neutral than controls. This means that in patients with schizophrenia, facial mimicry in response to positive and negative emotions represents a crucial bottom-up process to correctly judge, from a dimensional point of view, the perceived emotion. The aim of the second study was to investigate on the other hand, a possible connection between phenomenological experience (i.e., the mind level) and neurophysiological mechanisms (i.e., the body level), explored through the motor facial mimicry in response to emotional stimuli, previously demonstrated to be a mirror neurons mechanism proxy. For this purpose, eighteen SzSp patients (comprising 14 patients with schizophrenia from previous study plus 4 patients with Schizotypal Personality Disorder) were tested with the same multimodal paradigm, in which positive and negative emotional stimuli were shown in different modalities while Electromyographic activity of facial muscles was recorded. Abnormal subjective experiences were measured by means Bonn scale (BSABS). BSABS items were then grouped following the composition of seven a priori scales described by Parnas and colleagues’ work (2003). Correlations analyses were then performed between Electromyographic facial reactions and BSABS scales. We found an imbalance in emotional motor resonance with a selective bias toward negative stimuli and single-sensory modalities in SzSp patients, which probably led them to a multisensory integration impairment. Most interestingly, we discovered a robust correlation between Self-disorders scale and Electromyographic facial reactions in response to negative stimuli, presented only in auditory modality. Moreover, by dividing SzSp patients in Externalizers and Internalizers for positive and negative emotions, we found that Externalizers patients for negative emotions showed a greater number of psychotic episodes and higher scores on the BSABS Cluster 3 (Vulnerability) with respect to Internalizers. Externalizers for positive emotions, on the other hand, showed higher scores on the BSABS Cluster 5 (“Interpersonal Irritation”) with respect to Internalizers. In conclusion, our multimodal experimental paradigm proved to be sensitive enough to successfully explore emotional motor resonance in response to different perceptual modalities and emotional valence. Our results showed that in SzSp patients a likely imbalance in somatosensory feedback toward negative stimuli and single-sensory modalities could lead to perceptual incoherence and hence to disjointed self-experiences, described as “self-disorders” by phenomenological psychiatrists, regarded as the core deficit in schizophrenia. Indeed, EMG activations in response to auditory negative stimuli strongly correlate with self-disorders, meaning that the aberrant salience of auditory negative stimuli perhaps plays a key role in schizophrenia pathology (e.g., in auditory hallucinations). The paradigm employed in our study, allowing the exploration of bodily motor resonance in response to different perceptual modalities and emotional valence, might be a promising heuristic model to investigate multisensory disintegration and perceptual incoherence as possible early markers of schizophrenia, given their close connection with self-disorders, particularly in clinical asymptomatic, genetically high-risk individuals.