Decoupling of spontaneous facial mimicry from emotion recognition in schizophrenia
Introduction
Abnormalities of emotional experience were recognized as central to schizophrenia by Kraepelin and Bleuler who believed “flat” and “inappropriate” affect to be core features of the illness (see Trémeau, 2006 for a review). Although there is a long history of emotion research in schizophrenia, much of the past work has focused on facial emotion recognition performance and anhedonia (Horan et al., 2005.) Less known is the relationship between the conscious experience of emotion and the unconscious activation of bodily responses that might also be altered in schizophrenia. Interestingly, while some aspects of emotional functioning appear to be altered in individuals with schizophrenia, others might be intact. For instance, although emotion perception and expression have been consistently found to be impaired, emotional experience seems largely unaffected in schizophrenia (for a review see Kring and Elis, 2013). This suggests that while people with schizophrenia report subjective emotional experiences similar to those reported by control individuals, they have difficulty recognizing the emotional facial expressions of others, and exhibit atypical psychophysiological responses to emotional stimuli. Producing and recognizing emotional expressions is crucial to communicating internal feelings and intentions (Ekman et al., 1979). Thus, the social function of emotions (i.e., communicating affective states and understanding the experiences of others) appears to be compromised in schizophrenia.
Appropriate emotional responses within a social interaction are crucial to successful communication and navigation of interpersonal relationships. Research suggests that the facial expression of emotions is reduced in individuals with schizophrenia, even when they report experiencing an emotion (Berenbaum and Oltmanns, 1992, Kring and Moran, 2008). However, studies using facial electromyography (fEMG) found that the recruitment of facial muscles underlying the production of facial expressions is intact in this population (Kring et al., 1999). Together, these results suggest that although observed emotional expressions are affected in schizophrenia, the engagement of facial muscles associated with these expressions is not. In other words, while overt facial expressions are reduced, the underlying moto-kinetic process seems intact.
The ability to recognize the emotional states of others is also critical to social functioning and predicts functional outcome (Hooker and Park, 2002). Emotion detection and identification have been consistently found to be impaired across the schizophrenia spectrum: from individuals at ultra high-risk for psychosis (Amminger et al., 2012a, Cohen et al., 2015, Gooding and Tallent, 2003, Phillips and Seidman, 2008), to first-episode patients (Herbener et al., 2005), and individuals with schizophrenia (Edwards et al., 2002, Kohler et al., 2003, Berenbaum and Oltmanns, 1992). Importantly, emotion recognition deficits in schizophrenia are independent of medication effects and demographic factors such as race and gender (Kohler et al., 2010). Additionally, emotion recognition deficits appear to be independent of the stage of schizophrenia illness, already contributing to social functioning impairments in emerging psychotic illness (Amminger et al., 2012b).
Research suggests that the ability to identify emotions in others might rely on automatic motor processes such as spontaneous bodily coordination (Lakin and Chartrand, 2003, Moody et al., 2018, Prochazkova and Kret, 2017). For instance, facial mimicry, the automatic process by which individuals match other's facial expressions during social interactions (Dimberg, 1990) has been shown to contribute to emotion recognition (Goldman and Sripada, 2005, Niedenthal et al., 2010). When facial mimicry is blocked with a muscle paralytic, the ability to identify facial expression of emotions is impaired in healthy individuals (Oberman et al., 2007, Neal and Chartrand, 2011). Furthermore, a specific pattern of muscle activation can induce an emotion (Prigent et al., 2014), suggesting that the automatic mimicry of other's facial expressions allows us to share their emotional experience. The facial feedback hypothesis further posits that facial synchrony promotes empathy (Adelman and Zajonc, 1999), highlighting the importance of mimicry for social connectedness. In sum, the automatic mimicry of others’ facial expressions mediates emotional contagion, social functioning, and embodied affect. Therefore, deficits in facial mimicry could contribute to emotion identification deficits.
Although it is well established that individuals with schizophrenia exhibit decreased spontaneous facial expressions, studies investigating facial mimicry in this population remain sparse and have yielded mixed results (Kring, 1999). Indeed, facial mimicry has previously been found to be both intact (Chechko et al., 2016) and impaired (Varcin et al., 2010) in individuals with schizophrenia. Thus, it remains unclear whether spontaneous mimicry is altered in schizophrenia. Interestingly, intentional facial expression imitation has been found impaired in schizophrenia (Schwartz et al., 2006), and broader deficits in action imitation have been linked to altered brain activation in this population (Thakkar et al., 2014). Similar disruptions of automatic facial mimicry could explain deficits in emotion recognition and broader social deficits in individuals with schizophrenia.
Deficits in emotion recognition are well established in the literature, however, the ability of people with schizophrenia to automatically mimic the facial expressions of others remains unclear. Furthermore, to our knowledge, automatic facial mimicry and emotion identification have never been tested simultaneously in schizophrenia. In the current study, we assessed performance on a novel dynamic emotion recognition task while monitoring facial mimicry using fEMG. Given past findings, we expected the performance of individuals with schizophrenia to be less accurate than that of matched controls during the emotion recognition task. With respect to facial mimicry measured by fEMG, we expected individuals with schizophrenia to show reduced activity of the zygomatic and corrugator muscles. Although the findings of facial mimicry in schizophrenia are mixed, we decided to test the hypothesis that deficits in facial synchrony underlie impaired emotion recognition in schizophrenia.
Section snippets
Participants
Twenty-one individuals who met the DSM-V criteria for schizophrenia (SZ) were recruited from an outpatient day facility in Nashville, TN. Diagnosis was confirmed with the Structured Clinical Interview for DSM-V (SCID-5RV; First et al., 2015). Symptoms were assessed with the Brief Psychiatric Rating Scale (BPRS; Overall and Gorham, 1962), the Scale for the Assessment of Positive Symptoms (SAPS; Andreasen, 1984), and the Scale for the Assessment of Negative Symptoms (SANS; Andreasen, 1989). All
ERRATA performance
As expected, SZ were less accurate than CO at recognizing avatar's facial expression on ERRATA across emotions (SZ: 51.3% correct, CO: 58.9% correct; OR = 0.69, p < 0.001). Thus, the odds of SZ correctly identifying an emotion were 31% lower than those of CO. When examined per emotion, recognition rates were significantly lower in SZ compared to CO for fear (OR = 0.43, p < 0.001) and surprise (OR = 0.45, p = 0.011), but not for anger, contempt, joy or sadness (all p 〉 0.05). After correcting
Discussion
SZ's impaired performance on ERRATA is in line with a large body of literature documenting emotion identification deficits in this population (for a review see Kohler et al., 2010). Importantly, our results also replicate those of previous studies using dynamic emotional facial stimuli (Archer et al., 1994, Johnston et al., 2010). We found that SZ's performance was affected at all levels of emotional intensity. Although performance was not affected for all emotions, no discernable pattern of
Acknowledgments
This work was supported by NARSAD, MH106748 and the Gertrude Conaway Vanderbilt Endowment fund. We acknowledge and thank Alena Gizdić, Jacqueline Roig, Andrea Prada, Justin Hong, and Eunsol Chon for their help with data collection. We also thank our participants for their time and dedication.
Declaration of conflict of interest
The authors report no conflict of interest.
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