Next Article in Journal
Successful Hemispherotomy in a Patient with Encephalopathy with Continuous Spikes and Waves during Sleep Related to Neonatal Thalamic Hemorrhage: A Case Report with Intracranial Electroencephalogram Findings
Next Article in Special Issue
Differential Influence of the Dorsal Premotor and Primary Somatosensory Cortex on Corticospinal Excitability during Kinesthetic and Visual Motor Imagery: A Low-Frequency Repetitive Transcranial Magnetic Stimulation Study
Previous Article in Journal
Impact of Cognitive Reserve and Premorbid IQ on Cognitive and Functional Status in Older Outpatients
Previous Article in Special Issue
Procedural Learning through Action Observation: Preliminary Evidence from Virtual Gardening Activity in Intellectual Disability
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Efficacy of Facial Exercises in Facial Expression Categorization in Schizophrenia

1
Department of Neuroscience and Rehabilitation, University of Ferrara, via Fossato di Mortara 19, 44121 Ferrara, Italy
2
Department of Neuroscience, Biomedicine and Movement Sciences, University of Verona, 37134 Verona, Italy
3
Integrated Department of Mental Health and Addictive Behavior, Local Health Trust of Ferrara, 44124 Ferrara, Italy
*
Author to whom correspondence should be addressed.
Brain Sci. 2021, 11(7), 825; https://doi.org/10.3390/brainsci11070825
Submission received: 1 June 2021 / Revised: 15 June 2021 / Accepted: 21 June 2021 / Published: 22 June 2021
(This article belongs to the Special Issue The Role of the Sensorimotor System in Cognitive Functions)

Abstract

:
Embodied cognition theories suggest that observation of facial expression induces the same pattern of muscle activation, and that this contributes to emotion recognition. Consequently, the inability to form facial expressions would affect emotional understanding. Patients with schizophrenia show a reduced ability to express and perceive facial emotions. We assumed that a physical training specifically developed to mobilize facial muscles could improve the ability to perform facial movements, and, consequently, spontaneous mimicry and facial expression recognition. Twenty-four inpatient participants with schizophrenia were randomly assigned to the experimental and control group. At the beginning and at the end of the study, both groups were submitted to a facial expression categorization test and their data compared. The experimental group underwent a training period during which the lip muscles, and the muscles around the eyes were mobilized through the execution of transitive actions. Participants were trained three times a week for five weeks. Results showed a positive impact of the physical training in the recognition of others’ facial emotions, specifically for the responses of “fear”, the emotion for which the recognition deficit in the test is most severe. This evidence suggests that a specific deficit of the sensorimotor system may result in a specific cognitive deficit.

Graphical Abstract

1. Introduction

Schizophrenia is characterized by heterogeneous positive and negative symptom constellations [1]. Negative symptoms refer to a diminution or absence of normal behaviors, they account for a large part of the long-term morbidity and poor functional outcome in patients with the disorder [2,3,4], and have been reported as among the most common first symptom of schizophrenia [5]. Although positive symptoms are generally effectively managed with available antipsychotic medications, limited treatment options are available for negative symptoms [6]. Negative symptoms can be categorized into two independent factors: diminished expression, and apathy [2]. Diminished expression mainly includes reduction in the expression of facial emotions. Interestingly, considerable research evidence indicates that facial mimicry contributes to accurate and efficient recognition of facial expressions [7,8] which is essential for social cognition [9]. Indeed, individuals with schizophrenia experience problems in face emotion recognition throughout the course of the disorder [10,11]. Rather than a general deficit that encompasses all emotions, schizophrenia may be associated with a more specific deficit in the processing of a subset of negative emotions, including sadness and fear [12,13,14,15,16]. Furthermore, these specific deficits have been demonstrated in individuals with first-episode psychosis [17], and in individuals who are “at risk” for psychosis [18], suggesting that they may serve as markers of risk [19].
The possibility that reduced expression of facial emotions contributes to the difficulty in recognizing facial expressions in patients with schizophrenia has recently been considered in a facial expression categorization test experiment. Results showed that patients’ identification rates were lower than healthy controls, specifically for the responses fear and sadness [20]. Interestingly, in healthy participants, the identification rates at the same test were significantly modulated by constraint facial postures [21]. Participants were required to label pictures randomly taken from four morphed continua between two emotional facial expressions, while they were submitted either to a lower or to an upper face posture manipulation. The stretching of the mouth (i.e., participants were required to maintain a stick horizontally between the teeth without touching it with the lips) increased the percentage of happy average responses, and the upper face posture manipulation (i.e., participants were asked to frown and then a Band-Aid was applied in proximity to corrugator muscle, covering the eyebrows and partially lowering the eyelids) increased the percentage of sad average responses. These effects were found only for intermediate values of the continuum, where the expressions were more ambiguous. The authors assumed that facial postural manipulation induced a specific sensorimotor activation which enhanced the detection of visual cues congruent with that sensorimotor state. Specifically, they concluded that the implementation of low-level movement details influenced the discrimination of ambiguous facial expressions differing for a specific involvement of those movement details [21]. This interpretation of the results is congruent with embodied cognition theories, which suggest that we understand others’ emotions by reproducing the perceived expression in our own facial musculature (facial mimicry), and the mere observation of a facial expression can evoke the corresponding emotion in the perceivers. Consequently, the inability to form facial expressions would affect the experience of emotional understanding [22,23,24,25,26].
Therefore, it is possible that, in patients with schizophrenia, an increase in the ability to perceive and perform facial movements leads to an improvement in the recognition of facial expressions. Indeed, facial expressions are principally the result of stereotyped movements of facial skin and fascia due to contraction of the facial muscles in certain combinations. Such contractions create folds, lines, and wrinkles in the skin and cause movement of facial landmarks such as mouth corners and eyebrows which represent the most salient aspects of most expressions [27,28]. Consequently, as happens for all skeletal muscles, specific facial muscle mobilization training could lead to an improvement in the ability to modulate the recruitment of motor units. Furthermore, literature reports that physical therapy approaches play an important role in the multidisciplinary treatment of people with schizophrenia [29,30,31,32,33].
Facial muscle rehabilitation is successfully applied in individuals with facial paralysis and distorted facial expressions and movements, secondary to a facial neuromotor disorder [34,35,36,37]. It is worth noting that the neuromotor control of facial movements appears different from the usual motor control mechanisms of skeletal muscles due to the limited ability of the facial muscles to provide feedback. Intrinsic muscle receptors and joint receptors, primary sources for peripheral proprioceptive feedback to the central nervous system, are few or absent in the face [38,39]. To overcome the physiological absence of proprioception which presumably renders the brain uninformed of facial muscle performance, the facial neuromuscular reeducation approach of neurological patients consists of movement exercises accompanied by surface EMG biofeedback or mirror feedback [37]. Individuals who are provided with precise, extrinsic feedback about facial muscle activity learn to recruit the appropriate motor units for the desired movement, as it happens in relearning movement patterns involving the peripheral neuromuscular system.
On this basis, the present work proposed a functional physical training of the facial muscles to patients with schizophrenia. To ensure that training was well received by patients and that it can be easily used as rehabilitation therapy in public health facilities, the use of extrinsic feedback has not been envisaged. To inform patients about the correctness of the execution of the proposed movements, each exercise was designed as a transitive action, which acts towards an object to achieve a certain goal (e.g., to move a light ball by blowing through a straw). As a result, the achievement of the goal performed the feedback function such as the EMG signal or the image in the mirror. The training protocol was based on the parameters individuated by the Facial Action Coding System (FACS) [28,40] which systematically assessed the muscular components of facial behavior. FACS identified the appearance changes related to facial movements and aimed to identify individual muscle contractions, focusing not on the expression of emotions, but on the production of spontaneous facial movements. FACS uses numbers to refer to the appearance changes associated with 33 facial muscle contractions, or action units (AUs). Most AUs refer to the contraction of single muscles, but some muscles always co-occur, or are capable of producing different movements. Thus, the correspondence between facial muscles and movements is not always direct. Therefore, the present training protocol was specifically designed to mobilize the face according to the AU profiles of happiness, fear, anger, and sadness. For example, the happiness profile is characterized by AU 6 + 12. The action descriptor of AU 6 is “cheek raiser”, while that of AU 12 is “lip corner puller”. Consequently, examples of the exercises proposed to enhance the ability to express happiness were “move the glasses placed on the nose upwards using the cheek muscles”, and “maintain a stick horizontally between the teeth without touching it with the lips”.
The main aim of the present study was to test the effects of facial muscle mobilization training in patients with schizophrenia on performance in a facial expression categorization test [21]. To this end, the patients were tested before and after the training period, and their results were compared with those of a control group of patients with schizophrenia housed in the same psychiatric residence who did not participate in the training. The time interval between the two test phases was the same in the two groups. We expected an improvement in the recognition of sadness and fear, expressions for which patients with schizophrenia show difficulty in recognition [20].

2. Materials and Methods

2.1. Participants

Twenty-four inpatient participants with schizophrenia-spectrum disorders (SSD) classified according to the International Statistical Classification of Diseases and Related Health Problems 10th Revision (ICD-10) participated in this study, gave their written informed consent, and were randomly assigned to the experimental (n = 12; 8 females; mean age = 53.3 years, standard deviation = 8.81) and control (n = 12; 3 females; mean age = 47.9 years, standard deviation = 9.7) group. For each participant, Table 1 reports ICD-10 codes and description of main symptoms.
All participants were native Italian speakers of Caucasian ethnicity (as were the models depicted in the stimuli) and reported having normal or corrected-to-normal visual acuity. The patients were hosted at the long-term psychiatric residence “Il Convento” and psychiatric day center “Il Convento” in Ferrara (Italy). Participants were unaware of the purposes of the study. The procedures were approved by the local ethics committee (ref.: EM255-2020_UniFe/170592_EM) and were in accordance with the guidelines of the Declaration of Helsinki. Both groups of participants underwent the facial expression categorization test [20,21] twice. During the month between the first (Test 1) and second (Test 2) test administration, the participants in the experimental group were involved in physical training, while the participants in the control group carried out the activities proposed by the nursing home.

2.2. Facial Physical Training

The participants of the experimental group were involved in the training protocol in groups of four, for three 45-minute sessions per week, for five subsequent weeks (total 15 sessions). The timing of the protocol is based on those of the closest protocol in the literature, namely the Action Observation Treatment (AOT; [41]). AOT is a rehabilitation approach that aims to reactivate the sensorimotor skills to perform transitive actions in neurological patients. Specifically, we adapted it as follows: We slightly lengthened the duration of each session (45 min instead of 30), reduced the number of weekly sessions (3 days a week instead of 5) and lengthened the number of weeks (5 instead of 4). The choice of making groups of 4 people was based on having a group that was either too big nor too small. The training was performed in a dedicated room in which there were chairs, tables and the disposable material necessary to perform the exercises. To help the experimenter, a staff member of the healthcare facility was also present. Each exercise was explained and shown by the experimenter to the whole group. Subsequently, each participant performed the exercise for about 5 min, alone or with the help of the operator. During each session an average of 5 exercises was proposed. Exercises varied each time, and each of them was proposed several times during the different sessions.
As anticipated in the Introduction section, the facial physical training protocol was designed to mobilize the face according to the AUs profiles of happiness, fear, anger, and sadness (Table 2) and the relative action descriptors (Table 3), reported by [40].
The considered action descriptors essentially concern the movements of the lips and the muscles around the eyes, and the facial exercises proposed mainly involved these two facial districts. As already stated, we did not want to use any kind of external feedback as is commonly the case with neurological patients [37]. Patients with schizophrenia do not willingly accept the application of electrodes, nor observe their image in the mirror. We therefore decided to invent a series of exercises that required the execution of transitive actions. In other words, actions aimed at some objects, the result of which (the maintenance or mobilization of the objects) performed the feedback function of the correct execution of the exercise. We have not been able to exploit the literature to use transitive actions for the facial muscles, as so far only transitive actions involving the upper or lower limbs have been described [41]. The list of exercises is reported in Table 4.

2.3. Facial Expression Categorization Test

2.3.1. Procedure

The participants in the Experimental group were tested the week before and after the training period, which lasted five weeks. The participants in the control group were also tested twice and the time interval between the two test phases was the same as that of the experimental group.
Stimuli consisted of 88 pictures of two human face models (one female, one male), selected in a previous study [42], and used here with permission (Figure 1). They were the result of a morphed transformation of four original pictures of each model portraying different emotion expressions (anger, fear, happiness and sadness) [28]. This transformation gave rise to four continua, anger-fear, anger-sadness, fear-happiness and happiness-sadness, each composed of 11 images. The three figures in the center of the continuum were presented four times each, while the others were presented twice, as in previous studies [20,21]. The total number of stimuli presented was 224 (28 for each model in each continuum × 2 models × 4 continua), subdivided into four blocks of 56 trials each. For more technical details, see [20,21].
Participants sat in front of a 19-inch LCD monitor (resolution: 1.280 × 800 pixels; refresh frequency: 60 Hz) on which stimuli appeared on a grey background subtending an 11° × 17° square region around the fovea. Stimulus-presentation timing and randomization were controlled with E-prime V2.0 (Psychology Software Tools Inc., Pittsburgh, PA, USA).
Each trial began with the presentation of a central fixation cross lasting 250 ms, followed by the presentation in the center of the screen of a randomly selected stimulus, lasting 500 ms. After the stimulus disappeared, four text boxes, “anger” (rabbia in Italian), “fear” (paura), “happiness” (felicità), and “sadness” (tristezza), appeared on the screen in line. The order of the four text boxes was balanced between the participants. Participants were asked to say the name of the emotion the face most resembled, and the experimenter recorded the response on the data recording computer.

2.3.2. Data Analysis

For each continuum, we grouped responses according to levels, as indicated in Figure 1. For each emotion, we calculated the sum of relative responses given in trials belonging to the less ambiguous level of the two continua in which the emotion was present. Specifically, for anger, we calculated the sum of responses given at level 1 of the anger-fear continuum and at level 1 of the anger-sadness continuum; for fear, the sum of responses given at level 3 of the anger-fear continuum and at level 1 of the fear-happiness continuum; for sadness, the sum of responses given at level 3 of the anger-sadness continuum and at level 3 of the happiness-sadness continuum; for happiness, the sum of responses given at level 1 of the happiness-sadness continuum and at the level 3 of the fear-happiness continuum. Therefore, for each emotion, we calculated the number of responses given in 48 trials. We decided to consider these trials since our group previously found [20] that patients with schizophrenia differed from controls in the number of responses given at the less ambiguous levels of this same test.
The number of responses for each emotion was entered into a three-way 2 × 2 × 4 repeated-measure analysis of variance (ANOVA) with group (experimental, control) as between-subject variable, and test order (1, 2) and emotion (happiness, fear, anger, sadness) as within-subject variables. All pairwise comparisons were performed using the Bonferroni post-hoc test. A significance threshold of p < 0.05 was set for all statistical analyses. Effect sizes were estimated using the partial eta square measure (ηp2). The data are reported as the mean ± standard error of the mean (sem).

3. Results

The three-way ANOVA performed on the number of responses revealed that the group main effect (F1,22 = 4.129, p = 0.054, ηp2 = 0.158), the test order main effect (F1,22 = 1.676, p = 0.209, ηp2 = 0.070) and the two-way interaction test order × emotion (F3,66= 2.572, p = 0.061, ηp2 = 0.105) were not significant. The emotion main effect was significant (F3,66 = 19.779, p < 0.001, ηp2 = 0.473). The post-hoc analysis indicated that the number of happiness (42.3 ± 1.11) and sadness (38.5 ± 1.13) responses were greater than the number of fear (32.5 ± 1.29; all ps < 0.001) and angry (32.8 ± 1.89; respectively p < 0.001 and p = 0.002) responses. Happiness and sadness did not differ from each other (p = 0.08), and nor did fear and angry (p = 1).
The two-way interaction test order × group (F1,22 = 22.765, p < 0.001, ηp2 = 0.508), the two-way interaction emotion × group (F3,66 = 5.515, p = 0.002, ηp2 = 0.200), and the three-way interaction test order × emotion × group (F3,66 = 3.567, p = 0.018, ηp2 = 0.139) were significant.
Post-hoc analysis of the two-way interaction test order × group showed that in Test 1, the number of responses of the experimental (36.7 ± 1.31) and control (35.7 ± 1.49) groups did not differ (p = 1.000), and in Test 2 they were significantly greater for the experimental group (experimental, 40.1 ± 0.84; control, 33.7 ± 1.58, p = 0.014). The number of responses increased significantly in Test 2 for the experimental group only (experimental, p = 0.002; control, p = 0.134).
The post-hoc analysis of the three-way interaction test order × emotion × group showed a significant increase in the number of responses fear of the experimental group between Test 1 (30.9 ± 2.45) and Test 2 (38.3 ± 1.27, p < 0.001). Within each emotion, no other differences between the responses of the same group to the two tests (all ps > 0.08), or between the groups within the same test (all ps > 0.213), were significant (Figure 2).

4. Discussion

The aim of the present study was to test the effects of facial muscle mobilization training in patients with schizophrenia on performance in a facial expression categorization test [21]. The hypothesis was that, in patients with schizophrenia, the reduction in the expression of facial emotions is among the possible causes of problems in the recognition of others’ facial emotions. To this end, the patients were tested before (Test 1) and after (Test 2) a training period during which the lip muscles and the muscles around the eyes were mobilized through the execution of transitive actions. The data obtained in the two sessions of the facial expression categorization test were compared with those of a control group of patients with schizophrenia who did not participate in the training. Results showed a positive impact of the physical training in the recognition of others’ facial emotions. Specifically, the number of responses increased significantly in Test 2 with respect to Test 1 for the experimental group only. Furthermore, in Test 1, the number of responses of the two groups did not differ, and in Test 2 they were significantly greater for the experimental group. Previous data showed that the identification rate at the same facial expression categorization task was statistically significantly lower in patients with schizophrenia than in matched healthy participants [20]. The difference in performance was constantly present during trials requiring to produce the response fear, and less dramatically during trials requiring the response sadness. These findings are in agreement with evidence in literature that indicates that schizophrenia may be associated with a specific deficit in the processing of a subset of negative emotions including sadness and fear [12,13,14,15,16]. Therefore, we expected an increase in the ability to recognize the emotions for which the deficit is present. The results showed a specific increase in the number of responses of “fear”, the emotion for which the recognition deficit on this test is most severe.
The hypothesis underlying the present study arises from the claims of the embodied theories of cognition [43,44,45,46], according to which, stimulus recognition is supported by the automatic re-instantiation of modality-specific states captured during perception, action, and interoception of past experience with the stimulus [22]. In particular, the ability to recognize and understand the facial expressions of others depends on the automatic evocation of the same facial expression in the observer (i.e., spontaneous mimicry; [47,48,49,50,51]). Indeed, evidence shows that preventing participants from engaging expression-relevant facial muscles can impair their ability to detect briefly presented or otherwise ambiguous facial expressions that involve that specific muscle [52,53,54,55,56,57]. Interestingly, a consistent finding in the literature on emotion in schizophrenia is that individuals with schizophrenia are less facially expressive than individuals without schizophrenia in response to a variety of contexts and evocative stimuli [58]. They display fewer facial expressions in response to emotionally evocative film clips [59,60,61,62,63,64,65,66], foods [59], and social interactions [60,66,67,68,69,70,71,72,73]. Importantly, diminished expression is observed among individuals with schizophrenia both on [59,74] and off medication [63,64,65]. Therefore, we assumed that, as happens for all skeletal muscles, a physical training specifically developed to mobilize facial muscles could improve the ability to perform facial movements, and, consequently, even spontaneous mimicry and the related facial expression recognition. The positive influence of the physical training in the facial expression categorization test used in the present study supports this possibility. Indeed, this test was demonstrated to be a sensitive method to prove the role of the sensorimotor system in the perception of others’ actions, given that in healthy participants a facial postural manipulation influenced the identification rates [21].
Facial expressions are extremely relevant to social cognition. Information on the others’ affective states (e.g., others’ emotions) and on the environment (e.g., dangers from fearful reactions) could be extracted from facial expressions [9]. Several are the interventions that attempt to ameliorate deficits in social cognition in clients with schizophrenia. Targeted interventions train clients on aspects of one specific domain of social cognition [75,76,77]. The “training of affect recognition” (TAR) [78,79] primarily targets impairments in facial affect recognition, and it may be considered the most representative one. It is based on errorless learning, over-learning, and immediate positive feedback and feature abstraction. Since intensive coaching and modeling by the therapist is necessary, working with groups of more than two patients does not appear to be feasible. Therefore, despite the evidence of the positive effects of the TAR [78,79,80], the cost of personnel for this intervention is high. The present study proposes a less expensive alternative readily accepted and performed by patients.
This exercise protocol could be included among the different exercise therapies that have been proposed as an adjunct treatment in the multidisciplinary care of people with schizophrenia. Numerous randomized controlled trials [81] and meta-analyses [82] have shown a positive effect of exercise in treating schizophrenia. Specifically, there is evidence that aerobic, strength exercises, and yoga reduce psychiatric symptoms, state anxiety, and psychological distress and improve health-related quality of life. Furthermore, aerobic exercise improves short term memory, and progressive muscle relaxation reduces state anxiety and psychological distress [32]. These data, therefore, affirm the importance of the role of fitness trainers in meeting the mental and physical health needs of people with mental illness [33]. However, mental health facilities often do not have gyms or large spaces available for aerobic or fitness physical activity, and, furthermore, in many countries, the fitness trainer is not part of the multidisciplinary team working in mental health settings. The present training protocol, however, is based on performing transitive actions in a non-aerobic context where users are sitting or standing. Transitive actions are meaningful gestures implying the use of an object. Some examples of the proposed exercises are to inflate balloons, to push a small ball towards a target by blowing through a straw, to hold round objects of various sizes by tightly contracting the muscles around the eyes. To train in this type of action, a specific education in fitness is not necessary. Instead, education as psychiatric rehabilitation therapist is required, which develops the skills and knowledge necessary to work with patients with psychiatric disabilities, covering topics that include skills training, cognitive rehabilitation, and motivational strategies. This figure is normally part of the group that operates in mental health contexts, with the role of putting into practice the rehabilitation and educational interventions proposed by the therapeutic project. Therefore, the rehabilitation intervention proposed here can be easily applied by mental health services without the need for new professional figures or spaces with specific characteristics.
There are several limitations of this study that require further investigation to verify the outcome of this treatment. The heterogeneity of the pathological characteristics of the small sample studied may have influenced the results. Further studies are also needed to verify the duration of the effects of this training over time, and possibly propose changes to the timing and proposed exercises. Finally, it is necessary to investigate whether this protocol positively influences not only the ability to recognize but also to express emotions, and whether its effects lead to an overall improvement in social cognition.
By concluding, the results of this study bring for the first time evidence in favor of the efficacy of a rehabilitation approach dedicated to the training of sensorimotor skills in improving cognitive functions of those suffering from a severe mental disorder. They also suggest a broader application of mental health interventions, i.e., they must not be limited to social and psychological approaches, but must also include approaches based on the body and its interaction with the environment. The demonstration that an intervention to increase the ability to perform facial actions influences the perception of facial expressions indicates that a specific deficit of the sensorimotor system may result in a specific cognitive deficit, supporting the hypothesis that the sensorimotor system plays a central role in cognitive functions.

Author Contributions

Conceptualization, L.C.; data curation, F.P., S.M. and L.C.; formal analysis, S.M. and L.C.; investigation, F.P., V.C., R.B. and F.S.; methodology, F.P. and L.C.; project administration, L.C.; resources, L.C.; software, S.M. and L.C.; supervision, L.C.; validation, S.M. and L.C.; writing—original draft, L.C.; writing—review and editing, L.C. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

The study was conducted according to the guidelines of the Declaration of Helsinki, and approved by the Ethics Committee of AREA VASTA EMILIA CENTRO (protocol code EM255-2020_UniFe/170592_EM; date of approval February 2020).

Informed Consent Statement

Informed consent was obtained from all subjects involved in the study.

Data Availability Statement

The data presented in this study are openly available in FigShare at https://doi.org/10.6084/m9.figshare.14710638.v1. Dataset posted on 1 June 2021.

Acknowledgments

The authors gratefully acknowledge Professor Seth Pollak for providing the set of stimuli, and thank all the patients who agreed to participate in the study, and the members of the health facilities who collaborated with the researchers during the training sessions (Elisa Massimo, Samuele Lovera, Gianna Procino, Maria Luigia Cicchitti, Cinzia Perelli, Federica Marchesini, Floriana Recine, Cristina Maria Spadoni, Marsela Gerveshi, Antonella Nava, Marina Zappaterra, Barbara Bottoni, Rita Piccinini, Diana Maria Battista, Irene Pontarelli).

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Kahn, R.S.; Sommer, I.E.; Murray, R.M.; Meyer-Lindenberg, A.; Weinberger, D.R.; Cannon, T.D.; O’Donovan, M.; Correll, C.U.; Kane, J.M.; van Os, J.; et al. Schizophrenia. Nat. Rev. Dis. Prim. 2015, 1, 15067. [Google Scholar] [CrossRef]
  2. Galderisi, S.; Mucci, A.; Buchanan, R.W.; Arango, C. Negative symptoms of schizophrenia: New developments and unanswered research questions. Lancet Psychiatr. 2018, 5, 664–677. [Google Scholar] [CrossRef]
  3. Kirkpatrick, B.; Buchanan, R.W.; Ross, D.E.; Carpenter, J. A separate disease within the syndrome of schizophrenia. Arch. Gen. Psychiatr. 2001, 58, 165–171. [Google Scholar] [CrossRef] [PubMed]
  4. Milev, P.; Ho, B.C.; Arndt, S.; Andreasen, N.C. Predictive values of neurocognition and negative symptoms on functional outcome in schizophrenia: A longitudinal first-episode study with 7-year follow-up. Am. J. Psychiatr. 2005, 162, 495–506. [Google Scholar] [CrossRef]
  5. An Der Heiden, W.; Häfner, H. The epidemiology of onset and course of schizophrenia. Eur. Arch. Psychiatr. Clin. Neurosci. 2000, 250, 292–303. [Google Scholar] [CrossRef]
  6. Carbon, M.; Correll, C.U. Thinking and acting beyond the positive: The role of the cognitive and negative symptoms in schizophrenia. CNS Spectr. 2014, 19, 38–52. [Google Scholar] [CrossRef]
  7. Künecke, J.; Hildebrandt, A.; Recio, G.; Sommer, W.; Wilhelm, O. Facial EMG responses to emotional expressions are related to emotion perception ability. PLoS ONE 2014, 9, e84053. [Google Scholar] [CrossRef]
  8. Ipser, A.; Cook, R. Inducing a concurrent motor load reduces categorization precision for facial expressions. J. Exp. Psychol. Hum. Percept. Perform. 2016, 42, 706–718. [Google Scholar] [CrossRef]
  9. Adolphs, R. Recognizing emotion from facial expressions: Psychological and neurological mechanisms. Behav. Cogn. Neurosci. Rev. 2002, 1, 21–62. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  10. Edwards, J.; Jackson, H.J.; Pattison, P.E. Emotion recognition via facial expression and affective prosody in schizophrenia: A methodological review. Clin. Psychol. Rev. 2002, 22, 789–832. [Google Scholar] [CrossRef]
  11. Kohler, C.G.; Walker, J.B.; Martin, E.A.; Healey, K.M.; Moberg, P.J. Facial emotion perception in schizophrenia: A meta-analytic review. Schizophr. Bull. 2010, 36, 1009–1019. [Google Scholar] [CrossRef]
  12. Kucharska-Pietura, K.; David, A.S.; Masiak, M.; Phillips, M.L. Perception of facial and vocal affect by people with schizophrenia in early and late stages of illness. Br. J. Psychiatr. 2005, 187, 523–528. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  13. Archer, J.; Hay, D.C.; Young, A.W. Movement, face processing and schizophrenia: Evidence of a differential deficit in expression analysis. Br. J. Clin. Psychol. 1994, 33, 517–528. [Google Scholar] [CrossRef]
  14. Bellack, A.S.; Blanchard, J.J.; Mueser, K.T. Cue Availability and Affect Perception in Schizophrenia. Schizophr. Bull. 1996, 22, 535–544. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  15. Gaebel, W.; Wölwer, W. Facial expression and emotional face recognition in schizophrenia and depression. Eur. Arch. Psychiatr. Clin. Neurosci. 1992, 242, 46–52. [Google Scholar] [CrossRef]
  16. Schneider, F.; Gur, R.C.; Gur, R.E.; Shtasel, D.L. Emotional processing in schizophrenia: Neurobehavioral probes in relation to psychopathology. Schizophr. Res. 1995, 17, 67–75. [Google Scholar] [CrossRef]
  17. Edwards, J.; Pattison, P.E.; Jackson, H.J.; Wales, R.J. Facial affect and affective prosody recognition in first-episode schizophrenia. Schizophr. Res. 2001, 48, 235–253. [Google Scholar] [CrossRef]
  18. Amminger, G.P.; Schäfer, M.R.; Papageorgiou, K.; Klier, C.M.; Schlögelhofer, M.; Mossaheb, N.; Werneck-Rohrer, S.; Nelson, B.; McGorry, P.D. Emotion recognition in individuals at clinical high-risk for schizophrenia. Schizophr. Bull. 2012, 38, 1030–1039. [Google Scholar] [CrossRef]
  19. Comparelli, A.; Corigliano, V.; De Carolis, A.; Mancinelli, I.; Trovini, G.; Ottavi, G.; Dehning, J.; Tatarelli, R.; Brugnoli, R.; Girardi, P. Emotion recognition impairment is present early and is stable throughout the course of schizophrenia. Schizophr. Res. 2013, 143, 65–69. [Google Scholar] [CrossRef]
  20. Mele, S.; Bivi, R.; Borra, L.; Callegari, V.; Caracciolo, S.; Tugnoli, S.; Craighero, L. Efficacy of theatre activities in facial expression categorization in schizophrenia. Arts Psychother. 2019, 63, 141–150. [Google Scholar] [CrossRef]
  21. Mele, S.; Ghirardi, V.; Craighero, L. Facial expressions as a model to test the role of the sensorimotor system in the visual perception of the actions. Exp. Brain Res. 2017, 235, 3771–3783. [Google Scholar] [CrossRef]
  22. Niedenthal, P.M. Embodying emotion. Science 2007, 316, 1002–1005. [Google Scholar] [CrossRef] [Green Version]
  23. Niedenthal, P.M.; Mermillod, M.; Maringer, M.; Hess, U. The Simulation of Smiles (SIMS) model: Embodied simulation and the meaning of facial expression. Behav. Brain Sci. 2010, 33, 417–433. [Google Scholar] [CrossRef] [PubMed]
  24. Price, T.F.; Harmon-Jones, E. Embodied emotion: The influence of manipulated facial and bodily states on emotive responses. WIREs Cogn. Sci. 2015, 6, 461–473. [Google Scholar] [CrossRef]
  25. Prenger, M.T.M.; Macdonald, P.A. Problems with Facial Mimicry Might Contribute to Emotion Recognition Impairment in Parkinson’s Disease. Parkinsons Dis. 2018, 2018, 5741941. [Google Scholar] [CrossRef] [Green Version]
  26. De Stefani, E.; Nicolini, Y.; Belluardo, M.; Ferrari, P.F. Congenital facial palsy and emotion processing: The case of Moebius syndrome. Genes Brain Behav. 2019, 18, e12548. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  27. Ekman, P.; Friesen, W.V. Pictures of Facial Affect; Consulting Psychologists Press: Palo Alto, CA, USA, 1976. [Google Scholar]
  28. Ekman, P.; Friesen, W.V.; Hager, J.C. The Facial Action Coding System; Consulting Psychologists Press: Palo Alto, CA, USA, 1975; Volume 50, ISBN 0931835011. [Google Scholar]
  29. Rosenbaum, S.; Tiedemann, A.; Sherrington, C.; Curtis, J.; Ward, P.B. Physical activity interventions for people with mental illness: A systematic review and meta-analysis. J. Clin. Psychiatr. 2014, 75, 964–974. [Google Scholar] [CrossRef]
  30. Vancampfort, D.; Correll, C.U.; Scheewe, T.W.; Probst, M.; De Herdt, A.; Knapen, J.; De Hert, M. Progressive muscle relaxation in persons with schizophrenia: A systematic review of randomized controlled trials. Clin. Rehabil. 2013, 27, 291–298. [Google Scholar] [CrossRef] [PubMed]
  31. Stubbs, B.; Mitchell, A.J.; De Hert, M.; Correll, C.U.; Soundy, A.; Stroobants, M.; Vancampfort, D. The prevalence and moderators of clinical pain in people with schizophrenia: A systematic review and large scale meta-analysis. Schizophr. Res. 2014, 160, 1–8. [Google Scholar] [CrossRef]
  32. Vancampfort, D.; Probst, M.; Skjaerven, L.H.; Catalán-Matamoros, D.; Lundvik-Gyllensten, A.; Gómez-Conesa, A.; Ijntema, R.; de Hert, M. Systematic review of the benefits of physical therapy within a multidisciplinary care approach for people with schizophrenia. Phys. Ther. 2012, 92, 11–23. [Google Scholar] [CrossRef] [Green Version]
  33. Vera-Garcia, E.; Mayoral-Cleries, F.; Vancampfort, D.; Stubbs, B.; Cuesta-Vargas, A.I. A systematic review of the benefits of physical therapy within a multidisciplinary care approach for people with schizophrenia: An update. Psychiatr. Res. 2015, 229, 828–839. [Google Scholar] [CrossRef]
  34. Brach, J.S.; VanSwearingen, J.M.; Lenert, J.; Johnson, P.C. Facial neuromuscular retraining for oral synkinesis. Plast. Reconstr. Surg. 1997, 99, 1922–1933. [Google Scholar] [CrossRef]
  35. VanSwearingen, J.M.; Brach, J.S. Changes in facial movement and synkinesis with facial neuromuscular reeducation. Plast. Reconstr. Surg. 2003, 111, 2370–2375. [Google Scholar] [CrossRef]
  36. Manikandan, N. Effect of facial neuromuscular re-education on facial symmetry in patients with Bell’s palsy: A randomized controlled trial. Clin. Rehabil. 2007, 21, 338–343. [Google Scholar] [CrossRef]
  37. VanSwearingen, J. Facial rehabilitation: A neuromuscular reeducation, patient-centered approach. Facial Plast. Surg. 2008, 24, 250–259. [Google Scholar] [CrossRef]
  38. Baumel, J.J. Trigeminal-Facial Nerve Communications: Their Function in Facial Muscle Innervation and Reinnervation. Arch. Otolaryngol. 1974, 99, 34–44. [Google Scholar] [CrossRef] [PubMed]
  39. Burgess, P.R.; Wei, J.Y.; Clark, F.J.; Simon, J. Signaling of kinesthetic information by peripheral sensory receptors. Annu. Rev. Neurosci. 1982, 5, 171–187. [Google Scholar] [CrossRef]
  40. Ekman, P.; Friesen, W.V.; Hager, J.C. Emotional Facial Action Coding System. Manual and Investigator’s Guide; Research Nexus: Salt Lake City, UT, USA, 2002. [Google Scholar]
  41. Buccino, G. Action observation treatment: A novel tool in neurorehabilitation. Philos. Trans. R. Soc. B Biol. Sci. 2014, 369, 20130185. [Google Scholar] [CrossRef] [PubMed]
  42. Pollak, S.D.; Kistler, D.J. Early experience is associated with the development of categorical representations for facial expressions of emotion. Proc. Natl. Acad. Sci. USA 2002, 99, 9072–9076. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  43. Decety, J.; Chaminade, T. The Neurophysiology of Imitation and Intersubjectivity. In Perspectives on Imitation; Hurley, S., Chater, N., Eds.; The MIT Press: Cambridge, MA, USA, 2005; pp. 119–140. [Google Scholar]
  44. Gallese, V. The roots of empathy: The shared manifold hypothesis and the neural basis of intersubjectivity. Psychopathology 2003, 36, 171–180. [Google Scholar] [CrossRef]
  45. Gallese, V. Embodied Simulation: From Mirror Neuron Systems to Interpersonal Relations. In Empathy and Fairness; Wiley: New York, NY, USA, 2008; pp. 3–12. ISBN 9780470030585. [Google Scholar]
  46. Keysers, C.; Gazzola, V. Integrating simulation and theory of mind: From self to social cognition. Trends Cogn. Sci. 2007, 11, 194–196. [Google Scholar] [CrossRef]
  47. Dimberg, U. Facial Reactions to Facial Expressions. Psychophysiology 1982, 19, 643–647. [Google Scholar] [CrossRef]
  48. Korb, S.; Grandjean, D.; Scherer, K.R. Timing and voluntary suppression of facial mimicry to smiling faces in a Go/NoGo task-An EMG study. Biol. Psychol. 2010, 85, 347–349. [Google Scholar] [CrossRef]
  49. Dimberg, U.; Thunberg, M.; Grunedal, S. Facial reactions to emotional stimuli: Automatically controlled emotional responses. Cogn. Emot. 2002, 16, 449–471. [Google Scholar] [CrossRef]
  50. Bornemann, B.; Winkielman, P.; van der Meer, E. Can you feel what you do not see? Using internal feedback to detect briefly presented emotional stimuli. Int. J. Psychophysiol. 2012, 85, 116–124. [Google Scholar] [CrossRef]
  51. Dimberg, U.; Thunberg, M.; Elmehed, K. Unconscious facial reactions to emotional facial expressions. Psychol. Sci. 2000, 11, 86–89. [Google Scholar] [CrossRef] [PubMed]
  52. Bulnes, L.C.; Mariën, P.; Vandekerckhove, M.; Cleeremans, A. The effects of Botulinum toxin on the detection of gradual changes in facial emotion. Sci. Rep. 2019, 9, 11734. [Google Scholar] [CrossRef] [Green Version]
  53. Davis, J.D.; Winkielman, P.; Coulson, S. Sensorimotor simulation and emotion processing: Impairing facial action increases semantic retrieval demands. Cogn. Affect. Behav. Neurosci. 2017, 17, 652–664. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  54. Niedenthal, P.M.; Brauer, M.; Halberstadt, J.B.; Innes-Ker, Å.H. When did her smile drop? Facial mimicry and the influences of emotional state on the detection of change in emotional expression. Cogn. Emot. 2001, 15, 853–864. [Google Scholar] [CrossRef]
  55. Oberman, L.M.; Winkielman, P.; Ramachandran, V.S. Face to face: Blocking facial mimicry can selectively impair recognition of emotional expressions. Soc. Neurosci. 2007, 2, 167–178. [Google Scholar] [CrossRef]
  56. Neal, D.T.; Chartrand, T.L. Embodied emotion perception: Amplifying and dampening facial feedback modulates emotion perception accuracy. Soc. Psychol. Personal. Sci. 2011, 2, 673–678. [Google Scholar] [CrossRef]
  57. Stel, M.; Van Knippenberg, A. The role of facial mimicry in the recognition of affect. Psychol. Sci. 2008, 19, 984–985. [Google Scholar] [CrossRef] [PubMed]
  58. Kring, A.M.; Moran, E.K. Emotional response deficits in schizophrenia: Insights from affective science. Schizophr. Bull. 2008, 34, 819–834. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  59. Berenbaum, H.; Oltmanns, T.F. Emotional Experience and Expression in Schizophrenia and Depression. J. Abnorm. Psychol. 1992, 101, 37–44. [Google Scholar] [CrossRef]
  60. Salem, J.E.; Kring, A.M. Flat affect and social skills in schizophrenia: Evidence for their independence. Psychiatr. Res. 1999, 87, 159–167. [Google Scholar] [CrossRef]
  61. Earnst, K.S.; Kring, A.M. Emotional responding in deficit and non-deficit schizophrenia. Psychiatr. Res. 1999, 88, 191–207. [Google Scholar] [CrossRef]
  62. Henry, J.D.; Green, M.J.; de Lucia, A.; Restuccia, C.; McDonald, S.; O’Donnell, M. Emotion dysregulation in schizophrenia: Reduced amplification of emotional expression is associated with emotional blunting. Schizophr. Res. 2007, 95, 197–204. [Google Scholar] [CrossRef] [PubMed]
  63. Kring, A.M.; Earnst, K.S. Stability of emotional responding in schizophrenia. Behav. Ther. 1999, 30, 373–388. [Google Scholar] [CrossRef]
  64. Kring, A.M.; Kerr, S.L.; Smith, D.A.; Neale, J.M. Flat Affect in Schizophrenia Does Not Reflect Diminished Subjective Experience of Emotion. J. Abnorm. Psychol. 1993, 102, 507–517. [Google Scholar] [CrossRef]
  65. Kring, A.M.; Neale, J.M. Do schizophrenic patients show a disjunctive relationship among expressive, experiential, and psychophysiological components of emotion? J. Abnorm. Psychol. 1996, 105, 249–257. [Google Scholar] [CrossRef] [PubMed]
  66. Mattes, R.M.; Schneider, F.; Heimann, H.; Birbaumer, N. Reduced emotional response of schizophrenic patients in remission during social interaction. Schizophr. Res. 1995, 17, 249–255. [Google Scholar] [CrossRef]
  67. Blanchard, J.J.; Sayers, S.L.; Collins, L.M.; Bellack, A.S. Affectivity in the problem-solving interactions of schizophrenia patients and their family members. Schizophr. Res. 2004, 69, 105–117. [Google Scholar] [CrossRef] [PubMed]
  68. Borod, J.C.; Alpert, M.; Brozgold, A.; Martin, C.; Welkowitz, J.; Diller, L.; Peselow, E.; Angrist, B.; Lieberman, A. A preliminary comparison of flat affect schizophrenics and brain-damaged patients on meausres of affective processing. J. Commun. Disord. 1989, 22, 93–104. [Google Scholar] [CrossRef]
  69. Gaebel, W.; Wölwer, W. Facial expressivity in the course of schizophrenia and depression. Eur. Arch. Psychiatr. Clin. Neurosci. 2004, 254, 335–342. [Google Scholar] [CrossRef] [PubMed]
  70. Krause, R.; Steimer, E.; Sänger-Alt, C.; Wagner, G. Facial Expression of Schizophrenic Patients and Their Interaction Partners. Psychiatry 1989, 52, 1–12. [Google Scholar] [CrossRef]
  71. Kring, A.M.; Alpert, M.; Neale, J.M.; Harvey, P.D. A multimethod, multichannel assessment of affective flattening in schizophrenia. Psychiatr. Res. 1994, 54, 211–222. [Google Scholar] [CrossRef]
  72. Martin, C.C.; Borod, J.C.; Alpert, M.; Brozgold, A.; Welkowitz, J. Spontaneous expression of facial emotion in schizophrenic and right-brain-damaged patients. J. Commun. Disord. 1990, 23, 287–301. [Google Scholar] [CrossRef]
  73. Trémeau, F.; Malaspina, D.; Duval, F.; Corrêa, H.; Hager-Budny, M.; Coin-Bariou, L.; Macher, J.P.; Gorman, J.M. Facial expressiveness in patients with schizophrenia compared to depressed patients and nonpatient comparison subjects. Am. J. Psychiatr. 2005, 162, 92–101. [Google Scholar] [CrossRef] [Green Version]
  74. Aghevli, M.A.; Blanchard, J.J.; Horan, W.P. The expression and experience of emotion in schizophrenia: A study of social interactions. Psychiatr. Res. 2003, 119, 261–270. [Google Scholar] [CrossRef]
  75. Horan, W.P.; Kern, R.S.; Green, M.F.; Penn, D.L. Social cognition training for individuals with schizophrenia: Emerging evidence. Am. J. Psychiatr. Rehabil. 2008, 11, 205–252. [Google Scholar] [CrossRef]
  76. Jin, H.C.; Jin, H.K.; Lee, J.; Green, M.F. Social cognition training for individuals with schizophrenia: A review of targeted interventions. Clin. Psychopharmacol. Neurosci. 2009, 7, 29–38. [Google Scholar]
  77. Wölwer, W.; Combs, D.R.; Frommann, N.; Penn, D.L. Treatment approaches with a special focus on social cognition: Overview and empirical results. In Neurocognition and Social Cognition in Schizophrenia Patients: Basic Concepts and Treatment; Karger Medical and Scientific Publishers: Basel, Switzerland, 2010; Volume 177, pp. 61–78. ISBN 9783805593397. [Google Scholar]
  78. Wölwer, W.; Frommann, N. Social-cognitive remediation in schizophrenia: Generalization of effects of the training of affect recognition (TAR). Schizophr. Bull. 2011, 37, S63–S70. [Google Scholar] [CrossRef] [Green Version]
  79. Wölwer, W.; Frommann, N.; Halfmann, S.; Piaszek, A.; Streit, M.; Gaebel, W. Remediation of impairments in facial affect recognition in schizophrenia: Efficacy and specificity of a new training program. Schizophr. Res. 2005, 80, 295–303. [Google Scholar] [CrossRef]
  80. Frommann, N.; Streit, M.; Wölwer, W. Remediation of facial affect recognition impairments in patients with schizophrenia: A new training program. Psychiatr. Res. 2003, 117, 281–284. [Google Scholar] [CrossRef]
  81. Gorczynski, P.; Faulkner, G. Exercise therapy for schizophrenia. Schizophr. Bull. 2010, 36. [Google Scholar] [CrossRef]
  82. Firth, J.; Cotter, J.; Elliott, R.; French, P.; Yung, A.R. A systematic review and meta-analysis of exercise interventions in schizophrenia patients. Psychol. Med. 2015, 45, 1343–1361. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Figure 1. The 88 stimuli used in the facial expression categorization test, separated for each continuum.
Figure 1. The 88 stimuli used in the facial expression categorization test, separated for each continuum.
Brainsci 11 00825 g001
Figure 2. Mean values of responses for each emotion (happiness, fear, anger, sadness), for the experimental (leftmost panel) and control (rightmost panel) group, at Test 1 (black bars) and Test 2 (grey bars). * indicate statistically significant comparisons. Thin lines above histograms indicate standard error of the mean.
Figure 2. Mean values of responses for each emotion (happiness, fear, anger, sadness), for the experimental (leftmost panel) and control (rightmost panel) group, at Test 1 (black bars) and Test 2 (grey bars). * indicate statistically significant comparisons. Thin lines above histograms indicate standard error of the mean.
Brainsci 11 00825 g002
Table 1. List of participants, indicating the relative age, gender, ICD-10 code, and the main symptoms. Specifically, the codes pertaining to the participants are: (i) F20.0 paranoid schizophrenia; (ii) F20.1 hebephrenic schizophrenia; (iii) F20.5 residual schizophrenia; (iv) F25.2 schizoaffective disorder, mixed type.
Table 1. List of participants, indicating the relative age, gender, ICD-10 code, and the main symptoms. Specifically, the codes pertaining to the participants are: (i) F20.0 paranoid schizophrenia; (ii) F20.1 hebephrenic schizophrenia; (iii) F20.5 residual schizophrenia; (iv) F25.2 schizoaffective disorder, mixed type.
Experimental GroupControl Group
AgeGenderICD-10 CodeMain SymptomsAgeGenderICD-10 CodeMain Symptoms
57MF 20.5Affective flattening; poverty of speech; reduced social functioning33MF 20.0Chronic persecutory delusional disorder; auditory hallucinations
62MF 25.2Persecutory delusional ideas; emotional instability; relational isolation50MF 20.0Chronic persecutory delusional disorder
45FF 25.2Affective instability; delusional persecutory cues; incongruity of thought40FF 20.1Alterations of affectivity; fluctuating hallucinations; disorganized behavior and thinking
57FF 20.0Persecutory delusional ideation; auditory hallucinations56MF 20.0Chronic persecutory and erotomanic delusional disorder; auditory hallucinations
41FF 25.2Affective instability; delusional persecutory cues; incongruity of thought34FF 20.0Chronic persecutory delusional disorder
35FF 20.1Alterations of affectivity; fluctuating and fragmentary delusions; unpredictable behavior54FF 20.0Mystical Chronic Delusional Disorder
53MF 20.5Affective flattening; poverty of speech; reduced social functioning53MF 20.0Chronic persecutory delusional disorder
63FF 20.1Alterations of affectivity; fluctuating delusions and hallucinations; mannerisms; fatuous and inappropriate mood; disorganized thinking; incoherent speech42MF 25.2Persecutory delusional ideas; mind reading; emotional instability
55FF 20.1Affective flattening; loss of initiative; social isolation66MF 20.0Chronic persecutory delusional disorder; apathy; abulia; relational isolation
52MF 20.5Affective flattening; poverty of speech; reduced social functioning56MF 20.0Chronic persecutory delusional disorder; apathy; abulia; relational isolation
58FF 20.0Chronic persecutory delusional disorder49MF 20.5Psychomotor slowdown; psychoaffective flattening; passivity and lack of initiative; poverty of speech
62FF 20.1Affective flattening; loss of initiative; social isolation45MF 20.5Affective flattening; poverty of speech; reduced social functioning
Table 2. List of expressions considered in the facial expression categorization test and relative FACS action units [40].
Table 2. List of expressions considered in the facial expression categorization test and relative FACS action units [40].
EmotionAction Units (AUs)
Anger4 + 5 + 7 + 23
Fear1 + 2 + 4 + 5 + 7 + 20 + 26
Happiness6 + 12
Sadness1 + 4 + 15
Table 3. List of FACS action units, relative action descriptors, and underlying facial muscles [40], of the expressions considered in the facial expression categorization test.
Table 3. List of FACS action units, relative action descriptors, and underlying facial muscles [40], of the expressions considered in the facial expression categorization test.
AU NumberAction DescriptorMuscular Basis
1Inner brow raiserFrontalis (Pars Medialis)
2Outer brow raiserFrontalis (Pars Lateralis)
4Brow lowererDepressor Glabellae
Depressor Supercilii
Corrugator Supercilii
5Upper lid raiserLevator Palpebrae Superioris Superior Tarsal Muscle
6Cheek raiserOrbicularis Oculi
(Pars Orbitalis)
7Lid tightenerOrbicularis Oculi
(Pars Palpebralis)
12Lip corner pullerZygomaticus Major
15Lip corner depressorDepressor Anguli Oris
20Lip stretcherRisorius, Platysma
23Lip tightenerOrbicularis Oris
26Jaw dropMasseter
Table 4. List of facial exercises.
Table 4. List of facial exercises.
Facial DistrictExercise
Mobilization of the lipshold a stick horizontally between the teeth without touching it with the lips
hold a stick horizontally between the lips without touching it with the teeth
hold a stick vertically between the lips without touching it with the teeth
hold objects of varying heaviness between the upper lip and nose
hold round objects of various sizes and textures between the lips
push a small ball towards a target by blowing through a straw
make bubbles in different amounts of water by blowing through a straw
inflate balloons with different resistance
make soap bubbles
Mobilization of the muscles around the eyesmove the glasses placed on the nose upwards using the cheek muscles
hold round objects of various sizes by tightly contracting the muscles around both eyes
hold round objects of various sizes by tightly contracting the muscles around one eye, and look with the other eye
remove a little piece of paper placed between the eyebrows by frowning
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Pancotti, F.; Mele, S.; Callegari, V.; Bivi, R.; Saracino, F.; Craighero, L. Efficacy of Facial Exercises in Facial Expression Categorization in Schizophrenia. Brain Sci. 2021, 11, 825. https://doi.org/10.3390/brainsci11070825

AMA Style

Pancotti F, Mele S, Callegari V, Bivi R, Saracino F, Craighero L. Efficacy of Facial Exercises in Facial Expression Categorization in Schizophrenia. Brain Sciences. 2021; 11(7):825. https://doi.org/10.3390/brainsci11070825

Chicago/Turabian Style

Pancotti, Francesco, Sonia Mele, Vincenzo Callegari, Raffaella Bivi, Francesca Saracino, and Laila Craighero. 2021. "Efficacy of Facial Exercises in Facial Expression Categorization in Schizophrenia" Brain Sciences 11, no. 7: 825. https://doi.org/10.3390/brainsci11070825

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop