INTRODUCTION
Social functioning deficits are more pronounced in schizophrenia than in any other psychiatric illness (Mueser & Bellack, Reference Mueser, Bellack, Mueser and Tarrier1998), with social cognitive impairment consistently identified as a key predictor of social function outcomes (Brekke, Hoe, Long, & Green, Reference Brekke, Hoe, Long and Green2007; Brüne, Reference Brüne2005; Pijnenborg, Withaar, Evans, van den Bosch, Timmerman, & Brouwer, Reference Pijnenborg, Withaar, Evans, van den Bosch, Timmerman and Brouwer2009). Much of this social cognitive research has focused on higher-level aspects of empathic behavior, and in particular emotion recognition (decoding of affective cues) and cognitive empathy (the understanding of another’s beliefs and desires), with impairments consistently identified in both of these components (Brüne, Reference Brüne2005; Edwards, Jackson, & Pattison, Reference Edwards, Jackson and Pattison2002; Langdon, Coltheart, & Ward, Reference Langdon, Coltheart and Ward2006). However, empathy is a multifaceted construct that is considered to involve not only higher-level facets, but also lower-level facets such as the emotional experience of a perceived affective state, often referred to as affective empathy (Baron-Cohen, Reference Baron-Cohen, Ellis and Bjorklund2005; Decety & Meyer, Reference Decety and Meyer2008; Leiberg & Anders, Reference Leiberg and Anders2006; Preston & de Waal, Reference Preston and de Waal2002; Singer & Lamm, Reference Singer and Lamm2009). Preliminary evidence indicates that, as with the other facets of empathy, affective empathy is disrupted in schizophrenia (Derntl et al., Reference Derntl, Finkelmeyer, Toygar, Hulsmann, Schneider and Falkenberg2009; Shamay-Tsoory, Shur, Harari, & Levkovitz, Reference Shamay-Tsoory, Shur, Harari and Levkovitz2007).
Although empathic deficits are well documented in schizophrenia, the precise mechanisms contributing to these difficulties have not yet been identified. Specifically, there is a relative dearth of research examining early or low-level processes that are involved in the experience of empathy in this population. As such, it is unclear as to whether a disruption in the low-level processes that are associated with empathic responding, may be underlying any empathic difficulties in this group. One such low-level mechanism that has been identified as an important contributor to an empathic response is rapid facial mimicry (for a review, see Singer & Lamm, Reference Singer and Lamm2009). This response refers to the tendency for individuals to involuntarily and rapidly synchronize their facial expressions with observed expressions (Dimberg, Reference Dimberg1982; Dimberg & Lundqvist, Reference Dimberg and Lundqvist1988, Reference Dimberg and Lundqvist1990; Dimberg, Thunberg, & Elmehed, Reference Dimberg, Thunberg and Elmehed2000). This form of motor mimetic responding has been considered as contributing to the experience of empathy (e.g., see Singer & Lamm, Reference Singer and Lamm2009) as well as a form of empathy in its own right (Blair, Reference Blair2005).
Involuntary facial mimicry has been implicated in, and thought to facilitate, empathy via a process of simulation (Decety & Jackson, Reference Decety and Jackson2004; Oberman & Ramachandran, Reference Oberman and Ramachandran2007). According to the simulation account, we come to empathize with others by involuntarily and subconsciously mimicking (i.e., “mirroring”) the observed emotional expressions of others; this mimicry, or embodied representation, facilitates emotion understanding and serves to induce an appropriate empathic response (Adolphs, Reference Adolphs2002; Decety & Jackson, Reference Decety and Jackson2004; Preston & deWaal, Reference Preston and de Waal2002). Rapid facial mimicry in response to the observation of others’ emotional facial expressions has been interpreted as evidence for this simulation account of empathy (Oberman & Ramachandran, Reference Oberman and Ramachandran2007). Consistent with this notion, functional magnetic resonance imaging (fMRI) indicates that in nonclinical volunteers the observation and imitation of emotional facial expressions activates a similar neural network (Carr, Iacobone, Dubearu, Mazziotta, & Lenzi, Reference Carr, Iacoboni, Dubeau, Mazziotta and Lenzi2003).
The simulationist view of empathy is linked to perception-action models of empathic responding putatively argued to be supported by the human mirror neuron system (MNS; Preston & deWaal, Reference Preston and de Waal2002). Originally identified in macaque monkeys, mirror neurons refer to cortical brain cells that are named due to their tendency to activate both when an individual performs an action and when an individual observes the same action performed by another (Buccino & Amore, Reference Buccino and Amore2008; di Pellegrino, Fadiga, Fogassi, Gallese, & Rizzolatti, Reference di Pellegrino, Fadiga, Fogassi, Gallese and Rizzolatti1992). Although ongoing controversy remains surrounding the precise specificity and brain regions involved, in humans, neuroimaging studies have provided evidence for a network that appears to subserve such perception-action coupling—the human MNS (Decety, Chaminade, Grezes, & Meltzoff, Reference Decety, Chaminade, Grezes and Meltzoff2002; Iacoboni, Woods, Brass, Bekkering, Mazziotta, & Rizzolatti, Reference Iacoboni, Woods, Brass, Bekkering, Mazziotta and Rizzolatti1999; Iacoboni et al., Reference Iacoboni, Koski, Brass, Bekkering, Woods and Dubeau2001). Some key components of this network are considered to be the superior temporal sulcus, inferior parietal lobe, and inferior frontal gyrus (Iacoboni & Dapretto, Reference Iacoboni and Dapretto2006; Rizzolatti & Craighero, Reference Rizzolatti and Craighero2004).
Importantly, social cognitive difficulties in first episode psychosis have been shown to be related to structural abnormalities in the MNS network, and it has been argued that these, “. . . may account for the social cognitive deficits present in some psychiatric disorders, such as schizophrenia.” (p. 79, Bertrand, Achim, Harvey, Sutton, Malla, & Lepage, Reference Enticott, Hoy, Herring, Johnston, Daskalakis and Fitzgerald2008). Moreover, in a recent transcranial magnetic stimulation experiment, Enticott, Hoy, Herring, Johnston, Daskalakis, and Fitzgerald (Reference Enticott, Hoy, Herring, Johnston, Daskalakis and Fitzgerald2008) provided preliminary evidence that individuals with schizophrenia demonstrated reduced mirror neuron activation in premotor cortices of the brain compared with nonclinical individuals. Taken together, there are compelling reasons for assessing whether rapid facial mimicry responses are disrupted in this population.
Rapid facial mimicry responses are generally detected using facial electromyography (EMG; measurement of changes in the electrical activity of muscles), a technique which is sensitive to even subtle changes in facial muscle activity. Numerous EMG studies have shown that distinct facial reactions are reliably elicited by the mere perception of emotional facial expressions (Dimberg, Reference Dimberg1982; Dimberg & Thunberg, Reference Dimberg and Thunberg1998; Dimberg et al., Reference Dimberg, Thunberg and Elmehed2000). That is, images of angry facial expressions evoke increased corrugator supercilii (i.e., brow) activity relative to happy facial expressions, and images of happy facial expressions evoke increased zygomaticus major (i.e., cheek) activity relative to angry (Dimberg, Reference Dimberg1982; Dimberg & Petterson, Reference Dimberg and Petterson2000; Dimberg & Thunberg, Reference Dimberg and Thunberg1998; Dimberg et al., Reference Dimberg, Thunberg and Elmehed2000; Dimberg, Thunberg, & Grunedal, Reference Dimberg, Thunberg and Grunedal2002). Facial mimicry reactions in nonclinical individuals reliably occur within one second of stimulus presentation (Bailey, Henry, & Nangle, Reference Bailey, Henry and Nangle2009; Dimberg et al., Reference Dimberg, Thunberg and Elmehed2000; Moody, McIntosh, Mann, & Weisser, Reference Moody, McIntosh, Mann and Weisser2007). Furthermore, attesting to the robust nature of this response, facial mimicry has been shown to occur within one second of stimulus exposure following explicit instructions not to react (Dimberg et al., Reference Dimberg, Thunberg and Grunedal2002) and when images are presented subliminally (Bailey & Henry, Reference Bailey and Henry2009; Dimberg et al., Reference Dimberg, Thunberg and Elmehed2000).
The primary aim of the present study was to provide the first assessment of whether low-level rapid facial mimicry reactions are, as with other empathic behaviors, disrupted in schizophrenia. The few EMG studies that have been conducted in this group have predominantly examined facial reactions in response to nonfacial stimuli (Mattes, Schneider, Heimann, & Birbaumer, Reference Mattes, Schneider, Heimann and Birbaumer1995; Wolf et al., Reference Wolf, Mass, Kiefer, Eckert, Weinhold and Wiedemann2004; Wolf, Mass, Kiefer, Wiedemann, & Naber, Reference Wolf, Mass, Kiefer, Wiedemann and Naber2006). Furthermore, the one EMG study that has presented images of facial stimuli examined facial responding over an extended timeframe (collapsed across seven seconds poststimulus exposure; Kring, Kerr, Earnst, Reference Kring, Kerr and Earnst1999). The results indicated that zygomaticus activity in the schizophrenia group was comparable to that of the control group when exposed to positive facial expressions. Unexpectedly, however, the schizophrenia group exhibited greater corrugator activity when exposed to negative facial expressions, and Kring et al. suggested that this may not have been a “mimicry” reaction per se, but instead may have reflected processes related to confusion.
Importantly, facial EMG responses that occur within 1 s poststimulus exposure are less susceptible to the influences of puzzlement and confusion due to their relative rapidity, spontaneity, and subconscious nature (Dimberg et al., Reference Dimberg, Thunberg and Elmehed2000; Moody & McIntosh, Reference Moody, McIntosh, Rogers and Williams2006). Thus, although Kring et al. (Reference Kring, Kerr and Earnst1999) identified an intact mimicry response in those with schizophrenia over an extended timeframe, it was predicted that because empathic behaviors are disrupted in this group (and have been argued to reflect structural abnormalities in the human MNS; Bertrand et al., Reference Bertrand, Achim, Harvey, Sutton, Malla and Lepage2008) schizophrenia would be associated with abnormalities in the empathy-related rapid facial mimicry response. A secondary aim was to assess whether any observed abnormalities in facial muscle activity are related to clinical symptoms of the disorder, and in particular, blunted affect.
METHOD
Participants
Twenty-five clinical participants (10 males) and 25 controls (11 males) completed this study. All clinical participants were recruited from outpatient clinics in Sydney, and had received diagnoses of schizophrenia (n = 15) or schizoaffective disorder (n = 10) by treating psychiatrists according to the DSM-IV (American Psychiatric Association, 1994). All participants were aged over 18 and in a stable phase of illness. No significant differences were observed between schizoaffective or schizophrenia participants on any of the experimental variables of interest. The control participants were recruited from the general community via advertisements. All participants received approximately AUD$10 per hour (≈ US$9) for participation, and exclusion criteria included a neurological disorder, presence of motor abnormalities, alcohol/drug abuse, or any sensory impairment that would interfere with testing. Control participants were additionally screened to ensure that they had no personal history of psychopathology.
Background information for the two groups is reported in Table 1. In addition to being closely matched for gender (40% vs. 44% male for the schizophrenia and control groups, respectively), it can be seen that the two groups did not differ in age or years of education. The two groups were also matched with regard to current intelligence as indexed by the Wechsler Abbreviated Scale of Intelligence (WASI; Wechsler, Reference Wechsler1999), as well as premorbid intelligence as indexed by prorated Full Scale IQ on the National Adult Reading Test (NART; Nelson & Willison, Reference Nelson and Willison1991). However, greater negative affect, as indexed by the Depression Anxiety Stress Scales-21 (DASS-21; Lovibond & Lovibond, Reference Lovibond and Lovibond1995), was reported by the schizophrenia group relative to the control group.
Characteristics of the schizophrenia and control participants
Note
Data for the NART, WASI, and SAPS/SANS are missing for one clinical participant. WASI refers to Wechsler Abbreviated Scale of Intelligence; NART refers to National Adult Reading Test; SAPS refers to the Scale for the Assessment of Positive Symptoms; SANS refers to the Scale for the Assessment of Negative Symptoms; CPZ refers to chlorpromazine; DASS-21 refers to the Depression Anxiety Stress Scales.
a Although this conversion is controversial as applied to atypical antipsychotics, it is nevertheless useful for assessing broad trends across patient groups. For details on the conversion procedure used, see Henry, Green, de Lucia, Restuccia, McDonald, and O’Donnell (Reference Henry, Green, de Lucia, Restuccia, McDonald and O’Donnell2007).
Twenty-four clinical participants were receiving antipsychotic medication (21 atypical, 2 typical, 1 combined typical and atypical). It can be seen in Table 1 that the mean dose of antipsychotic medication received was very comparable to the mean dosage levels reported by a large-scale audit of outpatient antipsychotic usage (360 ± 253 mg/day chlorpromazine equivalents; Humberstone, Wheeler, & Lambert, Reference Humberstone, Wheeler and Lambert2004). It can also be seen that, while the average age of onset and duration of illness indicated the clinical sample were chronic (20.2 and 22.7 years, respectively), scores on the Scale for the Assessment of Negative Symptoms (SANS; Andreasen, Reference Andreasen1984a) and the Scale for the Assessment of Positive Symptoms (SAPS; Andreasen, Reference Andreasen1984b), indicated a relatively mild level of symptom presentation (consistent with all participants presenting in a stable phase of illness).
Procedure and Measures
Passive viewing facial electromyography paradigm
The current study closely followed the procedures set out by Bailey et al. (Reference Bailey, Henry and Nangle2009). Consistent with prior research demonstrating greater expressivity in the muscle regions of the left side of the face (see, e.g., Dimberg & Petterson, Reference Dimberg and Petterson2000), surface EMG was used to record changes in the levels of muscle activity over the left corrugator and zygomaticus regions. Recording over these regions to index responding to angry and happy expressions is considered standard in facial EMG research, as corrugator activity has been shown to be a sensitive marker of angry expressions and zygomaticus activity is particularly responsive to expressions of happiness (Tassinary & Cacioppo, Reference Tassinary, Cacioppo, Cacioppo, Tassinary and Bernston2000). Site preparation and electrode placement adhered to the standard procedure set out by Tassinary and Cacioppo (Reference Tassinary, Cacioppo, Cacioppo, Tassinary and Bernston2000). The skin over the zygomaticus, corrugator, and center of the forehead was cleansed with an alcohol wipe and then gently abraded with NuPrep gel (Weaver and Co., Aurora, CO). Four gold-plated bipolar surface electrodes, with hat-shaped discs and 9-mm housings, were placed in pairs over the left zygomaticus and corrugator muscle regions, roughly parallel to the length of the muscle, with an interelectrode distance of approximately 1.25 cm; an additional electrode was placed approximately in the center of the forehead, acting as a ground. The electrodes were attached with Ten20 conductive paste (Weaver and Co.) and fastened with medical tape. Muscle activity was continuously recorded with a PowerLab 8/30 Data Acquisition System (AD Instruments, Castle Hill, Australia) at a sampling rate of 2000 Hz with a 10- to 500-Hz bandpass filter, a 60-Hz notch filter, and an amplification factor of 20,000. The PowerLab was triggered by DMDX (Version 3.2.3.0), software that precisely synchronized timing of the facial expression presentations with the recording of the data acquisition system.
Participants were told that they would be watching a series of stimuli on a monitor and that they should try to remain still throughout the procedure. To disguise the true purpose of the study, participants were also told that the EMG sensors were measuring changes in sweat gland activity (see Bailey et al., Reference Bailey, Henry and Nangle2009). The stimuli were 16 × 24 cm black and white pictures of happy and angry facial expressions (Ekman & Friesen, Reference Ekman and Friesen1976) that were presented approximately 60 cm in front of the participant. Each trial commenced with a 50 ms soft orienting tone which was followed by the presentation of a facial expression 1 s later. Each face was displayed on the monitor for 5 s, followed by a blank screen for 6 s. Consistent with several previous studies (Bailey et al., Reference Bailey, Henry and Nangle2009; Dimberg & Thunberg, Reference Dimberg and Thunberg1998; McIntosh, Reichmann-Decker, Winkielman, & Wilbarger, Reference McIntosh, Reichmann-Decker, Winkielman and Wilbarger2006), pictures of eight different people (four male, four female) were presented to participants. Happy and angry expressions were presented in nonmixed randomized blocks of eight trials (e.g., eight happy images, followed by eight angry images). Again, this procedure was consistent with prior research examining facial EMG reactions to facial stimuli (see Bailey et al., Reference Bailey, Henry and Nangle2009; Dimberg, Reference Dimberg1982; Dimberg & Lundqvist, Reference Dimberg and Lundqvist1990; Dimberg & Petterson, Reference Dimberg and Petterson2000; Dimberg & Thunberg, Reference Dimberg and Thunberg1998; McIntosh et al., Reference McIntosh, Reichmann-Decker, Winkielman and Wilbarger2006). Each participant viewed a total of two blocks (one happy, one angry), and these blocks were counterbalanced across participants.
Raw EMG signals were screened for electrical noise and movement artifacts. In addition, a coder who was blind to condition watched videotapes of each participant and noted when they were not watching the stimulus or when they made extraneous movements such as yawning. These amounted to less than 5% of trials, which were deleted from subsequent analyses. An orienting tone, rather than a fixation cross, was used because it alerted the participant to the presentation of the stimulus, and indicated to the rater the time at which they should expect the participant to be looking at the monitor.
The average EMG signal was calculated using the root-mean-square (RMS) method, which represents the square root of the average power of the EMG signal over a given period of time (Tassinary & Cacioppo, Reference Tassinary, Cacioppo, Cacioppo, Tassinary and Bernston2000). The baseline for each trial was calculated as the average RMS EMG activity 500 ms before each stimulus presentation. The average of each 100 ms period was calculated separately for each expression valence (eight happy, eight angry) to reduce potential variability of responding across trials. Subsequently, the average RMS EMG percentage change from baseline (normalized EMG), averaged across individual trials within each block, was calculated for the window 0–1000 ms poststimulus onset. Consistent with research suggesting that in nonclinical individuals rapid facial mimicry reactions occur within one second of stimulus onset (Dimberg et al., Reference Dimberg, Thunberg and Grunedal2002; McIntosh et al., Reference McIntosh, Reichmann-Decker, Winkielman and Wilbarger2006), facial muscle activity in the period 0–1000 ms poststimulus onset was considered for examination of rapid facial mimicry reactions.
Administration of facial EMG and the measures of cognitive and clinical functioning were counterbalanced. All testing procedures received ethical approval from the South Eastern Sydney Area Health Service in conjunction with the University of New South Wales.
RESULTS
EMG Response to Facial Emotion Stimuli
For the EMG analyses, the first step was to examine whether any group differences in average corrugator and zygomaticus EMG activity emerged for the 500 ms before presentation of the facial stimuli. Averaged across the eight stimulus presentations for each block, there were no group differences in either corrugator or zygomaticus baseline activity (all ps > .05).
The next step was to ascertain whether there were overall differences between the two groups in magnitude of responding to the facial stimuli. Independent samples t tests indicated that there were no differences in the level of corrugator or zygomaticus activity between the schizophrenia and control groups, averaged across angry and happy emotional stimuli (p = .365 and p = .263, respectively). In addition, differences in facial responding were examined between the schizophrenia and schizoaffective groups. Independent samples t tests indicated comparable responding in the schizophrenia and schizoaffective groups in both corrugator and zygomaticus regions to happy and angry images (all ps > .05). There were also no differences in the level of corrugator or zygomaticus activity between the schizophrenia and schizoaffective groups, averaged across angry and happy emotional stimuli (all ps > .05).
The pattern of facial responding was then assessed—and specifically, whether appropriate mimicry responses were shown by each group (i.e., whether zygomaticus activity was greater in response to happy relative to angry facial expressions, and whether corrugator activity was greater in response to angry relative to happy expressions). A 2 (group: control, schizophrenia) × 2 (target expression: happy, angry) × 10 (time poststimulus onset: 0–100, 100–200, 200–300, 300–400, 400–500, 500–600, 600–700, 700–800, 800–900, 900–1000 ms) repeated-measures mixed-design analysis of variance was conducted separately for the zygomaticus and corrugator muscle regions. The statistical assumptions for conventional repeated measures procedures were met. Data for the zygomaticus and corrugator responses for each group are shown in Figure 1.
Mean corrugator and zygomaticus electromyographic response as percentage change from baseline (+SE) to angry and happy stimuli for control and schizophrenia participants.
For the zygomaticus region, there was no main effect of emotion, F(1,48) = 1.00; p = .321; ηp2 = .02, or of group, F(1,48) = 1.28; p = .263; ηp2 = .02. There was also no interaction between emotion and time, F(9,432) = 1.53; p = .134; ηp2 = .03, time and group, F(9,432) = 0.69; p = .720; ηp2 = .014 and no three-way interaction between emotion, time and group, F(9,432) = 1.20; p = .296, ηp2 = .02. However, there was a main effect of time, F(9, 432) = 4.31, p < .001; ηp2 = .08, and most importantly, an interaction between emotion and group, F(1,48) = 5.16; p = .028; ηp2 = .09.
To follow up the interaction between emotion and group, independent samples t tests were conducted. These indicated that the two groups exhibited comparable zygomaticus activity in response to facial stimuli depicting anger, t(48) = 0.86; p = .394, but that zygomaticus muscle activity was lower in the schizophrenia group when viewing facial stimuli depicting happiness, t(48) = 2.07; p = .044. Within-subject comparisons also indicated that there was a trend for zygomaticus activity in response to happy (relative to angry) facial expressions to be increased in the control group (p = .069). However, this was not the case for the schizophrenia group (p = .224), for whom the pattern of responding was in the opposite direction to that which would be congruent with a mimicry response [i.e., it can be seen in Figure 1 that there was a trend for greater cheek activity to angry (relative to happy) facial expressions]. The main effect of time was not followed up formally, but indicated that there was increased zygomaticus activity as a function of time.
For the corrugator region, there was no main effect of emotion, F(1,48) = 1.93; p = .171; ηp2 = .03, or of group, F(1,48) = 0.84; p = .365; ηp2 = .01. There was also no interaction between emotion and time, F(9,432) = 1.133; p = .338; ηp2 = .02, nor time and group, F(9,432) = .685; p = .723; ηp2 = .01, and no three-way interaction between emotion, time and group, F(9,432) = 1.58; p = .119; ηp2 = .03. However, there was a main effect of time, F(9,432) = 6.54; p < .001; ηp2 = .12, and again, most importantly, an interaction between emotion and group, F(1,48) = 4.54; p = .038; ηp2 = .09. The main effect of time was again not followed up formally, but indicated that over time there was a general trend for corrugator muscle activity to decrease.
Independent samples t tests to follow up the interaction between emotion and group indicated that the two groups exhibited comparable corrugator activity in response to facial stimuli depicting happiness, t(48) = 0.63; p = .533, but that corrugator muscle activity was lower in the schizophrenia group when viewing facial stimuli depicting anger, t(48) = 2.19; p = .034. Within-subject comparisons also indicated that the control group exhibited greater corrugator activity in response to angry (relative to happy) facial expressions (p = .043); however, this was not the case for the schizophrenia participants (p = .521).
Correlates of Facial Mimicry Response
The final analyses focused on investigating the correlates of zygomaticus muscle activity to happy facial stimuli, and corrugator muscle activity to angry facial stimuli (i.e., patterns of facial responding consistent with intact happy and angry mimicry responses, respectively). Results are reported in Table 2. In both groups, neither type of facial muscle activity was related to current or premorbid intelligence, or to negative affect (all ps > .05). Furthermore, facial muscle activity was not related to any clinical characteristics in the schizophrenia group as indexed by the SANS and the SAPS, duration of illness and chlorpromazine equivalents (all ps > .05).
Pearson correlations between zygomaticus activity to happy facial stimuli and corrugator facial muscle activity to angry facial stimuli with measures of cognitive function, negative affect, and psychopathology.
Note
Additional partial correlations (controlling for medication) revealed no associations between pattern of responding and key clinical variables (SAPS, SANS, blunted affect, duration of illness; ps > 0.5). WASI refers to Wechsler Abbreviated Scale of Intelligence; NART refers to National Adult Reading Test; DASS-21 refers to the Depression Anxiety Stress Scales; SAPS refers to the Scale for the Assessment of Positive Symptoms; SANS refers to the Scale for the Assessment of Negative Symptoms; CPZ refers to chlorpromazine.
DISCUSSION
The nonclinical control group displayed a distinct pattern of EMG responding consistent with a typical “mimicry” response (i.e., greater zygomaticus activity in response to happy faces relative to angry, and greater corrugator activity to angry faces relative to happy). That is, the mere perception of an emotional facial expression led control participants to rapidly and involuntarily produce a corresponding facial reaction within one second of stimulus exposure. It should be noted that the pattern of controls’ corrugator activity in response to angry facial expressions was not an absolute increase in relation to the prestimulus (baseline) levels. A comparable pattern of facial EMG activity, however, has been observed in other studies examining this rapid facial mimicry response and has been attributed to preparatory activity of the brow (Dimberg, Hansson, & Thunberg, Reference Dimberg, Hansson and Thunberg1998; Dimberg et al., Reference Dimberg, Thunberg and Elmehed2000). The critical finding was that corrugator activity was greater to angry facial expressions than happy facial expressions in nonclinical controls, psychophysiologically constituting a facial mimicry response (Dimberg et al., Reference Dimberg, Thunberg and Elmehed2000). These findings are therefore consistent with considerable prior research demonstrating that emotional facial expressions are sufficient to elicit the most rapid of facial mimicry reactions (Bailey et al., Reference Bailey, Henry and Nangle2009; Dimberg et al., Reference Dimberg, Thunberg and Elmehed2000, Reference Dimberg, Thunberg and Grunedal2002; McIntosh et al., Reference McIntosh, Reichmann-Decker, Winkielman and Wilbarger2006).
However, because impairments in empathic responding are well documented in schizophrenia (Derntl et al., Reference Derntl, Finkelmeyer, Toygar, Hulsmann, Schneider and Falkenberg2009; Shamay-Tsoory et al., Reference Shamay-Tsoory, Shur, Harari and Levkovitz2007), and have been argued to reflect structural abnormalities in the human MNS (Bertrand et al., Reference Bertrand, Achim, Harvey, Sutton, Malla and Lepage2008), it was predicted that this group would exhibit a disruption in this empathy-related rapid facial mimicry response. Consistent with predictions, the schizophrenia group failed to produce involuntary facial reactions congruent with observed emotional facial expressions. These group differences could not be attributed to demographic factors, as the two groups were equated in age, years of education, gender, as well as premorbid and current intellectual abilities. Furthermore, the failure to identify any association between facial muscle activity and clinical or cognitive parameters suggests that the absence of a typical rapid facial mimicry response is not secondary to specific clinical features of the disorder. However, this does not preclude a specific association between social functioning and facial muscle activity. This is particularly salient following research noting that clinical symptoms and general cognition cannot wholly account for the variance in social functioning in schizophrenia (Milev, Ho, Arndt, & Andreassen, Reference Milev, Ho, Arndt and Andreassen2005; Pijnenborg et al., Reference Pijnenborg, Withaar, Evans, van den Bosch, Timmerman and Brouwer2009). Future research is needed to ascertain whether rapid facial movements relate to social functioning in this group. It should also be noted that the size of the schizophrenia sample was comparable to, or larger than, all previous EMG studies that have been conducted with this group (Median n = 17.5; Kring et al., Reference Kring, Kerr and Earnst1999; Mattes et al., Reference Mattes, Schneider, Heimann and Birbaumer1995; Wolf et al., Reference Wolf, Mass, Kiefer, Eckert, Weinhold and Wiedemann2004, Reference Wolf, Mass, Kiefer, Wiedemann and Naber2006).
The group differences also cannot be easily attributed to attentional or motivational factors. This is because rapid facial mimicry responses are involuntary, preconscious reactions, with their elicitation only requiring the mere observance of an emotional facial expression. Indeed, Dimberg et al. (Reference Dimberg, Thunberg and Grunedal2002) demonstrated that, even when explicitly instructed to inhibit facial muscle activity, participants still involuntarily produced rapid facial mimicry reactions. As the current study involved examination of videotaped recordings to ensure participants were watching the presented facial expressions, it is unlikely that clinical participants would have been able to consciously or unconsciously inhibit the evocation of these reactions as a result of diminished motivation.
Moreover, the group differences in early, rapid facial responding in the current study seem unlikely to reflect medication effects. First, as noted, no baseline differences in facial EMG activity were observed between the schizophrenia and control groups. This suggests that medication was not having any impact on prestimulus facial muscle tension. Second, no group differences were observed in the overall level of facial EMG activity in either the corrugator or zygomaticus muscle regions during stimulus exposure. This indicates that it was only the pattern of responding that differed between the two groups—not their overall reactivity. Third, no associations were found between chlorpromazine equivalents and facial muscle activity, nor were any associations identified between key clinical variables and facial responding after controlling for medication level. Finally, although Kring et al. (Reference Kring, Kerr and Earnst1999) examined facial EMG responding over a longer timeframe, no differences in EMG activity among individuals with schizophrenia receiving neuroleptic medication and those not taking medication were identified.
Involuntary facial mimicry has been implicated in, and thought to facilitate, empathy via processes of simulation and perception-action coupling subserved by the MNS (Gallese, Reference Gallese2001; Oberman & Ramachandran, Reference Oberman and Ramachandran2007; Preston & deWaal, Reference Preston and de Waal2002). Thus, involuntary facial mimicry has been regarded as an important low-level mechanism contributing to the experience of empathy (for a review, see Singer & Lamm, Reference Singer and Lamm2009). Consistent with this assumption, Sonnby-Borgstrom, Jonsoon, and Svensson (Reference Sonnby-Borgstrom, Jonsoon and Svensson2003) found that nonclinical volunteers psychometrically identified as being high in empathy produce more rapid, involuntary mimicry reactions compared with low-empathic individuals. Furthermore, atypical rapid facial mimicry reactions have been identified in autism spectrum disorders, a group also characterized by marked empathizing deficits and abnormal MNS activity (Beall, Moody, McIntosh, Hepburn, & Reed, Reference Beall, Moody, McIntosh, Hepburn and Reed2008; Cattaneo et al., Reference Cattaneo, Fabbri-Destro, Boria, Pieraccini, Monti and Cossu2007; Dapretto et al., Reference Dapretto, Davies, Pfeifer, Scott, Sigman and Bookheimer2006; Iacoboni & Dapretto, Reference Iacoboni and Dapretto2006; McIntosh et al., Reference McIntosh, Reichmann-Decker, Winkielman and Wilbarger2006; Oberman, Winkielman, & Ramachandran, Reference Oberman, Winkielman and Ramachandran2009). Having now also demonstrated a disruption in the elicitation of rapid facial mimicry reactions in schizophrenia, the current study points to a need for further research that directly maps how aberrant facial mimicry responses in this group relates to other lower- and higher-level empathic processes.
An important caveat, however, is that while rapid facial mimicry reactions have been linked to perception-action neural links mediated by the MNS (e.g., Niedenthal, Barsalou, Winkielman, Krauth-Gruber, & Ric, Reference Niedenthal, Barsalou, Winkielman, Krauth-Gruber and Ric2005; Williams, Whiten, Suddendorf, & Perrett, Reference Williams, Whiten, Suddendorf and Perrett2001), others have argued that such reactions might instead reflect an emotional response (e.g., Moody et al., Reference Moody, McIntosh, Mann and Weisser2007). This view stems from the finding that rapid facial reactions to affective stimuli can be modulated through emotion induction (Moody et al., Reference Moody, McIntosh, Mann and Weisser2007). Thus, although the present data have been interpreted within the context of potential human MNS abnormalities in schizophrenia, an important limitation of these data is the absence of specific information relating to the neurological profile of the schizophrenia participants tested. Further research incorporating neuroimaging techniques, such as fMRI, is therefore required to delineate the precise mechanisms underlying this empathy-related rapid facial response. At present, it is not clear whether an impaired involuntary mimicry response in schizophrenia (or autism) is due solely to a disrupted perception-action neural link or early emotional processing deficits (or a contribution of each). Future research should also incorporate emotional nonfacial stimuli to clarify whether an atypical involuntary mimicry response in schizophrenia reflects a face-specific processing deficit in this group (at a visual scanning or neural level) or a more general motor mimetic impairment. For example, in a voluntary imitation paradigm, Park, Matthews, and Gibson (Reference Park, Matthews and Gibson2008) found that individuals with schizophrenia demonstrated a range of impairments in motor imitation ability, from hand actions to voluntary imitation of emotional facial expressions.
To conclude, the present study provides the first evidence that individuals with schizophrenia demonstrate an atypical rapid facial mimicry response. Given that rapid facial mimicry has been conceptualized as an important mechanism in the experience of empathy, the current findings map onto the broader schizophrenia literature which has documented impairment in empathic behaviors, and more recently, abnormalities in the MNS. At present, the neural mechanisms and component processes that underlie the pervasive empathic and social cognitive deficits seen in schizophrenia remain poorly understood (Pinkham, Hopfinger, Pelphrey, Piven, & Penn, Reference Pinkham, Hopfinger, Pelphrey, Piven and Penn2008). These data highlight abnormalities in rapid facial mimicry responses, and their neural underpinnings, as one potential area that warrants further consideration.
ACKNOWLEDGMENTS
This research was supported by an Australian Research Council Discovery Grant. The authors acknowledge the Schizophrenia Research Institute for assisting with the recruitment of the volunteers participating in this research, as well as the participants themselves.
