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Deficits of subliminal self-face processing in schizophrenia
Consciousness and Cognition 79 (2020) 102896
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Deficits of subliminal self-face processing in schizophrenia Song Zhoua,1, Yuanyuan Xub,c,1, Nanbo Wanga, Shen Zhangd, Haiyan Genga, , ⁎ Hongxiao Jiab,c, ⁎
T
a
School of Psychological and Cognitive Sciences, Beijing Key Laboratory of Behavior and Mental Health, Peking University, Beijing, China The National Clinical Research Center for Mental Disorders & Beijing Key Laboratory of Mental Disorders, Beijing Anding Hospital, Capital Medical University, Beijing, China c Advanced Innovation Center for Human Brain Protection, Capital Medical University, Beijing, China d Department of Psychology, University of Wisconsin-Whitewater, Whitewater, WI, USA b
ARTICLE INFO
ABSTRACT
Keywords: Schizophrenia Face processing Self-face advantage Interocular suppression Subliminal
Most studies show that self-processing in schizophrenia is impaired at the supraliminal level. Schizophrenic patients generally lack the ability to prioritize the processing of self-related information, such as their own face. However, some evidence suggests that schizophrenic patients may retain intact subliminal processing abilities even though their conscious experiences are compromised. We conducted the first study exploring schizophrenic patients’ subliminal self-face processing. Using a breaking continuous flash suppression (bCFS) paradigm, we interocularly suppressed face images (self, famous, and unknown faces). Participants’ reaction times to detect the faces when they broke the suppression were recorded as an index for the subliminal processing of faces. Unlike the healthy controls, schizophrenic patients did not demonstrate a processing advantage for their own face when it broke interocular suppression; only a face familiarity effect was found. These findings contribute to the understanding of self-processing deficits in schizophrenia.
1. Introduction As a complex psychotic disorder, schizophrenia involves various symptoms, such as delusions, hallucinations, and cognitive impairments, which often cause patients to have difficulty functioning in their daily lives (Bellani & Brambilla, 2008; Berkovitch, Dehaene, & Gaillard, 2017; Oshima, Ito, Yagihashi, & Okagami, 1994). From a phenomenological view in psychopathology, these severe impairments are attributed to “self-disturbance”, which is the clinical core of the phenotypic traits of schizophrenia that refers to an unstable or distorted basic sense of self, as people with schizophrenia may have a diminished ownership of their experiences and disturbed self-other/self-world boundaries (Nelson et al., 2014a, 2014b). The underlying mechanism is that altered/aberrant neural activities in the brain, e.g., spatiotemporal changes in the brain’s spontaneous activity, may affect an individual’s ability to correctly distinguish between stimuli that should be labeled as originating from himself/herself and external stimuli from the environment at the experiential level (Northoff & Duncan, 2016; Northoff, 2014). An embodiment of the basic sense of self is one’s ability to recognize his/her own face (Kircher, Seiferth, Plewnia, Baar, & ⁎ Corresponding authors at: School of Psychological and Cognitive Sciences, Peking University, 5 Yiheyuan Road, Beijing 100871, China (H. Geng). Beijing Anding Hospital, Capital Medical University, Room 102, Xingzheng Building, 5th Ankanghutong, Deshengmenwai Street, Xicheng District, Beijing 100088, China (H. Jia). E-mail addresses: [email protected] (H. Geng), [email protected] (H. Jia). 1 These authors have contributed equally to this work and should be considered co-first authors.
https://doi.org/10.1016/j.concog.2020.102896 Received 10 July 2019; Received in revised form 21 December 2019; Accepted 1 February 2020 1053-8100/ © 2020 Elsevier Inc. All rights reserved.
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Schwabe, 2007). Normal individuals exhibit superior performance in recognizing self-related information, e.g., their own face, compared to other-related information, e.g., another person’s face because the “self” is such an important mediating construct in much of human social interactions and personalities (Anderson, 1984) that the perception, comprehension, and interpretation of various items as self-related benefit from advantages in cognitive processing (Brédart, Delchambre, & Laureys, 2006; Keenan, Freund, Hamilton, Ganis, & Pascual-Leone, 2000; Moray, 1959; Symons & Johnson, 1997; Tong & Nakayama, 1999; Yang, Wang, Gu, Gao, & Zhao, 2013). In some studies, people responded significantly faster and more accurately to the presentation of their self-face when judging the ownership of different faces (2010; Keenan et al., 1999; Ma & Han, 2009). Since the experiment tasks require participants to explicitly reference the attributes of stimuli (such as personality traits or faces) and relate them to the self, these studies are believed to examine self-referential processing (Northoff et al., 2006, 2016). Some studies, in contrast, examine self-related processing (Northoff et al., 2016, 2007, 2011). Instead of requiring explicit referencing between themselves and the stimuli, these studies asked participants to perform other cognitive tasks that were irrelevant to the self (such as discriminating orientations of the self-face and familiar faces, Ma & Han, 2009, 2010), during which a processing advantage is observed for self-related stimuli (e.g., the selfface). For people with schizophrenia, however, the literature has not been consistent regarding the advantage of processing one’s own face. Self-face processing itself can be either self-referential or self-related. In most self-referential studies involving judging the identity of different faces (e.g., Irani et al., 2006; Kircher et al., 2007) or deciding whether a morphed face was their own face (e.g., Heinisch, Wiens, Gründl, Juckel, & Brüne, 2013; Jia, Yang, Zhu, Liu, & Barnaby, 2015), schizophrenic patients showed an absence of the abovementioned advantage, demonstrating slower reaction times or no reaction time differences when identifying their own face vs. a familiar person’s face and/or lower accuracy when identifying their own face. Nevertheless, in studies examining self-related processing (e.g., when participants were asked to detect changes in rapidly presented unknown, self, or familiar faces), patients seemed to perform significantly better when the stimulus was related to the self-face (Kochs, Köhler, Merz, & Sterzer, 2017). Many factors, such as task type and demand, are thought to contribute to the mixed findings (Bortolon, Capdevielle, Salesse, & Raffard, 2016; Kochs et al., 2017). One factor that has not been examined is the level of awareness. The abovementioned studies, regardless of explicit self-referential or implicit self-related processing, all presented the stimuli above the awareness threshold. Given different lines of research showing that schizophrenic patients have intact subliminal processing of emotional faces (Kring, Siegel, & Barrett, 2014) and upright/inverted faces (Caruana, Stein, Watson, Williams, & Seymour, 2019) as well as eye gazes (Seymour, Rhodes, Stein, & Langdon, 2016), while supraliminal processing of similar facial stimuli is likely hampered (Hall et al., 2004; Marwick & Hall, 2008; Whittaker, Deakin, & Tomenson, 2001), it is possible that a similar dissociation exists in self-face processing in schizophrenic patients. Therefore, it is necessary to examine schizophrenic patients’ processing of their own face at the subliminal level. In particular, would schizophrenic patients have an advantage in processing their self-face compared to another’s face when the faces are presented subliminally? To address this question, we adopted the breaking continuous flash suppression (bCFS; Jiang, Costello, & He, 2007) paradigm, which has recently seen increased use in the investigation of unconscious processing (Gayet & Stein, 2017; Stein, Hebart, & Sterzer, 2011; Stein, Siebold, & van Zoest, 2016). In this paradigm, a face image is presented to participants’ nondominant eye with increasing contrast, while a dynamic set of noise images is presented to his/her dominant eye; this combination formulates interocular suppression and, consequently, results in a conscious perception of noise images, with the face image initially being invisible. However, as the contrast of the face image gradually increases, it will finally break the suppression to enter awareness and be recognized. This paradigm can stably block a visual stimulus from consciousness (i.e., being invisible) for a considerable amount of time until it is sufficiently processed to break into awareness (Jiang et al., 2007; but see Gayet, Van der Stigchel, & Paffen, 2014, which questions the awareness level during suppression). Since stimuli that have an advantage in subliminal processing would break interocular suppression faster than those without an advantage, the time needed for a face to break into awareness is taken as the measure of participants’ subliminal processing of that face (Jiang et al., 2007; Seymour et al., 2016; Tsuchiya, Moradi, Felsen, Yamazaki, & Adolphs, 2009). Therefore, observing possible time differences between the self- and other faces to break interocular suppression allows us to compare the processing of different faces. The face stimuli we used were participants’ own faces, a famous person's face and an unknown face from a stranger. To rule out possible alterative explanations for any results we might find, such as participants’ different criteria for detection or response speeds associated with different types of physical face stimuli, a control condition was included in the study, in which participants binocularly viewed the same stimuli as in the experimental condition but without interocular rivalry (Gayet, Paffen, Belopolsky, Theeuwes, & Van der Stigchel, 2016; Jiang et al., 2007). We also included healthy participants for comparison. If an advantage exists for the subliminal processing of the participants’ self-face, self-face stimuli would break the suppression faster than the famous face. Otherwise, if the self-face processing advantage is absent at the subliminal level, we predicted that no significant differences would be observed in the reaction times between the self-face and the famous face stimuli. 2. Methods 2.1. Participants The sample size of our study was determined via a priori power analysis using G*Power 3 (Faul, Erdfelder, Buchner, & Lang, 2009). With a power of 0.90, an alpha level of 0.05, and an estimated large effect size (partial η2 = 0.14) in subliminal self-processing (Geng, Zhang, Li, Tao, & Xu, 2012), the power analysis yielded an estimated sample size of 32 for the healthy controls (we assumed a similar sample size would be needed for patients). We terminated participant recruitment when the targeted number of eligible 2
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Table 1 Participants’ demographic and clinical characteristics. Patients (N = 35)
Age (years) Gender (M/F) Illness duration (years) CED (mg/day) PANSS total score Positive symptoms Negative symptoms General psychopathology
Control (N = 33)
Mean
SE
Mean
SE
23.26 14/21 4.21 591.2 63.71 14.37 18.97 30.37
± 0.95
24.67 12/21
± 0.51
± 0.69 ± 40.39 ± 1.35 ± 0.66 ± 0.80 ± 0.63
Note: M: male; F: female; CED: Chlorpromazine Equivalents Dose; PANSS: Positive and Negative Symptoms Scale; SE: standard error.
participants was achieved and finished data collection with the participants already scheduled. Our final sample included 35 schizophrenic patients and 33 healthy controls who were included in the data analysis. Schizophrenic patients were recruited from Beijing Anding Hospital and Capital Medical University, where they were being treated. The patients ranged in age from 16 to 60 years old. All of the patients met the criteria for schizophrenia in the Diagnostic and Statistical Manual of Mental Disorders, Fifth Edition (DSM-V, American Psychiatric Association, 2013) and were being medicated with antipsychotics at the time of the study. Substance abuse, comorbid neurological disorders, history of severe brain trauma or current use of electroconvulsive therapy were used as criteria to exclude ineligible participants. In addition, no participants experienced acute symptom exacerbations in the experiment. Healthy controls were recruited from the Beijing area through advertisements and staff working at the hospital. The age, gender and education level of healthy controls were roughly matched with those of the schizophrenic patient group (see Table 1, t (66)age = 1.28, page = 0.204; X2gender = 84.095, pgender = 0.758). Individuals who met the criteria for any disorder in the DSM-V or who had any first-degree relative with schizophrenia were excluded. All participants had normal or corrected-to-normal vision and were able to recognize the former Chinese Prime Minister Wen Jiabao from a facial picture provided prior to their participation in the experiment. The demographic and clinical characteristics of the two groups are presented in Table 1. This study was approved by the Ethics Review Committees of the Beijing Anding Hospital and Capital Medical University as well as by Peking University. All participants gave written informed consent before the study and received a full explanation of the study after their participation. 2.2. Stimuli 2.2.1. Face images The stimuli used in the current study were created in a manner similar to that used in our previous study (Geng et al., 2012). The self-face stimulus was a photograph of each participant’s own face taken by a research assistant in the lab with a digital camera prior to the experiment. The famous face stimulus was a photo of the former Chinese Prime Minister Wen Jiabao, who was highly familiar to the participants. The unknown face stimulus was a photograph of someone who the participants had never met. All face pictures were front-view shots with neutral facial expressions. In addition, a scrambled face was used in the catch trials (randomly scrambled into 169 blocks of 20 × 20 pixels, see Fig. 3), which was completely unrecognizable as any part of a face. All pictures were processed in Adobe Photoshop 5.0 to create standardized stimuli. Specifically, each image was modified to retain only the facial part between the forehead and chin, with the nose located at the center of the picture and the pupil to pupil distance equalized across pictures. Then, each modified image was resized to 256 × 256 pixels (5.51 × 5.51 visual angle) and matched on brightness (luminance = 3.7 cd/mm2) and contrast (root-mean-square contrast = 0.51). Final low-contrast blue face images were produced by removing the red and green color channels of these images, and these images were presented against a gray background (128, 128, 128 RGB). 2.2.2. Noise images Noise images that matched the size of the face images were created with OpenGL 2.0 (Silicon Graphics International Corp., Fremont, California, US), and these images were presented successively in sets during each trial of the experiment. In such a dynamic noise image set, each image consisted of differently mixed red and green squares of various sizes, and in each successive noise image, 10% of the area of the previous picture was replaced by new squares at random locations. The face and noise images were overlapped with each other at the center of the computer screen and were surrounded by a whiteblack frame (see Fig. 1). The noise images were always presented at full contrast, whereas the contrast of the face images was gradually increased in each trial.
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Fig. 1. Illustration of a critical trial in the experimental condition.
Fig. 2. Log-transformed reaction times of the self-face, famous face, and unknown face for schizophrenic participants and healthy controls, shown separately for the experimental and control conditions. *p < .05.
Fig. 3. The scrambled face used in the catch trials.
2.3. Procedure Our study used a 3 (Face: self vs. famous vs. unknown) × 2 (Group: schizophrenic patients vs. healthy controls) mixed factorial design for both the experimental and control conditions. 4
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The procedure used in this experiment was very similar to that of Geng et al. (2012). Participants attended the study individually, and a chin rest was used to maintain a viewing distance of 60 cm from the computer screen. After providing informed consent, the participants began the experiment with practice trials so that they could become familiar with the task. Then, participants completed two blocks of trials in random order, one for the experimental condition and the other for the control condition. In the experimental block, participants wore a pair of red-blue anaglyph glasses so that the noise images were only visible to their dominant eye through the red filter lens, and simultaneously, the face image was only visible to their other eye through the blue filter lens (see Fig. 1). The resulting interocular suppression consequently allowed participants to see continuous presentations of the noise images, but they were not aware of the existence of the face image until it broke into awareness. The set of noise images was presented at a rate of 100 Hz, which is believed to produce robust interocular suppression (Xu, Zhang, & Geng, 2011) compared to the common 10 Hz rate presentation (Tsuchiya & Koch, 2005). In the control block, instead of wearing the anaglyph glasses, participants were binocularly presented the face and noise stimuli without suppression. As a result, the face image coalesced with the dynamic noise pattern initially, but its contrast gradually increased. Meanwhile, the participants’ visual experiences mimicked those in the experimental condition, with the perception that the face image gradually emerged from the noise background at a certain time point. A total of 55 trials were included in each block, with 45 critical trials presenting face stimuli: self, famous, and unknown faces (15 trials for each face). The remaining 10 trials with scrambled faces were catch trials that were used to detect false alarms (i.e., when participants reported seeing a face or a facial part that was not actually present). If three or more false alarms occurred within a block, that block would restart. No participant exceeded this limit. Each critical trial began with the binocular presentation of a fixation cross, which flashed for 2000 ms to draw participants’ attention. Then, a set of noise images was presented to the dominant eye at full contrast, and at the same time, a face image was presented for 1000 ms to the nondominant eye of the participant with its contrast gradually increased from 0% to 100% (programmed by manipulating the alpha channel value of the pictures to change from 0 to 1). After reaching full contrast, the face image remained constant until the end of the trial. Given that the binocular presentation of stimuli in the control condition may make the task easier, the increase in the contrast of face images in that block was modified to be 4000 ms to match the difficulty level of the task to that in the experimental block. Participants were instructed to press the space bar as quickly as possible upon the appearance of the face image or any part of it. The face and noise images remained on the screen until a response was made or 10 s had elapsed. Participants’ reaction times were recorded as the time required for the face image to break interocular suppression. Trials with no response or with extreme reaction times (more than 3 standard deviations from the mean) were not included in the analysis (less than 5% of the total trials). 3. Results We performed log-transformation (log10) on each participant’s reaction times to account for the positively skewed distribution of the data (Caruana et al., 2019; Gayet & Stein, 2017; Heyman & Moors, 2014). Log-transformed reaction times in the experimental condition were subjected to a 3 × 2 repeated-measures ANOVA, with Face (self vs. famous vs. unknown) as a within-participants factor and Group (schizophrenic patients vs. healthy controls) as a betweenparticipants factor. Sidak correction was applied to all post hoc pairwise comparisons reported in this paper. The results revealed a significant main effect of Face, F(2, 65) = 14.238, p < .001, ηp2 = 0.305. In general, participants’ detection times to the self-face (M = 0.197 s, SEM = 0.017) and the famous face (M = 0.21 s, SEM = 0.016) were similar, t(65) = 1.625, p = .287, d = 0.197, but significantly faster than the detection of the unknown face (M = 0.237 s, SEM = 0.017), t self vs. unknown (65) = 5.125, p < .001, d = 0.621, t famous vs. unknown (65) = 3.857, p = .002, d = 0.468 (see Fig. 2). The main effect of Group was also significant, F(1, 66) = 0.547, p < .001, ηp2 = 0.286. The healthy controls (M = 0.132 s, SEM = 0.023) responded significantly faster than the patients (M = 0.298 s, SEM = 0.023). These main effects were qualified by a significant Face × Group interaction, F(2, 65) = 3.335, p = .042, ηp2 = 0.093. For the healthy participants, the self-face (M = 0.101 s, SEM = 0.017) was detected faster than the famous face (M = 0.132 s, SEM = 0.015), t(32) = 2.583, p = .031, d = 0.45, and the famous face was detected faster than the unknown face (M = 0.161 s, SEM = 0.017), t(32) = 2.636, p = .026, d = 0.459. However, for the schizophrenic patients, the only significant difference was the faster detection time of the famous face (M = 0.288 s, SEM = 0.029) than the unknown face (M = 0.314 s, SEM = 0.029), t(35) = 2.6, p = .048, d = 0.439. The detection time of the self-face (M = 0.292 s, SEM = 0.028) and other faces were not significantly different, t self vs. famous (35) = 0.364, p = .977, d = 0.061, t self vs. unknown (35) = 1.909, p = .161, d = 0.323. The same 3 × 2 ANOVA was conducted on the log-transformed reaction times in the control condition. The main effect of Face was significant, F(2, 65) = 26.556, p < .001, ηp2 = 0.45. Participants had similar detection times for the self-face (M = 0.159 s, SEM = 0.017) and the famous face (M = 0.159 s, SEM = 0.018), t(65) = 0, p = 1, d = 0, but both of these times were faster than their detection time for the unknown face (M = 0.214 s, SEM = 0.018), t self vs. unknown (65) = 5.5, p < .001, d = 0.667, t famous vs. unknown (65) = 6.875, p < .001, d = 0.833 (see Fig. 2). The main effect of Group was also significant, F(1, 66) = 16.820, p < .001, ηp2 = 0.203, with faster detection of the faces in the healthy group (M = 0.107 s, SEM = 0.025) than in the schizophrenia group (M = 0.247 s, SEM = 0.024). However, the interaction between Face and Group was not significant, F(2, 65) = 0.286, p = .752, ηp2 = 0.009. 4. Discussion Although ample evidence has demonstrated the advantage of processing one’s own face in healthy individuals (2010; Keenan et al., 1999; Ma & Han, 2009), most studies have suggested a lack of the self-advantage effect in schizophrenic patients when 5
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identifying their own faces compared to a familiar face (e.g., Bortolon et al., 2016; Irani et al., 2006) when these studies were carried out above the conscious level of the participants. Given that dissociation of supraliminal and subliminal cognitive processing often exists (e.g., Geng et al., 2012) and that evidence indicates different performance for schizophrenic patients at different levels of awareness (see Berkovitch et al., 2017 for a review), we incorporated a bCFS paradigm in a commonly used face detection task to examine whether the subliminal processing of the self-face remains intact in schizophrenic patients (i.e., demonstrating a self-face advantage). Although the self-face processing advantage involves comparing the self-face and another face, if the other face is a stranger’s face, it is unclear whether any findings reflect a face familiarity effect or the uniqueness of the self-face, as the self-face is also more familiar than the unknown face (Qin et al., 2012). Therefore, by including a famous/familiar face condition, we can control for familiarity, and then a comparison of the processing of the self-face with that of a familiar face can determine whether a self-face advantage exists in subliminal face processing. Additionally, by comparing participants’ processing of the famous face with that of the unknown face, we assessed the existence of subliminal familiarity effects. Our findings revealed a subliminal self-face advantage in the healthy controls, as they showed significantly faster reaction times for the self-face than for the famous face in the experimental condition. However, such a self-face processing advantage was not found in the schizophrenic patients. The speed of detecting the self-face for schizophrenic patients was comparable to that of the famous face. Given that the famous face entered awareness faster than the unknown face (the familiarity effect), which means that participants did process the face stimuli, the absence of the advantage for the self-face over the famous face probably suggests impaired subliminal self-face processing in schizophrenic patients. This finding is surprising and interesting because in other CFS studies with different stimuli, such as gazes, upright/inverted faces or emotional faces, schizophrenic patients showed intact unconscious processing at the subliminal level (Caruana et al., 2019; Kring et al., 2014; Seymour et al., 2016). In fact, to date, research tends to find defective supraliminal cognitive processing in schizophrenic patients, such as visual perception, metacognition, or self-monitoring, but preserved automatic processing, which relies less on consciousness (Berkovitch et al., 2017; Kochs et al., 2017). Nevertheless, schizophrenic patients in our study seemed to have compromised performance when detecting their own faces below the awareness threshold. Since past research showing intact subliminal processing among schizophrenic patients mostly used tasks irrelevant to the self, we speculate that unlike general cognitive abilities, self-face processing is impaired among schizophrenic patients because it is self-related. Given that the existing neural evidence on sense of self is largely based on supraliminal self-processing, future research should explore the representation of subliminal self-processing in the brains of healthy people as well as in schizophrenic patients. Meanwhile, for both the schizophrenic patients and the healthy controls, the famous face broke suppression significantly faster than the unknown face both in the experimental condition and in the control condition. In other words, these results demonstrate a familiarity effect. This effect exists in subliminal face processing in schizophrenic patients, as well as in healthy people, in accordance with the supraliminal results of previous research (Heinisch et al., 2013; Kochs et al., 2017; Yun et al., 2014). Given that evidence exists showing that schizophrenic patients are able to subliminally process other facial information (Caruana et al., 2019; Kring et al., 2014; Seymour et al., 2016), the face familiarity effects found in our study enrich our understanding of schizophrenic patients’ capacities at the subliminal level. Why did schizophrenic patients fail to exhibit a self-face advantage but did experience an intact familiarity effect? This result may have occurred because the perceptional encoding of a face remains unimpaired, but the patients have difficulty associating the face with its identity. In addition, having a relatively short illness duration (4 years on average) may contribute to an intact familiarity effect in patients (Bortolon, Capdevielle, & Raffard, 2015), even subliminally. At the neural level, self-specific processing and face familiarity processing are believed to be associated with distinct networks (Keenan, Wheeler, Gallup, and Pascual-Leone, 2000; Zhang, Zhu, Xu, Jia, & Liu, 2012). Compared to unknown faces, familiar faces selectively activate brain regions such as the bilateral temporoparietal lobe, medial prefrontal cortex and precuneus (Sugiura et al., 2008; Taylor et al., 2009; Uddin, Kaplan, MolnarSzakacs, Zaidel, & Iacoboni, 2005). However, compared to familiar faces, self-face processing further activates regions such as the superior, middle, and inferior frontal gyri, as well as the inferior parietal lobe in the right hemisphere, along with bilateral ventral occipitotemporal regions (Decety & Chaminade, 2003; Platek & Kemp, 2009; Platek et al., 2004, 2006; Sugiura et al., 2008; Uddin et al., 2005). This separation between the neural mechanisms of the self and familiarity processing makes it possible that selfprocessing could be damaged, but familiarity processing could remain intact. In the current design, we included a control condition that presented the same face stimuli to create similar subject experiences as in the experimental condition, except that the control condition did not involve interocular suppression. Since there were no significant reaction time differences when responding to the self-face vs. the famous face in this control condition (for both schizophrenic patients and healthy controls), we can rule out the possibility that the findings in the experimental condition were simply due to the physical characteristics of the face stimuli (Gayet et al., 2016). We recognize that there are some debates on whether bCFS is an ideal paradigm for examining unconscious processing (e.g., completely blocking awareness regardless of stimuli characteristics and postperceptual factors in participants’ responses). In addition, some may argue that the catch trials used in our study created postperceptual confounds as they may incentivize participants to delay their reaction. However, given that we found significantly different reaction times between the self-face and familiar face in the experimental condition but not in the control condition for healthy people, such results tend to support our argument for selfprocessing rather than confounding factors such as postperceptual reactions. Still, the characteristics of patients’ subliminal selfprocessing should be further explored with other paradigms in the future. In conclusion, in the current study, we found that schizophrenic patients had impaired self-face processing at the subliminal level, but their processing of face familiarity was intact. These findings help further our understanding of self-related deficits in 6
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schizophrenia. Future studies should continue to investigate subliminal self-processing and related factors in healthy and schizophrenic populations. CRediT authorship contribution statement Song Zhou: Conceptualization, Methodology, Software, Investigation, Data curation, Formal analysis, Writing - original draft. Yuanyuan Xu: Conceptualization, Methodology, Software, Investigation, Data curation, Formal analysis, Writing - original draft. Nanbo Wang: Conceptualization, Methodology, Formal analysis, Writing - original draft, Writing - review & editing, Visualization. Shen Zhang: Conceptualization, Methodology, Formal analysis, Writing - original draft, Writing - review & editing. Haiyan Geng: Conceptualization, Methodology, Validation, Formal analysis, Writing - original draft, Writing - review & editing, Resources, Supervision, Project administration, Funding acquisition. Hongxiao Jia: Conceptualization, Methodology, Validation, Formal analysis, Writing - original draft, Resources, Supervision, Project administration, Funding acquisition. Declaration of Competing Interest All authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgments This research was supported by grants from the National Natural Science Foundation of China to HG (31671131, 31271202 and 30870763) and HJ (81873398). Appendix A. Supplementary material Supplementary data to this article can be found online at https://doi.org/10.1016/j.concog.2020.102896. References Anderson, J. R. (1984). The development of self-recognition: A review. Developmental Psychobiology: The Journal of the International Society for Developmental Psychobiology, 17, 35–49. https://doi.org/10.1016/s0273-2297(84)80006-4. American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (DSM-5®). American Psychiatric Pub. Bellani, M., & Brambilla, P. (2008). The use and meaning of the continuous performance test in schizophrenia. Epidemiology and Psychiatric Sciences, 17(3), 188–191. https://doi.org/10.1017/s1121189x00001275. Berkovitch, L., Dehaene, S., & Gaillard, R. (2017). Disruption of conscious access in schizophrenia. Trends in Cognitive Sciences, 21(11), 878–892. https://doi.org/10. 1016/j.tics.2017.08.006. Bortolon, C., Capdevielle, D., & Raffard, S. (2015). Face recognition in schizophrenia disorder: A comprehensive review of behavioral, neuroimaging and neurophysiological studies. Neuroscience & Biobehavioral Reviews, 53, 79–107. https://doi.org/10.1016/j.neubiorev.2015.03.006. Bortolon, C., Capdevielle, D., Salesse, R. N., & Raffard, S. (2016). Further insight into self-face recognition in schizophrenia patients: Why ambiguity matters. Journal of Behavior Therapy and Experimental Psychiatry, 50, 215–222. https://doi.org/10.1016/j.jbtep.2015.09.006. Brédart, S., Delchambre, M., & Laureys, S. (2006). Short article one's own face is hard to ignore. Quarterly Journal of Experimental Psychology, 59(1), 46–52. https://doi. org/10.1080/17470210500343678. Caruana, N., Stein, T., Watson, T., Williams, N., & Seymour, K. (2019). Intact prioritisation of unconscious face processing in schizophrenia. Cognitive Neuropsychiatry, 24(2), 135–151. https://doi.org/10.1080/13546805.2019.1590189. Decety, J., & Chaminade, T. (2003). When the self represents the other: A new cognitive neuroscience view on psychological identification. Consciousness and Cognition, 12(4), 577–596. https://doi.org/10.1016/s1053-8100(03)00076-x. Faul, F., Erdfelder, E., Buchner, A., & Lang, A. G. (2009). Statistical power analyses using G* Power 3.1: Tests for correlation and regression analyses. Behavior Research Methods, 41(4), 1149–1160. https://doi.org/10.3758/BRM.41.4.1149. Gayet, S., Paffen, C. L., Belopolsky, A. V., Theeuwes, J., & Van der Stigchel, S. (2016). Visual input signaling threat gains preferential access to awareness in a breaking continuous flash suppression paradigm. Cognition, 149, 77–83. https://doi.org/10.1016/j.cognition.2016.01.009. Gayet, S., & Stein, T. (2017). Between-subject variability in the breaking continuous flash suppression paradigm: Potential causes, consequences, and solutions. Frontiers in Psychology, 8, 437. https://doi.org/10.3389/fpsyg.2017.00437. Gayet, S., Van der Stigchel, S., & Paffen, C. L. (2014). Breaking continuous flash suppression: Competing for consciousness on the pre-semantic battlefield. Frontiers in Psychology, 5, 460. https://doi.org/10.3389/fpsyg.2014.00460. Geng, H., Zhang, S., Li, Q., Tao, R., & Xu, S. (2012). Dissociations of subliminal and supraliminal self-face from other-face processing: Behavioral and ERP evidence. Neuropsychologia, 50(12), 2933–2942. https://doi.org/10.1016/j.neuropsychologia.2012.07.040. Hall, J., Harris, J. M., Sprengelmeyer, R., Sprengelmeyer, A., Young, A. W., Santos, I. M., ... Lawrie, S. M. (2004). Social cognition and face processing in schizophrenia. The British Journal of Psychiatry, 185(2), 169–170. https://doi.org/10.1192/bjp.185.2.169. Heinisch, C., Wiens, S., Gründl, M., Juckel, G., & Brüne, M. (2013). Self-face recognition in schizophrenia is related to insight. European Archives of Psychiatry and Clinical Neuroscience, 263(8), 655–662. https://doi.org/10.1016/s0920-9964(01)00310-3. Heyman, T., & Moors, P. (2014). Frequent words do not break continuous flash suppression differently from infrequent or nonexistent words: Implications for semantic processing of words in the absence of awareness. Plos One, 9(8), e104719. https://doi.org/10.1371/journal.pone.0104719. Irani, F., Platek, S. M., Panyavin, I. S., Calkins, M. E., Kohler, C., Siegel, S. J., ... Gur, R. C. (2006). Self-face recognition and theory of mind in patients with schizophrenia and first-degree relatives. Schizophrenia Research, 88(1–3), 151–160. https://doi.org/10.1016/j.schres.2006.07.016. Jia, H., Yang, J., Zhu, H., Liu, J., & Barnaby, N. (2015). Self-face recognition in the ultra-high risk for psychosis population. Early Intervention in Psychiatry, 9(2), 126–132. https://doi.org/10.1111/eip.12097. Jiang, Y., Costello, P., & He, S. (2007). Processing of invisible stimuli: Advantage of upright faces and recognizable words in overcoming interocular suppression. Psychological Science, 18(4), 349–355. https://doi.org/10.1111/j.1467-9280.2007.01902.x. Keenan, J. P., Freund, S., Hamilton, R. H., Ganis, G., & Pascual-Leone, A. (2000). Hand response differences in a self-face identification task. Neuropsychologia, 38(7), 1047–1053. https://doi.org/10.1016/s0028-3932(99)00145-1.
7
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S. Zhou, et al.
Keenan, J. P., McCutcheon, B., Freund, S., Gallup, G. G., Jr, Sanders, G., & Pascual-Leone, A. (1999). Left hand advantage in a self-face recognition task. Neuropsychologia, 37(12), 1421–1425. https://doi.org/10.1016/s0028-3932(99)00025-1. Keenan, J. P., Wheeler, M. A., Gallup, G. G., Jr, & Pascual-Leone, A. (2000). Self-recognition and the right prefrontal cortex. Trends in Cognitive Sciences, 4(9), 338–344. https://doi.org/10.1016/s1364-6613(00)01521-7. Kircher, T. T., Seiferth, N. Y., Plewnia, C., Baar, S., & Schwabe, R. (2007). Self-face recognition in schizophrenia. Schizophrenia Research, 94(1–3), 264–272. https://doi. org/10.1016/j.schres.2007.04.029. Kochs, A., Köhler, S., Merz, H., & Sterzer, P. (2017). Effects of self and familiarity on change detection in patients with schizophrenia. Psychiatry Research, 248, 140–146. https://doi.org/10.1016/j.psychres.2016.12.030. Kring, A. M., Siegel, E. H., & Barrett, L. F. (2014). Unseen affective faces influence person perception judgments in schizophrenia. Clinical Psychological Science, 2(4), 443–454. https://doi.org/10.1177/2167702614536161. Ma, Y., & Han, S. (2009). Self-face advantage is modulated by social threat–Boss effect on self-face recognition. Journal of Experimental Social Psychology, 45(4), 1048–1051. https://doi.org/10.1016/j.jesp.2009.05.008. Ma, Y., & Han, S. (2010). Why we respond faster to the self than to others? An implicit positive association theory of self-advantage during implicit face recognition. Journal of Experimental Psychology: Human Perception and Performance, 36(3), 619. https://doi.org/10.1037/a0015797. Marwick, K., & Hall, J. (2008). Social cognition in schizophrenia: A review of face processing. British Medical Bulletin, 88(1), 43–58. https://doi.org/10.1093/bmb/ ldn035. Moray, N. (1959). Attention in dichotic listening: Affective cues and the influence of instructions. Quarterly Journal of Experimental Psychology, 11(1), 56–60. https:// doi.org/10.1080/17470215908416289. Nelson, B., Whitford, T. J., Lavoie, S., & Sass, L. A. (2014a). What are the neurocognitive correlates of basic self-disturbance in schizophrenia?: Integrating phenomenology and neurocognition. Part 1 (Source monitoring deficits). Schizophrenia Research, 152(1), 12–19. https://doi.org/10.1016/j.schres.2013.06.022. Nelson, B., Whitford, T. J., Lavoie, S., & Sass, L. A. (2014b). What are the neurocognitive correlates of basic self-disturbance in schizophrenia?: Integrating phenomenology and neurocognition: Part 2 (aberrant salience). Schizophrenia Research, 152(1), 20–27. https://doi.org/10.1016/j.schres.2013.06.033. Northoff, G., Heinzel, A., De Greck, M., Bermpohl, F., Dobrowolny, H., & Panksepp, J. (2006). Self-referential processing in our brain—a meta-analysis of imaging studies on the self. Neuroimage, 31(1), 440–457. https://doi.org/10.1016/j.neuroimage.2005.12.002. Northoff, G. (2007). Psychopathology and pathophysiology of the self in depression—neuropsychiatric hypothesis. Journal of Affective Disorders, 104(1–3), 1–14. https://doi.org/10.1016/j.jad.2007.02.012. Northoff, G. (2011). Self and brain: What is self-related processing. Trends in Cognitive Sciences, 15(5), 186–187. https://doi.org/10.1016/j.tics.2011.03.001. Northoff, G. (2014). Resting state activity and the “stream of consciousness” in schizophrenia—neurophenomenal hypotheses. Schizophrenia Bulletin, 41(1), 280–290. https://doi.org/10.1093/schbul/sbu116. Northoff, G. (2016). Is the self a higher-order or fundamental function of the brain? The “basis model of self-specificity” and its encoding by the brain’s spontaneous activity. Cognitive Neuroscience, 7(1–4), 203–222. https://doi.org/10.1080/17588928.2015.1111868. Northoff, G., & Duncan, N. W. (2016). How do abnormalities in the brain’s spontaneous activity translate into symptoms in schizophrenia? From an overview of resting state activity findings to a proposed spatiotemporal psychopathology. Progress in Neurobiology, 145, 26–45. https://doi.org/10.1016/j.pneurobio.2016.08.003. Oshima, I., Ito, J., Yagihashi, M., & Okagami, K. (1994). The relationship between expressed emotion and daily life functioning of families who take care of the schizophrenics members. Seishin shinkeigaku zasshi= Psychiatria et neurologia Japonica, 96(7), 493–512 in Japanese. Platek, S. M., Keenan, J. P., Gallup, G. G., Jr, & Mohamed, F. B. (2004). Where am I? The neurological correlates of self and other. Cognitive Brain Research, 19(2), 114–122. https://doi.org/10.1016/j.cogbrainres.2003.11.014. Platek, S. M., Loughead, J. W., Gur, R. C., Busch, S., Ruparel, K., Phend, N., ... Langleben, D. D. (2006). Neural substrates for functionally discriminating self-face from personally familiar faces. Human Brain Mapping, 27(2), 91–98. https://doi.org/10.1002/hbm.20168. Platek, S. M., & Kemp, S. M. (2009). Is family special to the brain? An event-related fMRI study of familiar, familial, and self-face recognition. Neuropsychologia, 47(3), 849–858. https://doi.org/10.1016/j.neuropsychologia.2008.12.027. Qin, P., Liu, Y., Shi, J., Wang, Y., Duncan, N., Gong, Q., ... Northoff, G. (2012). Dissociation between anterior and posterior cortical regions during self-specificity and familiarity: A combined fMRI–meta-analytic study. Human Brain Mapping, 33(1), 154–164. https://doi.org/10.1002/hbm.21201. Stein, T., Hebart, M. N., & Sterzer, P. (2011). Breaking continuous flash suppression: A new measure of unconscious processing during interocular suppression? Frontiers in Human Neuroscience, 5, 167. https://doi.org/10.3389/fnhum.2011.00167. Seymour, K., Rhodes, G., Stein, T., & Langdon, R. (2016). Intact unconscious processing of eye contact in schizophrenia. Schizophrenia Research: Cognition, 3, 15–19. https://doi.org/10.1016/j.scog.2015.11.001. Stein, T., Siebold, A., & van Zoest, W. (2016). Testing the idea of privileged awareness of self-relevant information. Journal of Experimental Psychology: Human Perception and Performance, 42(3), 303. https://doi.org/10.1037/xhp0000197. Sugiura, M., Sassa, Y., Jeong, H., Horie, K., Sato, S., & Kawashima, R. (2008). Face-specific and domain-general characteristics of cortical responses during selfrecognition. Neuroimage, 42(1), 414–422. https://doi.org/10.1016/j.neuroimage.2008.03.054. Symons, C. S., & Johnson, B. T. (1997). The self-reference effect in memory: A meta-analysis. Psychological bulletin, 121(3), 371. https://doi.org/10.1037/0033-2909. 121.3.371. Taylor, M. J., Arsalidou, M., Bayless, S. J., Morris, D., Evans, J. W., & Barbeau, E. J. (2009). Neural correlates of personally familiar faces: Parents, partner and own faces. Human Brain Mapping, 30(7), 2008–2020. https://doi.org/10.1002/hbm.20646. Tong, F., & Nakayama, K. (1999). Robust representations for faces: Evidence from visual search. Journal of Experimental Psychology: Human Perception and Performance, 25(4), 1016. https://doi.org/10.1037//0096-1523.25.4.1016. Tsuchiya, N., & Koch, C. (2005). Continuous flash suppression reduces negative afterimages. Nature Neuroscience, 8(8), 1096. https://doi.org/10.1038/nn1500. Tsuchiya, N., Moradi, F., Felsen, C., Yamazaki, M., & Adolphs, R. (2009). Intact rapid detection of fearful faces in the absence of the amygdala. Nature Neuroscience, 12(10), 1224. https://doi.org/10.1038/nn.2380. Uddin, L. Q., Kaplan, J. T., Molnar-Szakacs, I., Zaidel, E., & Iacoboni, M. (2005). Self-face recognition activates a frontoparietal “mirror” network in the right hemisphere: An event-related fMRI study. Neuroimage, 25(3), 926–935. https://doi.org/10.1016/j.neuroimage.2004.12.018. Whittaker, J. F., Deakin, J. F. W., & Tomenson, B. (2001). Face processing in schizophrenia: Defining the deficit. Psychological Medicine, 31(3), 499–507. https://doi. org/10.1017/S0033291701003701. Xu, S., Zhang, S., & Geng, H. (2011). Gaze-induced joint attention persists under high perceptual load and does not depend on awareness. Vision Research, 51(18), 2048–2056. https://doi.org/10.1016/j.visres.2011.07.023. Yang, H., Wang, F., Gu, N., Gao, X., & Zhao, G. (2013). The cognitive advantage for one’s own name is not simply familiarity: An eye-tracking study. Psychonomic Bulletin & Review, 20(6), 1176–1180. https://doi.org/10.3758/s13423-013-0426-z. Yun, J. Y., Hur, J. W., Jung, W. H., Jang, J. H., Youn, T., Kang, D. H., ... Kwon, J. S. (2014). Dysfunctional role of parietal lobe during self-face recognition in schizophrenia. Schizophrenia Research, 152(1), 81–88. https://doi.org/10.1016/j.schres.2013.07.010. Zhang, L., Zhu, H., Xu, M., Jia, H., & Liu, J. (2012). Selective impairment in recognizing the familiarity of self faces in schizophrenia. Chinese Science Bulletin, 57(15), 1818–1823. https://doi.org/10.1007/s11434-012-5109-z.
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Deficits of subliminal self-face processing in schizophrenia Song Zhoua,1, Yuanyuan Xub,c,1, Nanbo Wanga, Shen Zhangd, Haiyan Genga, , ⁎ Hongxiao Jiab,c, ⁎
T
a
School of Psychological and Cognitive Sciences, Beijing Key Laboratory of Behavior and Mental Health, Peking University, Beijing, China The National Clinical Research Center for Mental Disorders & Beijing Key Laboratory of Mental Disorders, Beijing Anding Hospital, Capital Medical University, Beijing, China c Advanced Innovation Center for Human Brain Protection, Capital Medical University, Beijing, China d Department of Psychology, University of Wisconsin-Whitewater, Whitewater, WI, USA b
ARTICLE INFO
ABSTRACT
Keywords: Schizophrenia Face processing Self-face advantage Interocular suppression Subliminal
Most studies show that self-processing in schizophrenia is impaired at the supraliminal level. Schizophrenic patients generally lack the ability to prioritize the processing of self-related information, such as their own face. However, some evidence suggests that schizophrenic patients may retain intact subliminal processing abilities even though their conscious experiences are compromised. We conducted the first study exploring schizophrenic patients’ subliminal self-face processing. Using a breaking continuous flash suppression (bCFS) paradigm, we interocularly suppressed face images (self, famous, and unknown faces). Participants’ reaction times to detect the faces when they broke the suppression were recorded as an index for the subliminal processing of faces. Unlike the healthy controls, schizophrenic patients did not demonstrate a processing advantage for their own face when it broke interocular suppression; only a face familiarity effect was found. These findings contribute to the understanding of self-processing deficits in schizophrenia.
1. Introduction As a complex psychotic disorder, schizophrenia involves various symptoms, such as delusions, hallucinations, and cognitive impairments, which often cause patients to have difficulty functioning in their daily lives (Bellani & Brambilla, 2008; Berkovitch, Dehaene, & Gaillard, 2017; Oshima, Ito, Yagihashi, & Okagami, 1994). From a phenomenological view in psychopathology, these severe impairments are attributed to “self-disturbance”, which is the clinical core of the phenotypic traits of schizophrenia that refers to an unstable or distorted basic sense of self, as people with schizophrenia may have a diminished ownership of their experiences and disturbed self-other/self-world boundaries (Nelson et al., 2014a, 2014b). The underlying mechanism is that altered/aberrant neural activities in the brain, e.g., spatiotemporal changes in the brain’s spontaneous activity, may affect an individual’s ability to correctly distinguish between stimuli that should be labeled as originating from himself/herself and external stimuli from the environment at the experiential level (Northoff & Duncan, 2016; Northoff, 2014). An embodiment of the basic sense of self is one’s ability to recognize his/her own face (Kircher, Seiferth, Plewnia, Baar, & ⁎ Corresponding authors at: School of Psychological and Cognitive Sciences, Peking University, 5 Yiheyuan Road, Beijing 100871, China (H. Geng). Beijing Anding Hospital, Capital Medical University, Room 102, Xingzheng Building, 5th Ankanghutong, Deshengmenwai Street, Xicheng District, Beijing 100088, China (H. Jia). E-mail addresses: [email protected] (H. Geng), [email protected] (H. Jia). 1 These authors have contributed equally to this work and should be considered co-first authors.
https://doi.org/10.1016/j.concog.2020.102896 Received 10 July 2019; Received in revised form 21 December 2019; Accepted 1 February 2020 1053-8100/ © 2020 Elsevier Inc. All rights reserved.
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Schwabe, 2007). Normal individuals exhibit superior performance in recognizing self-related information, e.g., their own face, compared to other-related information, e.g., another person’s face because the “self” is such an important mediating construct in much of human social interactions and personalities (Anderson, 1984) that the perception, comprehension, and interpretation of various items as self-related benefit from advantages in cognitive processing (Brédart, Delchambre, & Laureys, 2006; Keenan, Freund, Hamilton, Ganis, & Pascual-Leone, 2000; Moray, 1959; Symons & Johnson, 1997; Tong & Nakayama, 1999; Yang, Wang, Gu, Gao, & Zhao, 2013). In some studies, people responded significantly faster and more accurately to the presentation of their self-face when judging the ownership of different faces (2010; Keenan et al., 1999; Ma & Han, 2009). Since the experiment tasks require participants to explicitly reference the attributes of stimuli (such as personality traits or faces) and relate them to the self, these studies are believed to examine self-referential processing (Northoff et al., 2006, 2016). Some studies, in contrast, examine self-related processing (Northoff et al., 2016, 2007, 2011). Instead of requiring explicit referencing between themselves and the stimuli, these studies asked participants to perform other cognitive tasks that were irrelevant to the self (such as discriminating orientations of the self-face and familiar faces, Ma & Han, 2009, 2010), during which a processing advantage is observed for self-related stimuli (e.g., the selfface). For people with schizophrenia, however, the literature has not been consistent regarding the advantage of processing one’s own face. Self-face processing itself can be either self-referential or self-related. In most self-referential studies involving judging the identity of different faces (e.g., Irani et al., 2006; Kircher et al., 2007) or deciding whether a morphed face was their own face (e.g., Heinisch, Wiens, Gründl, Juckel, & Brüne, 2013; Jia, Yang, Zhu, Liu, & Barnaby, 2015), schizophrenic patients showed an absence of the abovementioned advantage, demonstrating slower reaction times or no reaction time differences when identifying their own face vs. a familiar person’s face and/or lower accuracy when identifying their own face. Nevertheless, in studies examining self-related processing (e.g., when participants were asked to detect changes in rapidly presented unknown, self, or familiar faces), patients seemed to perform significantly better when the stimulus was related to the self-face (Kochs, Köhler, Merz, & Sterzer, 2017). Many factors, such as task type and demand, are thought to contribute to the mixed findings (Bortolon, Capdevielle, Salesse, & Raffard, 2016; Kochs et al., 2017). One factor that has not been examined is the level of awareness. The abovementioned studies, regardless of explicit self-referential or implicit self-related processing, all presented the stimuli above the awareness threshold. Given different lines of research showing that schizophrenic patients have intact subliminal processing of emotional faces (Kring, Siegel, & Barrett, 2014) and upright/inverted faces (Caruana, Stein, Watson, Williams, & Seymour, 2019) as well as eye gazes (Seymour, Rhodes, Stein, & Langdon, 2016), while supraliminal processing of similar facial stimuli is likely hampered (Hall et al., 2004; Marwick & Hall, 2008; Whittaker, Deakin, & Tomenson, 2001), it is possible that a similar dissociation exists in self-face processing in schizophrenic patients. Therefore, it is necessary to examine schizophrenic patients’ processing of their own face at the subliminal level. In particular, would schizophrenic patients have an advantage in processing their self-face compared to another’s face when the faces are presented subliminally? To address this question, we adopted the breaking continuous flash suppression (bCFS; Jiang, Costello, & He, 2007) paradigm, which has recently seen increased use in the investigation of unconscious processing (Gayet & Stein, 2017; Stein, Hebart, & Sterzer, 2011; Stein, Siebold, & van Zoest, 2016). In this paradigm, a face image is presented to participants’ nondominant eye with increasing contrast, while a dynamic set of noise images is presented to his/her dominant eye; this combination formulates interocular suppression and, consequently, results in a conscious perception of noise images, with the face image initially being invisible. However, as the contrast of the face image gradually increases, it will finally break the suppression to enter awareness and be recognized. This paradigm can stably block a visual stimulus from consciousness (i.e., being invisible) for a considerable amount of time until it is sufficiently processed to break into awareness (Jiang et al., 2007; but see Gayet, Van der Stigchel, & Paffen, 2014, which questions the awareness level during suppression). Since stimuli that have an advantage in subliminal processing would break interocular suppression faster than those without an advantage, the time needed for a face to break into awareness is taken as the measure of participants’ subliminal processing of that face (Jiang et al., 2007; Seymour et al., 2016; Tsuchiya, Moradi, Felsen, Yamazaki, & Adolphs, 2009). Therefore, observing possible time differences between the self- and other faces to break interocular suppression allows us to compare the processing of different faces. The face stimuli we used were participants’ own faces, a famous person's face and an unknown face from a stranger. To rule out possible alterative explanations for any results we might find, such as participants’ different criteria for detection or response speeds associated with different types of physical face stimuli, a control condition was included in the study, in which participants binocularly viewed the same stimuli as in the experimental condition but without interocular rivalry (Gayet, Paffen, Belopolsky, Theeuwes, & Van der Stigchel, 2016; Jiang et al., 2007). We also included healthy participants for comparison. If an advantage exists for the subliminal processing of the participants’ self-face, self-face stimuli would break the suppression faster than the famous face. Otherwise, if the self-face processing advantage is absent at the subliminal level, we predicted that no significant differences would be observed in the reaction times between the self-face and the famous face stimuli. 2. Methods 2.1. Participants The sample size of our study was determined via a priori power analysis using G*Power 3 (Faul, Erdfelder, Buchner, & Lang, 2009). With a power of 0.90, an alpha level of 0.05, and an estimated large effect size (partial η2 = 0.14) in subliminal self-processing (Geng, Zhang, Li, Tao, & Xu, 2012), the power analysis yielded an estimated sample size of 32 for the healthy controls (we assumed a similar sample size would be needed for patients). We terminated participant recruitment when the targeted number of eligible 2
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Table 1 Participants’ demographic and clinical characteristics. Patients (N = 35)
Age (years) Gender (M/F) Illness duration (years) CED (mg/day) PANSS total score Positive symptoms Negative symptoms General psychopathology
Control (N = 33)
Mean
SE
Mean
SE
23.26 14/21 4.21 591.2 63.71 14.37 18.97 30.37
± 0.95
24.67 12/21
± 0.51
± 0.69 ± 40.39 ± 1.35 ± 0.66 ± 0.80 ± 0.63
Note: M: male; F: female; CED: Chlorpromazine Equivalents Dose; PANSS: Positive and Negative Symptoms Scale; SE: standard error.
participants was achieved and finished data collection with the participants already scheduled. Our final sample included 35 schizophrenic patients and 33 healthy controls who were included in the data analysis. Schizophrenic patients were recruited from Beijing Anding Hospital and Capital Medical University, where they were being treated. The patients ranged in age from 16 to 60 years old. All of the patients met the criteria for schizophrenia in the Diagnostic and Statistical Manual of Mental Disorders, Fifth Edition (DSM-V, American Psychiatric Association, 2013) and were being medicated with antipsychotics at the time of the study. Substance abuse, comorbid neurological disorders, history of severe brain trauma or current use of electroconvulsive therapy were used as criteria to exclude ineligible participants. In addition, no participants experienced acute symptom exacerbations in the experiment. Healthy controls were recruited from the Beijing area through advertisements and staff working at the hospital. The age, gender and education level of healthy controls were roughly matched with those of the schizophrenic patient group (see Table 1, t (66)age = 1.28, page = 0.204; X2gender = 84.095, pgender = 0.758). Individuals who met the criteria for any disorder in the DSM-V or who had any first-degree relative with schizophrenia were excluded. All participants had normal or corrected-to-normal vision and were able to recognize the former Chinese Prime Minister Wen Jiabao from a facial picture provided prior to their participation in the experiment. The demographic and clinical characteristics of the two groups are presented in Table 1. This study was approved by the Ethics Review Committees of the Beijing Anding Hospital and Capital Medical University as well as by Peking University. All participants gave written informed consent before the study and received a full explanation of the study after their participation. 2.2. Stimuli 2.2.1. Face images The stimuli used in the current study were created in a manner similar to that used in our previous study (Geng et al., 2012). The self-face stimulus was a photograph of each participant’s own face taken by a research assistant in the lab with a digital camera prior to the experiment. The famous face stimulus was a photo of the former Chinese Prime Minister Wen Jiabao, who was highly familiar to the participants. The unknown face stimulus was a photograph of someone who the participants had never met. All face pictures were front-view shots with neutral facial expressions. In addition, a scrambled face was used in the catch trials (randomly scrambled into 169 blocks of 20 × 20 pixels, see Fig. 3), which was completely unrecognizable as any part of a face. All pictures were processed in Adobe Photoshop 5.0 to create standardized stimuli. Specifically, each image was modified to retain only the facial part between the forehead and chin, with the nose located at the center of the picture and the pupil to pupil distance equalized across pictures. Then, each modified image was resized to 256 × 256 pixels (5.51 × 5.51 visual angle) and matched on brightness (luminance = 3.7 cd/mm2) and contrast (root-mean-square contrast = 0.51). Final low-contrast blue face images were produced by removing the red and green color channels of these images, and these images were presented against a gray background (128, 128, 128 RGB). 2.2.2. Noise images Noise images that matched the size of the face images were created with OpenGL 2.0 (Silicon Graphics International Corp., Fremont, California, US), and these images were presented successively in sets during each trial of the experiment. In such a dynamic noise image set, each image consisted of differently mixed red and green squares of various sizes, and in each successive noise image, 10% of the area of the previous picture was replaced by new squares at random locations. The face and noise images were overlapped with each other at the center of the computer screen and were surrounded by a whiteblack frame (see Fig. 1). The noise images were always presented at full contrast, whereas the contrast of the face images was gradually increased in each trial.
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Fig. 1. Illustration of a critical trial in the experimental condition.
Fig. 2. Log-transformed reaction times of the self-face, famous face, and unknown face for schizophrenic participants and healthy controls, shown separately for the experimental and control conditions. *p < .05.
Fig. 3. The scrambled face used in the catch trials.
2.3. Procedure Our study used a 3 (Face: self vs. famous vs. unknown) × 2 (Group: schizophrenic patients vs. healthy controls) mixed factorial design for both the experimental and control conditions. 4
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The procedure used in this experiment was very similar to that of Geng et al. (2012). Participants attended the study individually, and a chin rest was used to maintain a viewing distance of 60 cm from the computer screen. After providing informed consent, the participants began the experiment with practice trials so that they could become familiar with the task. Then, participants completed two blocks of trials in random order, one for the experimental condition and the other for the control condition. In the experimental block, participants wore a pair of red-blue anaglyph glasses so that the noise images were only visible to their dominant eye through the red filter lens, and simultaneously, the face image was only visible to their other eye through the blue filter lens (see Fig. 1). The resulting interocular suppression consequently allowed participants to see continuous presentations of the noise images, but they were not aware of the existence of the face image until it broke into awareness. The set of noise images was presented at a rate of 100 Hz, which is believed to produce robust interocular suppression (Xu, Zhang, & Geng, 2011) compared to the common 10 Hz rate presentation (Tsuchiya & Koch, 2005). In the control block, instead of wearing the anaglyph glasses, participants were binocularly presented the face and noise stimuli without suppression. As a result, the face image coalesced with the dynamic noise pattern initially, but its contrast gradually increased. Meanwhile, the participants’ visual experiences mimicked those in the experimental condition, with the perception that the face image gradually emerged from the noise background at a certain time point. A total of 55 trials were included in each block, with 45 critical trials presenting face stimuli: self, famous, and unknown faces (15 trials for each face). The remaining 10 trials with scrambled faces were catch trials that were used to detect false alarms (i.e., when participants reported seeing a face or a facial part that was not actually present). If three or more false alarms occurred within a block, that block would restart. No participant exceeded this limit. Each critical trial began with the binocular presentation of a fixation cross, which flashed for 2000 ms to draw participants’ attention. Then, a set of noise images was presented to the dominant eye at full contrast, and at the same time, a face image was presented for 1000 ms to the nondominant eye of the participant with its contrast gradually increased from 0% to 100% (programmed by manipulating the alpha channel value of the pictures to change from 0 to 1). After reaching full contrast, the face image remained constant until the end of the trial. Given that the binocular presentation of stimuli in the control condition may make the task easier, the increase in the contrast of face images in that block was modified to be 4000 ms to match the difficulty level of the task to that in the experimental block. Participants were instructed to press the space bar as quickly as possible upon the appearance of the face image or any part of it. The face and noise images remained on the screen until a response was made or 10 s had elapsed. Participants’ reaction times were recorded as the time required for the face image to break interocular suppression. Trials with no response or with extreme reaction times (more than 3 standard deviations from the mean) were not included in the analysis (less than 5% of the total trials). 3. Results We performed log-transformation (log10) on each participant’s reaction times to account for the positively skewed distribution of the data (Caruana et al., 2019; Gayet & Stein, 2017; Heyman & Moors, 2014). Log-transformed reaction times in the experimental condition were subjected to a 3 × 2 repeated-measures ANOVA, with Face (self vs. famous vs. unknown) as a within-participants factor and Group (schizophrenic patients vs. healthy controls) as a betweenparticipants factor. Sidak correction was applied to all post hoc pairwise comparisons reported in this paper. The results revealed a significant main effect of Face, F(2, 65) = 14.238, p < .001, ηp2 = 0.305. In general, participants’ detection times to the self-face (M = 0.197 s, SEM = 0.017) and the famous face (M = 0.21 s, SEM = 0.016) were similar, t(65) = 1.625, p = .287, d = 0.197, but significantly faster than the detection of the unknown face (M = 0.237 s, SEM = 0.017), t self vs. unknown (65) = 5.125, p < .001, d = 0.621, t famous vs. unknown (65) = 3.857, p = .002, d = 0.468 (see Fig. 2). The main effect of Group was also significant, F(1, 66) = 0.547, p < .001, ηp2 = 0.286. The healthy controls (M = 0.132 s, SEM = 0.023) responded significantly faster than the patients (M = 0.298 s, SEM = 0.023). These main effects were qualified by a significant Face × Group interaction, F(2, 65) = 3.335, p = .042, ηp2 = 0.093. For the healthy participants, the self-face (M = 0.101 s, SEM = 0.017) was detected faster than the famous face (M = 0.132 s, SEM = 0.015), t(32) = 2.583, p = .031, d = 0.45, and the famous face was detected faster than the unknown face (M = 0.161 s, SEM = 0.017), t(32) = 2.636, p = .026, d = 0.459. However, for the schizophrenic patients, the only significant difference was the faster detection time of the famous face (M = 0.288 s, SEM = 0.029) than the unknown face (M = 0.314 s, SEM = 0.029), t(35) = 2.6, p = .048, d = 0.439. The detection time of the self-face (M = 0.292 s, SEM = 0.028) and other faces were not significantly different, t self vs. famous (35) = 0.364, p = .977, d = 0.061, t self vs. unknown (35) = 1.909, p = .161, d = 0.323. The same 3 × 2 ANOVA was conducted on the log-transformed reaction times in the control condition. The main effect of Face was significant, F(2, 65) = 26.556, p < .001, ηp2 = 0.45. Participants had similar detection times for the self-face (M = 0.159 s, SEM = 0.017) and the famous face (M = 0.159 s, SEM = 0.018), t(65) = 0, p = 1, d = 0, but both of these times were faster than their detection time for the unknown face (M = 0.214 s, SEM = 0.018), t self vs. unknown (65) = 5.5, p < .001, d = 0.667, t famous vs. unknown (65) = 6.875, p < .001, d = 0.833 (see Fig. 2). The main effect of Group was also significant, F(1, 66) = 16.820, p < .001, ηp2 = 0.203, with faster detection of the faces in the healthy group (M = 0.107 s, SEM = 0.025) than in the schizophrenia group (M = 0.247 s, SEM = 0.024). However, the interaction between Face and Group was not significant, F(2, 65) = 0.286, p = .752, ηp2 = 0.009. 4. Discussion Although ample evidence has demonstrated the advantage of processing one’s own face in healthy individuals (2010; Keenan et al., 1999; Ma & Han, 2009), most studies have suggested a lack of the self-advantage effect in schizophrenic patients when 5
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identifying their own faces compared to a familiar face (e.g., Bortolon et al., 2016; Irani et al., 2006) when these studies were carried out above the conscious level of the participants. Given that dissociation of supraliminal and subliminal cognitive processing often exists (e.g., Geng et al., 2012) and that evidence indicates different performance for schizophrenic patients at different levels of awareness (see Berkovitch et al., 2017 for a review), we incorporated a bCFS paradigm in a commonly used face detection task to examine whether the subliminal processing of the self-face remains intact in schizophrenic patients (i.e., demonstrating a self-face advantage). Although the self-face processing advantage involves comparing the self-face and another face, if the other face is a stranger’s face, it is unclear whether any findings reflect a face familiarity effect or the uniqueness of the self-face, as the self-face is also more familiar than the unknown face (Qin et al., 2012). Therefore, by including a famous/familiar face condition, we can control for familiarity, and then a comparison of the processing of the self-face with that of a familiar face can determine whether a self-face advantage exists in subliminal face processing. Additionally, by comparing participants’ processing of the famous face with that of the unknown face, we assessed the existence of subliminal familiarity effects. Our findings revealed a subliminal self-face advantage in the healthy controls, as they showed significantly faster reaction times for the self-face than for the famous face in the experimental condition. However, such a self-face processing advantage was not found in the schizophrenic patients. The speed of detecting the self-face for schizophrenic patients was comparable to that of the famous face. Given that the famous face entered awareness faster than the unknown face (the familiarity effect), which means that participants did process the face stimuli, the absence of the advantage for the self-face over the famous face probably suggests impaired subliminal self-face processing in schizophrenic patients. This finding is surprising and interesting because in other CFS studies with different stimuli, such as gazes, upright/inverted faces or emotional faces, schizophrenic patients showed intact unconscious processing at the subliminal level (Caruana et al., 2019; Kring et al., 2014; Seymour et al., 2016). In fact, to date, research tends to find defective supraliminal cognitive processing in schizophrenic patients, such as visual perception, metacognition, or self-monitoring, but preserved automatic processing, which relies less on consciousness (Berkovitch et al., 2017; Kochs et al., 2017). Nevertheless, schizophrenic patients in our study seemed to have compromised performance when detecting their own faces below the awareness threshold. Since past research showing intact subliminal processing among schizophrenic patients mostly used tasks irrelevant to the self, we speculate that unlike general cognitive abilities, self-face processing is impaired among schizophrenic patients because it is self-related. Given that the existing neural evidence on sense of self is largely based on supraliminal self-processing, future research should explore the representation of subliminal self-processing in the brains of healthy people as well as in schizophrenic patients. Meanwhile, for both the schizophrenic patients and the healthy controls, the famous face broke suppression significantly faster than the unknown face both in the experimental condition and in the control condition. In other words, these results demonstrate a familiarity effect. This effect exists in subliminal face processing in schizophrenic patients, as well as in healthy people, in accordance with the supraliminal results of previous research (Heinisch et al., 2013; Kochs et al., 2017; Yun et al., 2014). Given that evidence exists showing that schizophrenic patients are able to subliminally process other facial information (Caruana et al., 2019; Kring et al., 2014; Seymour et al., 2016), the face familiarity effects found in our study enrich our understanding of schizophrenic patients’ capacities at the subliminal level. Why did schizophrenic patients fail to exhibit a self-face advantage but did experience an intact familiarity effect? This result may have occurred because the perceptional encoding of a face remains unimpaired, but the patients have difficulty associating the face with its identity. In addition, having a relatively short illness duration (4 years on average) may contribute to an intact familiarity effect in patients (Bortolon, Capdevielle, & Raffard, 2015), even subliminally. At the neural level, self-specific processing and face familiarity processing are believed to be associated with distinct networks (Keenan, Wheeler, Gallup, and Pascual-Leone, 2000; Zhang, Zhu, Xu, Jia, & Liu, 2012). Compared to unknown faces, familiar faces selectively activate brain regions such as the bilateral temporoparietal lobe, medial prefrontal cortex and precuneus (Sugiura et al., 2008; Taylor et al., 2009; Uddin, Kaplan, MolnarSzakacs, Zaidel, & Iacoboni, 2005). However, compared to familiar faces, self-face processing further activates regions such as the superior, middle, and inferior frontal gyri, as well as the inferior parietal lobe in the right hemisphere, along with bilateral ventral occipitotemporal regions (Decety & Chaminade, 2003; Platek & Kemp, 2009; Platek et al., 2004, 2006; Sugiura et al., 2008; Uddin et al., 2005). This separation between the neural mechanisms of the self and familiarity processing makes it possible that selfprocessing could be damaged, but familiarity processing could remain intact. In the current design, we included a control condition that presented the same face stimuli to create similar subject experiences as in the experimental condition, except that the control condition did not involve interocular suppression. Since there were no significant reaction time differences when responding to the self-face vs. the famous face in this control condition (for both schizophrenic patients and healthy controls), we can rule out the possibility that the findings in the experimental condition were simply due to the physical characteristics of the face stimuli (Gayet et al., 2016). We recognize that there are some debates on whether bCFS is an ideal paradigm for examining unconscious processing (e.g., completely blocking awareness regardless of stimuli characteristics and postperceptual factors in participants’ responses). In addition, some may argue that the catch trials used in our study created postperceptual confounds as they may incentivize participants to delay their reaction. However, given that we found significantly different reaction times between the self-face and familiar face in the experimental condition but not in the control condition for healthy people, such results tend to support our argument for selfprocessing rather than confounding factors such as postperceptual reactions. Still, the characteristics of patients’ subliminal selfprocessing should be further explored with other paradigms in the future. In conclusion, in the current study, we found that schizophrenic patients had impaired self-face processing at the subliminal level, but their processing of face familiarity was intact. These findings help further our understanding of self-related deficits in 6
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schizophrenia. Future studies should continue to investigate subliminal self-processing and related factors in healthy and schizophrenic populations. CRediT authorship contribution statement Song Zhou: Conceptualization, Methodology, Software, Investigation, Data curation, Formal analysis, Writing - original draft. Yuanyuan Xu: Conceptualization, Methodology, Software, Investigation, Data curation, Formal analysis, Writing - original draft. Nanbo Wang: Conceptualization, Methodology, Formal analysis, Writing - original draft, Writing - review & editing, Visualization. Shen Zhang: Conceptualization, Methodology, Formal analysis, Writing - original draft, Writing - review & editing. Haiyan Geng: Conceptualization, Methodology, Validation, Formal analysis, Writing - original draft, Writing - review & editing, Resources, Supervision, Project administration, Funding acquisition. Hongxiao Jia: Conceptualization, Methodology, Validation, Formal analysis, Writing - original draft, Resources, Supervision, Project administration, Funding acquisition. Declaration of Competing Interest All authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgments This research was supported by grants from the National Natural Science Foundation of China to HG (31671131, 31271202 and 30870763) and HJ (81873398). Appendix A. Supplementary material Supplementary data to this article can be found online at https://doi.org/10.1016/j.concog.2020.102896. References Anderson, J. R. (1984). The development of self-recognition: A review. Developmental Psychobiology: The Journal of the International Society for Developmental Psychobiology, 17, 35–49. https://doi.org/10.1016/s0273-2297(84)80006-4. American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (DSM-5®). American Psychiatric Pub. Bellani, M., & Brambilla, P. (2008). The use and meaning of the continuous performance test in schizophrenia. Epidemiology and Psychiatric Sciences, 17(3), 188–191. https://doi.org/10.1017/s1121189x00001275. Berkovitch, L., Dehaene, S., & Gaillard, R. (2017). Disruption of conscious access in schizophrenia. Trends in Cognitive Sciences, 21(11), 878–892. https://doi.org/10. 1016/j.tics.2017.08.006. Bortolon, C., Capdevielle, D., & Raffard, S. (2015). Face recognition in schizophrenia disorder: A comprehensive review of behavioral, neuroimaging and neurophysiological studies. Neuroscience & Biobehavioral Reviews, 53, 79–107. https://doi.org/10.1016/j.neubiorev.2015.03.006. Bortolon, C., Capdevielle, D., Salesse, R. N., & Raffard, S. (2016). Further insight into self-face recognition in schizophrenia patients: Why ambiguity matters. Journal of Behavior Therapy and Experimental Psychiatry, 50, 215–222. https://doi.org/10.1016/j.jbtep.2015.09.006. Brédart, S., Delchambre, M., & Laureys, S. (2006). Short article one's own face is hard to ignore. Quarterly Journal of Experimental Psychology, 59(1), 46–52. https://doi. org/10.1080/17470210500343678. Caruana, N., Stein, T., Watson, T., Williams, N., & Seymour, K. (2019). Intact prioritisation of unconscious face processing in schizophrenia. Cognitive Neuropsychiatry, 24(2), 135–151. https://doi.org/10.1080/13546805.2019.1590189. Decety, J., & Chaminade, T. (2003). When the self represents the other: A new cognitive neuroscience view on psychological identification. Consciousness and Cognition, 12(4), 577–596. https://doi.org/10.1016/s1053-8100(03)00076-x. Faul, F., Erdfelder, E., Buchner, A., & Lang, A. G. (2009). Statistical power analyses using G* Power 3.1: Tests for correlation and regression analyses. Behavior Research Methods, 41(4), 1149–1160. https://doi.org/10.3758/BRM.41.4.1149. Gayet, S., Paffen, C. L., Belopolsky, A. V., Theeuwes, J., & Van der Stigchel, S. (2016). Visual input signaling threat gains preferential access to awareness in a breaking continuous flash suppression paradigm. Cognition, 149, 77–83. https://doi.org/10.1016/j.cognition.2016.01.009. Gayet, S., & Stein, T. (2017). Between-subject variability in the breaking continuous flash suppression paradigm: Potential causes, consequences, and solutions. Frontiers in Psychology, 8, 437. https://doi.org/10.3389/fpsyg.2017.00437. Gayet, S., Van der Stigchel, S., & Paffen, C. L. (2014). Breaking continuous flash suppression: Competing for consciousness on the pre-semantic battlefield. Frontiers in Psychology, 5, 460. https://doi.org/10.3389/fpsyg.2014.00460. Geng, H., Zhang, S., Li, Q., Tao, R., & Xu, S. (2012). Dissociations of subliminal and supraliminal self-face from other-face processing: Behavioral and ERP evidence. Neuropsychologia, 50(12), 2933–2942. https://doi.org/10.1016/j.neuropsychologia.2012.07.040. Hall, J., Harris, J. M., Sprengelmeyer, R., Sprengelmeyer, A., Young, A. W., Santos, I. M., ... Lawrie, S. M. (2004). Social cognition and face processing in schizophrenia. The British Journal of Psychiatry, 185(2), 169–170. https://doi.org/10.1192/bjp.185.2.169. Heinisch, C., Wiens, S., Gründl, M., Juckel, G., & Brüne, M. (2013). Self-face recognition in schizophrenia is related to insight. European Archives of Psychiatry and Clinical Neuroscience, 263(8), 655–662. https://doi.org/10.1016/s0920-9964(01)00310-3. Heyman, T., & Moors, P. (2014). Frequent words do not break continuous flash suppression differently from infrequent or nonexistent words: Implications for semantic processing of words in the absence of awareness. Plos One, 9(8), e104719. https://doi.org/10.1371/journal.pone.0104719. Irani, F., Platek, S. M., Panyavin, I. S., Calkins, M. E., Kohler, C., Siegel, S. J., ... Gur, R. C. (2006). Self-face recognition and theory of mind in patients with schizophrenia and first-degree relatives. Schizophrenia Research, 88(1–3), 151–160. https://doi.org/10.1016/j.schres.2006.07.016. Jia, H., Yang, J., Zhu, H., Liu, J., & Barnaby, N. (2015). Self-face recognition in the ultra-high risk for psychosis population. Early Intervention in Psychiatry, 9(2), 126–132. https://doi.org/10.1111/eip.12097. Jiang, Y., Costello, P., & He, S. (2007). Processing of invisible stimuli: Advantage of upright faces and recognizable words in overcoming interocular suppression. Psychological Science, 18(4), 349–355. https://doi.org/10.1111/j.1467-9280.2007.01902.x. Keenan, J. P., Freund, S., Hamilton, R. H., Ganis, G., & Pascual-Leone, A. (2000). Hand response differences in a self-face identification task. Neuropsychologia, 38(7), 1047–1053. https://doi.org/10.1016/s0028-3932(99)00145-1.
7
Consciousness and Cognition 79 (2020) 102896
S. Zhou, et al.
Keenan, J. P., McCutcheon, B., Freund, S., Gallup, G. G., Jr, Sanders, G., & Pascual-Leone, A. (1999). Left hand advantage in a self-face recognition task. Neuropsychologia, 37(12), 1421–1425. https://doi.org/10.1016/s0028-3932(99)00025-1. Keenan, J. P., Wheeler, M. A., Gallup, G. G., Jr, & Pascual-Leone, A. (2000). Self-recognition and the right prefrontal cortex. Trends in Cognitive Sciences, 4(9), 338–344. https://doi.org/10.1016/s1364-6613(00)01521-7. Kircher, T. T., Seiferth, N. Y., Plewnia, C., Baar, S., & Schwabe, R. (2007). Self-face recognition in schizophrenia. Schizophrenia Research, 94(1–3), 264–272. https://doi. org/10.1016/j.schres.2007.04.029. Kochs, A., Köhler, S., Merz, H., & Sterzer, P. (2017). Effects of self and familiarity on change detection in patients with schizophrenia. Psychiatry Research, 248, 140–146. https://doi.org/10.1016/j.psychres.2016.12.030. Kring, A. M., Siegel, E. H., & Barrett, L. F. (2014). Unseen affective faces influence person perception judgments in schizophrenia. Clinical Psychological Science, 2(4), 443–454. https://doi.org/10.1177/2167702614536161. Ma, Y., & Han, S. (2009). Self-face advantage is modulated by social threat–Boss effect on self-face recognition. Journal of Experimental Social Psychology, 45(4), 1048–1051. https://doi.org/10.1016/j.jesp.2009.05.008. Ma, Y., & Han, S. (2010). Why we respond faster to the self than to others? An implicit positive association theory of self-advantage during implicit face recognition. Journal of Experimental Psychology: Human Perception and Performance, 36(3), 619. https://doi.org/10.1037/a0015797. Marwick, K., & Hall, J. (2008). Social cognition in schizophrenia: A review of face processing. British Medical Bulletin, 88(1), 43–58. https://doi.org/10.1093/bmb/ ldn035. Moray, N. (1959). Attention in dichotic listening: Affective cues and the influence of instructions. Quarterly Journal of Experimental Psychology, 11(1), 56–60. https:// doi.org/10.1080/17470215908416289. Nelson, B., Whitford, T. J., Lavoie, S., & Sass, L. A. (2014a). What are the neurocognitive correlates of basic self-disturbance in schizophrenia?: Integrating phenomenology and neurocognition. Part 1 (Source monitoring deficits). Schizophrenia Research, 152(1), 12–19. https://doi.org/10.1016/j.schres.2013.06.022. Nelson, B., Whitford, T. J., Lavoie, S., & Sass, L. A. (2014b). What are the neurocognitive correlates of basic self-disturbance in schizophrenia?: Integrating phenomenology and neurocognition: Part 2 (aberrant salience). Schizophrenia Research, 152(1), 20–27. https://doi.org/10.1016/j.schres.2013.06.033. Northoff, G., Heinzel, A., De Greck, M., Bermpohl, F., Dobrowolny, H., & Panksepp, J. (2006). Self-referential processing in our brain—a meta-analysis of imaging studies on the self. Neuroimage, 31(1), 440–457. https://doi.org/10.1016/j.neuroimage.2005.12.002. Northoff, G. (2007). Psychopathology and pathophysiology of the self in depression—neuropsychiatric hypothesis. Journal of Affective Disorders, 104(1–3), 1–14. https://doi.org/10.1016/j.jad.2007.02.012. Northoff, G. (2011). Self and brain: What is self-related processing. Trends in Cognitive Sciences, 15(5), 186–187. https://doi.org/10.1016/j.tics.2011.03.001. Northoff, G. (2014). Resting state activity and the “stream of consciousness” in schizophrenia—neurophenomenal hypotheses. Schizophrenia Bulletin, 41(1), 280–290. https://doi.org/10.1093/schbul/sbu116. Northoff, G. (2016). Is the self a higher-order or fundamental function of the brain? The “basis model of self-specificity” and its encoding by the brain’s spontaneous activity. Cognitive Neuroscience, 7(1–4), 203–222. https://doi.org/10.1080/17588928.2015.1111868. Northoff, G., & Duncan, N. W. (2016). How do abnormalities in the brain’s spontaneous activity translate into symptoms in schizophrenia? From an overview of resting state activity findings to a proposed spatiotemporal psychopathology. Progress in Neurobiology, 145, 26–45. https://doi.org/10.1016/j.pneurobio.2016.08.003. Oshima, I., Ito, J., Yagihashi, M., & Okagami, K. (1994). The relationship between expressed emotion and daily life functioning of families who take care of the schizophrenics members. Seishin shinkeigaku zasshi= Psychiatria et neurologia Japonica, 96(7), 493–512 in Japanese. Platek, S. M., Keenan, J. P., Gallup, G. G., Jr, & Mohamed, F. B. (2004). Where am I? The neurological correlates of self and other. Cognitive Brain Research, 19(2), 114–122. https://doi.org/10.1016/j.cogbrainres.2003.11.014. Platek, S. M., Loughead, J. W., Gur, R. C., Busch, S., Ruparel, K., Phend, N., ... Langleben, D. D. (2006). Neural substrates for functionally discriminating self-face from personally familiar faces. Human Brain Mapping, 27(2), 91–98. https://doi.org/10.1002/hbm.20168. Platek, S. M., & Kemp, S. M. (2009). Is family special to the brain? An event-related fMRI study of familiar, familial, and self-face recognition. Neuropsychologia, 47(3), 849–858. https://doi.org/10.1016/j.neuropsychologia.2008.12.027. Qin, P., Liu, Y., Shi, J., Wang, Y., Duncan, N., Gong, Q., ... Northoff, G. (2012). Dissociation between anterior and posterior cortical regions during self-specificity and familiarity: A combined fMRI–meta-analytic study. Human Brain Mapping, 33(1), 154–164. https://doi.org/10.1002/hbm.21201. Stein, T., Hebart, M. N., & Sterzer, P. (2011). Breaking continuous flash suppression: A new measure of unconscious processing during interocular suppression? Frontiers in Human Neuroscience, 5, 167. https://doi.org/10.3389/fnhum.2011.00167. Seymour, K., Rhodes, G., Stein, T., & Langdon, R. (2016). Intact unconscious processing of eye contact in schizophrenia. Schizophrenia Research: Cognition, 3, 15–19. https://doi.org/10.1016/j.scog.2015.11.001. Stein, T., Siebold, A., & van Zoest, W. (2016). Testing the idea of privileged awareness of self-relevant information. Journal of Experimental Psychology: Human Perception and Performance, 42(3), 303. https://doi.org/10.1037/xhp0000197. Sugiura, M., Sassa, Y., Jeong, H., Horie, K., Sato, S., & Kawashima, R. (2008). Face-specific and domain-general characteristics of cortical responses during selfrecognition. Neuroimage, 42(1), 414–422. https://doi.org/10.1016/j.neuroimage.2008.03.054. Symons, C. S., & Johnson, B. T. (1997). The self-reference effect in memory: A meta-analysis. Psychological bulletin, 121(3), 371. https://doi.org/10.1037/0033-2909. 121.3.371. Taylor, M. J., Arsalidou, M., Bayless, S. J., Morris, D., Evans, J. W., & Barbeau, E. J. (2009). Neural correlates of personally familiar faces: Parents, partner and own faces. Human Brain Mapping, 30(7), 2008–2020. https://doi.org/10.1002/hbm.20646. Tong, F., & Nakayama, K. (1999). Robust representations for faces: Evidence from visual search. Journal of Experimental Psychology: Human Perception and Performance, 25(4), 1016. https://doi.org/10.1037//0096-1523.25.4.1016. Tsuchiya, N., & Koch, C. (2005). Continuous flash suppression reduces negative afterimages. Nature Neuroscience, 8(8), 1096. https://doi.org/10.1038/nn1500. Tsuchiya, N., Moradi, F., Felsen, C., Yamazaki, M., & Adolphs, R. (2009). Intact rapid detection of fearful faces in the absence of the amygdala. Nature Neuroscience, 12(10), 1224. https://doi.org/10.1038/nn.2380. Uddin, L. Q., Kaplan, J. T., Molnar-Szakacs, I., Zaidel, E., & Iacoboni, M. (2005). Self-face recognition activates a frontoparietal “mirror” network in the right hemisphere: An event-related fMRI study. Neuroimage, 25(3), 926–935. https://doi.org/10.1016/j.neuroimage.2004.12.018. Whittaker, J. F., Deakin, J. F. W., & Tomenson, B. (2001). Face processing in schizophrenia: Defining the deficit. Psychological Medicine, 31(3), 499–507. https://doi. org/10.1017/S0033291701003701. Xu, S., Zhang, S., & Geng, H. (2011). Gaze-induced joint attention persists under high perceptual load and does not depend on awareness. Vision Research, 51(18), 2048–2056. https://doi.org/10.1016/j.visres.2011.07.023. Yang, H., Wang, F., Gu, N., Gao, X., & Zhao, G. (2013). The cognitive advantage for one’s own name is not simply familiarity: An eye-tracking study. Psychonomic Bulletin & Review, 20(6), 1176–1180. https://doi.org/10.3758/s13423-013-0426-z. Yun, J. Y., Hur, J. W., Jung, W. H., Jang, J. H., Youn, T., Kang, D. H., ... Kwon, J. S. (2014). Dysfunctional role of parietal lobe during self-face recognition in schizophrenia. Schizophrenia Research, 152(1), 81–88. https://doi.org/10.1016/j.schres.2013.07.010. Zhang, L., Zhu, H., Xu, M., Jia, H., & Liu, J. (2012). Selective impairment in recognizing the familiarity of self faces in schizophrenia. Chinese Science Bulletin, 57(15), 1818–1823. https://doi.org/10.1007/s11434-012-5109-z.
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