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Childhood maltreatment impacts the early stage of facial emotion processing in young adults with negative schizotypy
Neuropsychologia 134 (2019) 107215
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Childhood maltreatment impacts the early stage of facial emotion processing in young adults with negative schizotypy Jingbo Gong a, b, Jianbo Liu c, **, Lizhi Shangguan a, Qin Zhang a, Zhu Peng a, Zun Li a, Chuwen Chen a, Lijuan Shi d, * a
Department of Applied Psychology, Hunan University of Chinese Medicine, Changsha, Hunan, China The Diagnosis of Chinese Medicine of the Key Laboratory of Hunan Province, Changsha, China Department of Child Psychiatry of Shenzhen Kangning Hospital, Shenzhen Mental Health Center, Shenzhen Institute of Mental Health, Shenzhen Key Laboratory of Mental Health, Shenzhen, China d School of Education, Hunan University of Science and Technology, Xiangtan, Hunan, China b c
A R T I C L E I N F O
A B S T R A C T :
Keywords: Childhood maltreatment Event-related potential Facial emotion processing Negative schizotypy P100 N170
Childhood maltreatment (CM) is a factor of risk for psychosis and is associated with alterations in facial emotion processing.Negative symptoms of schizophrenia-spectrum disorders are associated with deficits in facial emotion processing, but research findings on schizotypy are mixed. This study examined the early stage of facial emotion processing in young adults with high levels of negative schizotypy (NS) and explored the impact of childhood maltreatment. On the basis of the Social and Physical Anhedonia subscales of the Chapman Psychosis-Proneness Scales, a total of 74 high-NS and 52 low-NS individuals were recruited to complete the Childhood Trauma Questionnaire and the dot-probe task. The P100 and N170 components of event-related potentials were measured to assess the processing of four facial expressions of emotion. The high-NS group showed significantly reduced P100 amplitudes for all facial expressions. Angry and fearful expressions elicited larger N170 amplitudes than disgusted and happy expressions. Happy expressions elicited shorter N170 latencies than disgusted ex pressions. Compared to the high-NS group without CM, the high-NS group with CM had a longer latency of P100. Individuals with high NS, compared to individuals with low NS, have impaired fundamental visual processing, but intact processing of facial figurations. Childhood maltreatment may be a factor responsible for the patho logical state of the visual pathway in high NS group.
1. Introduction Growing evidence suggests impaired processing of facial emotions is a stable characteristic of schizophrenia (Addington and Addington, 1998; Barkl et al., 2014), and occurs in clinically and genetically high-risk individuals (Kohler et al., 2014; Lee et al., 2015; Li et al., 2010). Schizotypy reflects an underlying predisposition for schizo phrenia (Kwapil and Barrantes-Vidal, 2015), and includes dimensions of positive and negative symptoms (Ettinger et al., 2015; Kwapil et al., 2013). Research findings on facial emotion processing among individuals with schizotypal traits are mixed. Facial emotion processing by in dividuals with schizotypal traits is significantly poorer (Brown and Cohen, 2010; Statucka and Walder, 2017) than controls (Morrison et al.,
2013; Statucka and Walder, 2017), and significant between-group dif ferences have been reported primarily for processing neutral, but not emotional expressions (Brown and Cohen, 2010; Statucka and Walder, 2017). Yet other studies have not found poor performance in recognition of facial emotions among schizotypes than controls (Jahshan and Sergi, 2007; Toomey and Schuldberg, 1995; Toomey et al., 1999). Positive schizotypy (PS) is associated with a specific type of error, namely, incorrectly labeling angry expressions as happy, unlike negative schizotypy (NS), which is associated with poor facial emotion recogni tion (Bentin et al., 1996; Caharel et al., 2007; Earls et al., 2016; Joyce and Rossion, 2005; Morrison et al., 2013). Individuals with positive schizotypal traits pay less attention in the early stage of processing social rejection (Morrison et al., 2013) than those with negative schizotypal traits (Premkumar et al., 2015), yet both groups perceive facial
* Corresponding author. School of Education, Hunan University of Science and Technology, Xiangtan, 411201, Hunan, China. ** Corresponding author. E-mail addresses: [email protected] (J. Liu), [email protected] (L. Shi). https://doi.org/10.1016/j.neuropsychologia.2019.107215 Received 29 June 2019; Received in revised form 26 September 2019; Accepted 26 September 2019 Available online 28 September 2019 0028-3932/© 2019 Elsevier Ltd. All rights reserved.
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expressions of emotion as negative (Brown and Cohen, 2010). The re sults of research on the relationship between schizotypal traits and facial emotion processing are inconsistent, which might be related to how schizotypy is defined. Among patients with schizophrenia (Fett and Maat, 2013; Kohler et al., 2003; Romero-Ferreiro et al., 2016) and their non-psychotic siblings (Fett and Maat, 2013), deficits in facial emotion recognition were notably correlated with more severe negative symptoms. Childhood maltreatment (CM) is a factor of risk for psychosis (Varese et al., 2012), but how maltreatment alters neurocognitive systems that increase vulnerability to mental-health problems is unclear (McCrory and Viding, 2015), atypical processing of emotions has been implicated. CM influences sensitivity to stress and subsequent emotional reactivity to day-to-day stressors involving the processing of potential threats (Glaser et al., 2006; Myin-Germeys et al., 2001, 2005). Children and adults who have experienced maltreatment show preferential attention to threatening information (Pollak and Tolley-Schell, 2003; Shackman et al., 2007), perceive threats despite limited information, and do not easily shift their attention away from facial expressions of threat (Pollak and Tolley-Schell, 2003). Thus, CM may determine how emotional stimuli are processed (e.g., attending to negative stimuli and ignoring positive stimuli). Heightened reactivity to stressors, especially negative cues, is an essential feature of persons with schizophrenia (Linszen et al., 1997; Melle et al., 1996). An fMRI study reported an association of CM among patients with schizophrenia with greater differentiation in brain responses to negative and positive facial emotions (Aas et al., 2017). CM might alter later connections between stress-mediating brain circuits (e. g., in the amygdala and the posterior cingulate/precuneus region), thereby affecting social cognition in schizophrenia (Cancel et al., 2017). Thus, the impact of CM on facial emotion processing in schizophrenia should be examined further. Early processing of facial emotions consists of two stages associated with two event-related potentials (ERPs): the P100 (a positive potential occurring between 80 and 120 ms after stimulus onset), and the N170 (a negative face-specific deflection occurring 165–170 ms post-stimulus). The P100, which is measured over the occipital lobe, is involved in the early processing of visual stimuli. P100 amplitudes are larger for faces than objects, and therefore, are probably modulated by emotional facial expressions (Biotti et al., 2017; van Heijnsbergen et al., 2007). The results of studies on facial emotion processing in patients with schizo phrenia are mixed. Normal processing has been reported at the P100 stage (Jung et al., 2012; Lee et al., 2010), while a meta-analysis found patients had smaller P100 amplitudes to expressions or smaller P100 amplitudes to neutral and happy expressions, but no changes in response to fearful expressions (Earls et al., 2016). The N170, a posterior tem poral negative peak, produces the largest response to facial stimuli, which is more pronounced over the right hemisphere (Heisz et al., 2006). However, whether emotional valence affects N170 amplitudes and latencies is unclear (Vuilleumier and Pourtois, 2007). Many studies have found patients with schizophrenia have attenuated N170 ERP re sponses to facial stimuli (Campanella et al., 2006; Feuerriegel et al., 2015; McCleery et al., 2015; Wynn et al., 2013), and N170 deficits have been reported in relatives of schizophrenic patients (Ibanez et al., 2012). In conclusion, the results of studies on ERP-induced processing of facial emotions in persons with schizophrenia are inconsistent, which might be caused by illness-related factors, (e.g., inpatient treatment, age at onset, antipsychotics, and symptom severity) (Kohler et al., 2010). A few studies have reported reduced N170 amplitudes in response to faces by individuals with high levels of schizotypal traits (Batty et al., 2014; Brooks and Brenner, 2017), although early sensory processing of faces (P100) appeared intact (Batty et al., 2014). Since childhood maltreatment is a factor of risk for psychosis, which affects individuals’ emotional responses, and negative schizotypy characteristics, such as anhedonia, have a strong association with defi cits in facial emotion perception. Social anhedonia is a core attribute of individuals who are vulnerable to psychosis (Horan et al., 2007; Meehl,
Table 1 Demographic characteristics and clinical information.
Age Gender(M/F) CTQ-SF scores Emotional abuse Physical abuse Sexual abuse Emotional neglect Physical neglect PAS SAS Negative schizotypy
t/χ 2
p
1.20
0.958 0.95
0.34 0.33
2.82 2.24 1.59 4.83 2.80 3.79 3.09 4.72
0.315 0.152 0.460 0.567 1.323 9.18 9.66 13.81
0.753 0.879 0.647 0.572 0.188 0.000 0.000 0.000
High NS group (n ¼ 74)
Low NS group (n ¼ 52)
Mean
SD
Mean
SD
18.85 32/42
0.77
19.02 18/34
8.18 6.51 5.95 11.11 8.64 19.00 14.53 33.53
2.70 2.35 1.94 4.46 3.27 6.08 5.78 8.19
8.02 6.58 6.10 10.63 7.90 10.27 6.04 16.10
Note: NS ¼ negative schizotypy; CTQ¼ Childhood Trauma Questionnaire; SAS ¼ the Chapman Social; Anhedonia Scale; PAS ¼ the Chapman Physical Anhedonia Scale.
2017), and it predicts the onset of schizophrenia-spectrum disorders (Kwapil, 1998), therefore, it is necessary to explore the neural mecha nisms of abnormal facial emotion perception in individuals with high negative schizotypy (NS) and examine the impact of childhood maltreatment. We hypothesized that: (1) the early visual processing deficits (reduced P100 and N170 amplitudes) found in schizophrenia can be extended to individuals with higher levels of NS; and (2) Child hood maltreatment impacts the early stage of facial emotion processing in individuals with high NS. 2. Methods and materials 2.1. Participants During 2015–2017, three cross-sectional surveys were conducted with a convenience sample of first-year college students. The total effective number of completed questionnaires was 4902. A total of 300 students were identified as potential participants, of which 126 were randomly selected as participants. Cut-off scores for assignment to groups were according to the method by Wang et al. (2018). Based on students’ scores on the revised Social Anhedonia and Physical Anhe donia scales of the Chapman Psychosis-Proneness Scales, we divided the participants into two groups: the high-NS group (NS scores �23, n ¼ 74) and low-NS group (NS scores< 23, n ¼ 52) (Wang et al., 2018). The participants reported no history of psychiatric or neurological disorders when they were assessed using the Structured Clinical Interview for the Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition. Gender, age, and the scores on the Childhood Trauma Questionnaire-Short Form were matched in the two groups. Table 1 presents participants’ demographic and clinical characteristics. All participants were right-handed with normal or corrected to normal sight. Ten participants with invalid ERP data (e.g., excessive eye and head movements) were excluded from the analysis (Huffmeijer et al., 2014). The Ethical Committee of the Second Hospital Affiliated to Hunan University of Chinese Medicine approved the study. After explaining the study, we obtained participants’ written informed consent. They received financial compensation after completing all the tasks. 2.2. Measures 2.2.1. Chapman Psychosis-Proneness Scales (CPPS) All participants completed the four scales of the CPPS: the revised Social Anhedonia scale (RSAS) captures loss of interest in social re lationships, withdrawal, and/or inability to derive pleasure from inter personal relationships (Eckblad et al., 1982); the revised Physical Anhedonia scale (RPAS) measures failure to derive pleasure from 2
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Fig. 1. A trial sequence of the visual dot-probe task.
previously enjoyable stimuli (Chapman et al., 1976); the Magical Idea tion scale (MIS) assesses sub-clinical delusions and causation beliefs in personal influence over external events (Eckblad and Chapman, 1983); and the Perceptual Aberration scale (PAS) measures abnormal bodily perceptions (Chapman et al., 1978). The first two scales measure the negative dimension of schizotypy and the latter two measure the posi tive dimension of schizotypy. Participants’ responses to the RSAS and RPAS are reported in this study.
2.2.4. Electrophysiological recordings and data analysis Continuous electroencephalogram(EEG) activity was recorded using a Net Amps 300 high-impedance EEG amplifier (NetAmps 30.0, Elec trical Geodesics Inc. [EGI], Eugene, OR), with a 64-channel HydroCel Geodesic Sensor Net and a sampling rate of 500 Hz. Impedances were maintained below 50 kΩ during data collection, as recommended for this system (Ferree et al., 2001). All electrodes were manually refer enced to the vertex sensor Cz (set by EGI) and re-referenced off-line to the average electrodes. Off-line EEG data for extracting ERPs were analyzed using MATLAB (Mathworks Inc., Natick, MA) and EEGLAB. The continuous EEG was digitally filtered using a low pass of 30 Hz and a high pass of 0.1 Hz. EEG data were segmented into 1200-ms epochs, from 200 ms prior to the stimulus to 1000 ms after the stimulus. EEG artifacts caused by eye movements and blinks were removed through independent component analysis. Recording segments with more than 10 non-functional chan nels were rejected. These channels were replaced using spherical interpolation based on the given trial’s remaining sensors. The grand averages of the ERP waveforms were computed using the epochs for each stimulus type, yielding ERP waveforms for four condi tions: happy, angry, fearful, and disgusted. The amplitude and latency of the ERP components were measured as either the most positive or most negative data point in the specified latency window: P100, at the Oz, O1, and O2 electrode positions within an 80–170-ms window post-stimulus; and N170, at the P1, P7, and P9 (left hemisphere) and P2, P8, and P10 (right hemisphere) electrode positions, within a 150–200-ms window post-stimulus.
2.2.2. The Childhood Trauma Questionnaire-Short Form (CTQ-SF) Childhood maltreatment was evaluated using the Chinese version of the CTQ-SF, which showed good internal consistency and test-retest reliability in a sample of Chinese adolescents (Zhao et al., 2005). The 28-item CTQ-SF contains five subscales assessing different types of CM: emotional abuse, physical abuse, sexual abuse, emotional neglect, and physical neglect. Each item is rated on a 5-point ordinal scale from 1 (never true) to 5 (always true); seven items are reversed scored. Each subscale score ranges from 5 to 25 points and the total score ranges from 25 to 125 points; higher scores indicate more severe maltreatment during childhood. 2.2.3. Facial stimuli for the dot-probe task The dot probe task measures attentional biases induced by emotional and non-emotional stimuli (MacLeod et al., 1986). The dot-probe task was used to examine the neural mechanisms of early processing of facial emotions by individuals with high NS using ERP. Facial stimuli were chosen from the Chinese picture collection of emotional faces from the Institute of Psychology of the Chinese Academy of Sciences. In all, 54 neutral, 54 happy, and 54 negative expressions (18 angry, 18 fearful, and 18 disgusted expressions) were selected; half of them were male faces and half were female faces. The study consisted of 648 trials with 3 blocks; each block had 216 trials. Each trial began with a 500 ms fixation in the center of a screen, followed by a pair of emotional and neutral faces for 800 ms. Immediately following the offset of the faces, a dot probe (*) was presented in the same position as one of the two faces for 2000 ms. Participants were instructed to judge the side on which the dot had appeared and to indicate the correct response using a response box. They were exposed to one of two conditions on each trial: “congruent” trial—the facial expression of emotion and probe appeared on the same side or the “incongruent” trial—the probe appeared in a different loca tion from the facial expression. The experimental paradigm diagram see Fig. 1.
2.3. Statistical analysis Demographic data and participants’ scores on the self-report mea sures are presented. Data are presented as mean � standard deviation (SD). Age distributions and scores on the scales were analyzed using independent sample t-tests, and gender was analyzed by the chi-square test. We analyzed accuracy and reaction times (RTs) with a 2 � 2 � 4 repeated-measures design using multivariate analyses of variance (MANOVA) with group (high NS vs. low NS) as a between-subjects factor. Congruency (incongruent vs. congruent) and type of emotion (disgusted, fearful, angry, and happy) were within-subject factors. Repeated-measures ANOVAs were used to analyze potential differences in the P100 amplitudes and latencies with group (low NS vs. high NS) as a between-subjects factor, and type of emotion (happy, angry, fearful, and disgusted) and electrodes (O1, Oz, and O2) as within-subject factors. 3
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Fig. 2. Grand average ERPs elicited by emotional (angry, disgust, fear and happy) expressions at O1, O2 and Oz sites in high NS group and low NS group (A), along with scalp topographies of the P100 component (80–150 ms) in high NS group and low NS group, displaying a maximum at occipital electrodes (B).
4
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Fig. 3. Grand average ERPs elicited by emotional (angry, disgust, fear and happy) expressions in bilateral occipital temporal sites in high NS group and low NS group (A), along with scalp topographies of the N170 component (120–270 ms) in high NS group and low NS group, displaying a maximum at occipital electrodes (B).
Repeated-measures ANOVAs were used to analyze group (high NS vs. low NS) as a between-subjects factor and type of emotion (happy, angry, fearful, and disgusted) and hemisphere (right vs. left) as within-subject factors to examine differences in the N170 amplitudes and latencies. The Greenhouse-Geisser epsilon value was calculated when data from the repeated-measures analyses did not pass the sphericity test. Statistical significance for all tests was set at p < 0.05. SPSS 18.0 (IBM, Armonk,
NY) was used for all statistical analyses. 3. Results 3.1. Participants’ characteristics No significant differences were found between participants’ gender, 5
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Table 2 Peak latencies and amplitudes for the P100 and N170 components for each emotional face according to group (high NS vs low NS). The amplitudes and latencies of N170 are averaged across hemisphere. Data are mean � SD values. Group High NS group
Type of emotion
P1 Amplitude
N170 Amplitude
N170 Latency
O1
Oz
O2
O1
Oz
O2
Left
Right
Left
Right
angry
2.40 (2.41) 2.61 (2.37) 2.30 (2.30) 2.41 (2.16) 3.42 (2.49) 3.44 (2.40) 3.32 (2.63) 3.34 (2.31)
2.51 (2.62) 2.74 (2.42) 2.37 (2.46) 2.58 (2.29) 3.66 (2.59) 3.64 (2.47) 3.60 (2.74) 3.58 (2.48)
2.86 (2.51) 3.03 (2.51) 2.75 (2.53) 2.85 (2.32) 4.33 (2.66) 3.98 (2.45) 3.92 (2.80) 4.04 (2.57)
134.12 (23.77) 137.83 (23.55) 134.00 (23.73) 136.12 (22.92) 141.83 (18.49) 137.25 (20.75) 141.58 (19.54) 140.75 (19.54)
132.64 (26.69) 134.76 (24.68) 130.29 (27.28) 135.47 (26.34) 141.75 (19.14) 137.92 (19.05) 142.17 (19.39) 139.25 (20.51)
134.65 (24.91) 134.35 (23.12) 136.29 (23.43) 136.29 (24.56) 140.67 (20.22) 136.00 (18.19) 141.67 (17.44) 141.92 (17.09)
5.24 (2.99) 4.70 (2.73) 5.05 (2.74) 4.87 (2.70) 4.87 (2.36) 4.77 (2.57) 4.93 (2.59) 4.74 (2.42)
5.01 (3.00) 4.66 (2.87) 4.98 (2.72) 4.76 (2.64) 4.83 (2.99) 4.71 (3.01) 4.75 (3.21) 4.62 (3.06)
196.24 (19.09) 199.24 (16.38) 196.96 (17.31) 196.63 (14.82) 196.69 (15.07) 199.39 (17.21) 196.97 (20.98) 195.22 (17.31)
193.10 (18.56) 193.31 (18.12) 192.43 (17.82) 193.22 (18.75) 198.75 (16.83) 199.19 (16.13) 198.75 (17.84) 197.39 (17.68)
disgust fear happy
Low NS group
angry disgust fear happy
P1 Latency
Note: NS ¼ negative schizotypy; Left ¼ ERP average of channels P1, P7 and P9; Right ¼ ERP average of channels P2, P8 and P10.
age, or CTQ total and subscale scores. The high-NS group’s scores were significantly higher than the low-NS group on the RSAC and RPAS of the CPPS (Table 1).
statistically significant. The P100 had a significantly larger amplitude in the low-NS group than the high-NS group. Post-hoc analysis revealed larger P100 amplitudes at the right (O2) electrode compared to the left (O1) (p ¼ 0.001) or the midline (Oz) electrodes (p ¼ 0.001). No signifi cant effects were found for P100 latencies. The results of the MANOVA for the N170 amplitude showed a main effect of type of emotion (F(3, 114) ¼ 4.007, p ¼ 0.013, η2p ¼ 0.035), but no main effect of group (F(1,114) ¼ 0.081, p ¼ 0.776, η2p ¼ 0.001) or hemi sphere (F(1,114) ¼ 0.206, p ¼ 0.651, η2p ¼ 0.002). No interactions were significant. Post-hoc analysis showed angry facial expressions elicited a larger N170 amplitude than did disgusted (p ¼ 0.022) or happy ex pressions (p ¼ 0.001). Fearful facial expressions elicited a larger N170 amplitude than disgusted (p ¼ 0.036) or happy expressions (p ¼ 0.023). A main effect of type of emotion on the N170 latency (F(3, 114) ¼ 2.617, p ¼ 0.061, η2p ¼ 0.022) and a trend toward an interaction between group and hemisphere (F(1, 114) ¼ 3.768, p ¼ 0.055, η2p ¼ 0.032) were found. No other effects were significant. Post-hoc analysis revealed that happy facial expressions elicited a shorter N170 latency than disgusted ex pressions (p ¼ 0.001). Simple effects analysis revealed that the N170 latency in the high-NS group was shorter than that of the low-NS group in the right hemisphere, with a marginal statistical difference (p ¼ 0.08).
3.2. Behavioral data There was a main effect of congruency (F(1,123) ¼ 12.16, p ¼ 0.001
η2p ¼ 0.09) on RTs. Participants reactions were significantly quicker for incongruent trials than congruent trials. No other effects were found for RTs and no significant effects were found for accuracy (Ps > 0.05). 3.3. ERP data Grand mean ERPs to facial emotion and the according scalp topog raphies were illustrated separately for the P100 component at occipital sites (O1, O2, Oz) (see Fig. 2) and N170 component at bilateral occipital temporal sites (see Fig. 3) for high- and low-NS groups. Table 2 showed the P100 and N170 latencies and amplitudes for the high- and low-NS groups. The analyses revealed main effects of group (F(1,114) ¼ 7.20, p ¼ 0.008, η2p ¼ 0.059) and electrode site (F(2, 114) ¼ 10.421, p < 0.001, η2p ¼ 0.084), but no main effect of emotion (F(3,114) ¼ 0.779, p ¼ 0.497, η2p ¼ 0.007) on the P100 amplitude. No interaction effects were
Table 3 Peak latencies and amplitudes for the P100 components for each emotional face according to group (high NS with CM, high NS without CM, low NS with CM, low NS without CM). Data are mean � SD values. Group High NS with CM group
High NS without CM group
Low NS with CM group
Low NS without CM group
Type of emotion angry disgust fear happy angry disgust fear happy angry disgust fear happy angry disgust fear happy
P1 Amplitude
P1 Latency
O2
Oz
O1
O2
Oz
O1
2.74(2.31) 2.78(2.38) 2.76(2.29) 2.95(2.27) 2.99(2.73) 3.29(2.66) 2.75(2.79) 2.75(2.41) 3.99(2.89) 3.81(2.75) 3.19(3.02) 3.68(2.94) 4.64(2.44) 4.14(2.18) 4.60(2.44) 4.38(2.19)
2.15(2.48) 2.44(2.16) 2.40(2.35) 2.68(2.25) 2.89(2.74) 3.05(2.67) 2.34(2.61) 2.75(2.41) 3.16(2.54) 3.53(2.70) 2.85(2.83) 3.11(2.70) 4.12(2.60) 3.74(2.28) 4.28(2.52) 4.02(2.23)
2.12(2.39) 2.32(2.22) 2.22(2.11) 2.38(1.92) 2.70(2.42) 2.92(2.51) 2.40(2.51) 2.47(2.36) 2.76(2.29) 2.95(2.45) 2.47(2.34) 2.75(2.36) 4.01(2.55) 3.89(2.30) 4.11(2.68) 3.89(2.16)
135.31(27.35) 138.40(23.08) 140.11(24.28) 140.00(25.19) 133.94(22.45) 130.01(22.72) 132.24(22.13) 132.36(23.63) 136.52(20.16) 133.04(20.26) 136.70(17.67) 137.91(19.81) 144.48(19.91) 138.72(15.99) 146.24(16.25) 145.60(13.52)
132.34(29.32) 140.80(23.32) 132.69(30.08) 138.40(28.25) 132.97(24.04) 128.36(24.81) 127.76(24.16) 132.36(24.19) 138.61(19.62) 132.52(20.58) 136.70(21.53) 134.26(22.33) 144.64(18.61) 142.88(16.39) 147.20(16.00) 143.84(17.91)
137.60(23.77) 141.49(21.19) 139.77(21.82) 142.51(20.90) 130.42(23.58) 133.94(25.58) 127.88(24.46) 129.33(23.32) 138.96(19.00) 132.00(22.40) 138.43(21.77) 136.35(20.11) 144.48(17.97) 142.08(18.23) 144.48(17.18) 144.80(18.48)
Notes: NS ¼ negative schizotypy; CM ¼ childhood maltreatment. 6
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individuals during a facial emotion-processing task, to confirm prior findings on facial emotion processing in patients with schizophrenia. We evaluated individuals with high NS, which yielded more narrowly focused findings, and examined the impact of childhood maltreatment on their facial emotion processing. The ERP data demonstrated that all facial expressions elicited fewer positive P100 amplitudes in the high-NS group than the low-NS group; no differences in N170 amplitudes between the two groups were found. P100 indicates early visual processing (Allison et al., 1999) and face-specific categorization (Herrmann et al., 2005a, 2005b), and N170 indicates the visual processing of facial structures (Bentin et al., 1999), therefore, our results suggest impaired fundamental visual processing in high-NS individuals, although the processing of facial figurations ap pears to be intact. The decreased P100 amplitudes in the high-NS group is similar to P100 deficits found in patients with schizophrenia (Caharel et al., 2007; Campanella et al., 2006) and persons at-risk for schizo phrenia during facial processing (Wolwer et al., 2012). These findings suggest that deficits in facial emotion processing precede the onset of the initial psychotic episode, and therefore, may be a vulnerability marker for schizophrenia. Furthermore, P100 amplitude deficits in processing facial expressions are independent of emotions (happy, angry, disgusted, or fearful), indicating these deficits are not emotion specific in high-NS individuals. N170 deficits (i.e., reduced amplitude and delayed latency) in patients with schizophrenia during facial emotion processing have been reported (Herrmann et al., 2004; Johnston et al., 2005; Turetsky et al., 2007), but we did not find this or a similar deficit among in dividuals with high NS. This is most likely because deficits in high-NS persons are typically visuo-sensory specific, as reflected by P100 dif ferences between individuals with high and low NS, and less likely to be face-specific. The main effect of emotion was significant for N170 am plitudes, with angry and fearful expressions eliciting larger amplitudes than disgusted or happy expressions. No difference was found in the magnitude of the N170 amplitude priming effect for happy and disgusted faces. These findings suggest that affect modulates N170 processing, such that responses to faces with greater affective salience are enhanced compared to faces with less affective salience, as reported in previous studies (Ashley et al., 2004; Batty and Taylor, 2003; Blau et al., 2007). When examining the effect of childhood maltreatment on the early stage of facial emotion processing, we found that, compared to the high-NS group without CM, the high-NS group with CM had a longer latency of P100. It is well known that a prolonged of P100 latency in dicates a dysfunction of the visual pathway (Cant et al., 1978). There fore, childhood maltreatment may be a factor responsible for the pathological state of the visual pathway in high NS group. This study supports hemispheric specialization of facial emotion processing. The P100 amplitude was significantly larger over the right hemisphere compared to the left hemisphere and midline electrodes. For the N170 latency, a trend was found toward an interaction between group and hemisphere, with earlier responses over the right rather than the left hemisphere in the high-NS group. With regard to the N170 amplitude, we did not find lateralization effects as reported previously (Bentin et al., 1999; Joyce and Rossion, 2005); nor did some other studies find significant differences between the left and right sides (Botzel et al., 1995; Eimer, 2000; Rossion et al., 2000). Among the study’s limitations, the first is that our sample consisted of undergraduates students, which might decrease the generalizability of the findings to populations outside university settings. Second, we used self-report questionnaires to assess schizotypy and childhood maltreatment. Ecologically valid sampling methods might be more appropriate. Third, the effect of depression on facial emotion processing should have been addressed given the evidence that individuals with depression are poor at recognizing facial expressions of emotion, and depression is common in schizotypy. Depressive symptoms, including their effects on outcomes and ways to control for them, are important issues for future research in this area. In conclusion, our findings suggest individuals with high NS have
Table 4 The amplitudes and latencies of N170 averaged across hemisphere for each emotional face according to group (high NS with CM, high NS without CM, low NS with CM, low NS without CM). Data are mean � SD values. Group
Type of emotion
N170 Amplitude
N170 Latency
Left
Right
Left
Right
High NS with CM group
angry
5.38 (2.74) 5.07 (2.56) 5.35 (2.44) 5.18 (2.65) 5.09 (3.27) 4.30 (2.89) 4.72 (3.03) 4.54 (2.75) 5.61 (2.36) 5.20 (2.59) 5.63 (2.49) 5.43 (2.41) 4.19 (2.18) 4.38 (2.53) 4.29 (2.55) 4.10 (2.28)
5.46 (3.40) 5.22 (3.16) 5.34 (2.99) 5.13 (2.99) 4.53 (2.47) 4.07 (2.45) 4.61 (2.40) 4.38 (2.20) 5.49 (3.33) 5.06 (3.18) 5.39 (3.12) 5.29 (3.19) 4.22 (2.57) 4.39 (2.86) 4.17 (3.24) 4.01 (2.87)
196.04 (21.79) 200.65 (17.36) 196.95 (20.00) 195.89 (15.74) 196.44 (16.07) 195.07 (18.80) 196.97 (14.23) 197.41 (13.98) 193.51 (14.01) 193.10 (15.29) 191.42 (20.68) 199.36 (18.78) 199.63 (15.69) 205.17 (17.12) 202.08 (20.33) 199.36 (18.78)
192.50 (18.23) 191.66 (17.56) 192.23 (16.84) 194.36 (15.89) 193.74 (19.16) 197.41 (13.98) 192.65 (19.07) 192.00 (21.57) 197.80 (13.47) 197.68 (13.58) 195.77 (15.48) 193.80 (13.87) 199.63 (19.66) 200.59 (18.33) 201.49 (19.67) 200.69 (20.29)
disgust fear happy
High NS without CM group
angry disgust fear happy
Low NS with CM group
angry disgust fear happy
Low NS without CM group
angry disgust fear happy
Notes: NS ¼ negative schizotypy; CM ¼ childhood maltreatment.
3.4. The influence of CM on P100 and N170 amplitudes and latencies In order to explore the influence of CM on the early stage of facial emotion processing, the participants were further divided into four groups: high-NS group with CM, high-NS group without CM, low-NS group with CM, low-NS group without CM. Table 3 and Table 4 shows the P100 and N170 latencies and amplitudes for the four groups. Simi larly, repeated-measures ANOVAs were used to analyze potential dif ferences in the P100/and N170 amplitudes and latencies with group (high NS with CM, high NS without CM, low NS with CM, low NS without CM) as a between-subjects factor, and type of emotion (happy, angry, fearful, and disgusted) and electrodes (O1, Oz, and O2)/and hemisphere (right vs. left) as within-subject factors, respectively. The analyses revealed only a main effect of group on the P100 latency (F(3, 2 112) ¼ 3.301, p ¼ 0.023, ηp ¼ 0.081) and amplitude (F(3, 112) ¼ 3.332, 2 p ¼ 0.022, ηp ¼ 0.082). No main effect of group on N170 latency (F(3, 2 112) ¼ 1.288, p ¼ 0.282, ηp ¼ 0.033) and amplitude (F(3, 112) ¼ 1.516, 2 p ¼ 0.214, ηp ¼ 0.039). No interaction effects were statistically signifi cant. Post hoc tests revealed that P100 amplitude was significantly larger in the low-NS group without CM compared with the high-NS group with CM (p ¼ 0.003), in the low-NS group without CM compared to the highNS group without CM (p ¼ 0.014). The P100 latency was significantly shorter in the high-NS group without CM compared to the low-NS group without CM (p ¼ 0.003). The high-NS group without CM had shorter P100 latency compared to the high-NS group with CM, with a marginal statistical difference (p ¼ 0.063). 4. Discussion This study compared the brain activity of high-NS with low-NS 7
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impaired fundamental visual processing, but intact processing of facial figurations. Childhood maltreatment may be a factor responsible for the pathological state of the visual pathway in high NS group.
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CRediT authorship contribution statement Jingbo Gong: Writing - original draft, Writing - review & editing. Jianbo Liu: Conceptualization, Methodology, Writing - review & edit ing. Lizhi Shangguan: Investigation, Data curation. Qin Zhang: Investigation, Data curation. Zhu Peng: Investigation, Data curation. Zun Li: Investigation, Data curation. Chuwen Chen: Investigation, Data curation. Lijuan Shi: Formal analysis. Acknowledgements This work was supported by grants from Humanities and Social Science Fund of Ministry of Education(18YJC190004),the Natural Sci ence Foundation of Hunan Province (2017JJ3240), and the Hunan Ed ucation Department Excellent Youth Fund (18B219). Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi. org/10.1016/j.neuropsychologia.2019.107215. References Aas, M., Kauppi, K., Brandt, C.L., Tesli, M., Kaufmann, T., Steen, N.E., Agartz, I., Westlye, L.T., Andreassen, O.A., Melle, I., 2017. Childhood trauma is associated with increased brain responses to emotionally negative as compared with positive faces in patients with psychotic disorders. Psychol. Med. 47 (4), 669–679. Addington, J., Addington, D., 1998. Facial affect recognition and information processing in schizophrenia and bipolar disorder. Schizophr. Res. 32 (3), 171–181. Allison, T., Puce, A., Spencer, D.D., McCarthy, G., 1999. Electrophysiological studies of human face perception. I: potentials generated in occipitotemporal cortex by face and non-face stimuli (New York, N.Y. : 1991). Cerebr. Cortex 9 (5), 415–430. Ashley, V., Vuilleumier, P., Swick, D., 2004. Time course and specificity of event-related potentials to emotional expressions. Neuroreport 15 (1), 211–216. Barkl, S.J., Lah, S., Harris, A.W., Williams, L.M., 2014. Facial emotion identification in early-onset and first-episode psychosis: a systematic review with meta-analysis. Schizophr. Res. 159 (1), 62–69. Batty, M., Taylor, M.J., 2003. Early processing of the six basic facial emotional expressions. Brain research. Cogn. Brain Res. 17 (3), 613–620. Batty, R.A., Francis, A.J., Innes-Brown, H., Joshua, N.R., Rossell, S.L., 2014. Neurophysiological correlates of configural face processing in schizotypy. Front. Psychiatry 5, 101. Bentin, S., Allison, T., Puce, A., Perez, E., McCarthy, G., 1996. Electrophysiological studies of face perception in humans. J. Cogn. Neurosci. 8 (6), 551–565. Bentin, S., Deouell, L.Y., Soroker, N., 1999. Selective visual streaming in face recognition: evidence from developmental prosopagnosia. Neuroreport 10 (4), 823–827. Biotti, F., Gray, K.L.H., Cook, R., 2017. Impaired body perception in developmental prosopagnosia. Cortex; a journal devoted to the study of the nervous system and behavior, vol. 93, pp. 41–49. Blau, V.C., Maurer, U., Tottenham, N., McCandliss, B.D., 2007. The face-specific N170 component is modulated by emotional facial expression. Behav. Brain Funct. : BBF 3, 7. Botzel, K., Schulze, S., Stodieck, S.R., 1995. Scalp topography and analysis of intracranial sources of face-evoked potentials. Exp. Brain Res. 104 (1), 135–143. Brooks, G.A., Brenner, C.A., 2017. Is there a common vulnerability in cannabis phenomenology and schizotypy? The role of the N170 ERP. Schizophr. Res.. Brown, L.A., Cohen, A.S., 2010. Facial emotion recognition in schizotypy: the role of accuracy and social cognitive bias. J. Int. Neuropsychol. Soc. : JINS 16 (3), 474–483. Caharel, S., Bernard, C., Thibaut, F., Haouzir, S., Di Maggio-Clozel, C., Allio, G., Fouldrin, G., Petit, M., Lalonde, R., Rebai, M., 2007. The effects of familiarity and emotional expression on face processing examined by ERPs in patients with schizophrenia. Schizophr. Res. 95 (1–3), 186–196. Campanella, S., Montedoro, C., Streel, E., Verbanck, P., Rosier, V., 2006. Early visual components (P100, N170) are disrupted in chronic schizophrenic patients: an eventrelated potentials study. Neurophysiologie clinique ¼ Clinical neurophysiologyNeurophysiol. Clinique Clin. Neurophysiol. 36 (2), 71–78. Cancel, A., Comte, M., Boutet, C., Schneider, F.C., Rousseau, P.F., Boukezzi, S., Gay, A., Sigaud, T., Massoubre, C., Berna, F., Zendjidjian, X.Y., Azorin, J.M., Blin, O., Fakra, E., 2017. Childhood trauma and emotional processing circuits in schizophrenia: a functional connectivity study. Schizophr. Res. 184, 69–72. Cant, B., Hume, A.L., Shaw, N., 1978. Effects of luminence on the pattern visual evoked potential in multiple sclerosis. Electroencephalogr. Clin. Neurophysiol. 45 (4), 496–504.
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Childhood maltreatment impacts the early stage of facial emotion processing in young adults with negative schizotypy Jingbo Gong a, b, Jianbo Liu c, **, Lizhi Shangguan a, Qin Zhang a, Zhu Peng a, Zun Li a, Chuwen Chen a, Lijuan Shi d, * a
Department of Applied Psychology, Hunan University of Chinese Medicine, Changsha, Hunan, China The Diagnosis of Chinese Medicine of the Key Laboratory of Hunan Province, Changsha, China Department of Child Psychiatry of Shenzhen Kangning Hospital, Shenzhen Mental Health Center, Shenzhen Institute of Mental Health, Shenzhen Key Laboratory of Mental Health, Shenzhen, China d School of Education, Hunan University of Science and Technology, Xiangtan, Hunan, China b c
A R T I C L E I N F O
A B S T R A C T :
Keywords: Childhood maltreatment Event-related potential Facial emotion processing Negative schizotypy P100 N170
Childhood maltreatment (CM) is a factor of risk for psychosis and is associated with alterations in facial emotion processing.Negative symptoms of schizophrenia-spectrum disorders are associated with deficits in facial emotion processing, but research findings on schizotypy are mixed. This study examined the early stage of facial emotion processing in young adults with high levels of negative schizotypy (NS) and explored the impact of childhood maltreatment. On the basis of the Social and Physical Anhedonia subscales of the Chapman Psychosis-Proneness Scales, a total of 74 high-NS and 52 low-NS individuals were recruited to complete the Childhood Trauma Questionnaire and the dot-probe task. The P100 and N170 components of event-related potentials were measured to assess the processing of four facial expressions of emotion. The high-NS group showed significantly reduced P100 amplitudes for all facial expressions. Angry and fearful expressions elicited larger N170 amplitudes than disgusted and happy expressions. Happy expressions elicited shorter N170 latencies than disgusted ex pressions. Compared to the high-NS group without CM, the high-NS group with CM had a longer latency of P100. Individuals with high NS, compared to individuals with low NS, have impaired fundamental visual processing, but intact processing of facial figurations. Childhood maltreatment may be a factor responsible for the patho logical state of the visual pathway in high NS group.
1. Introduction Growing evidence suggests impaired processing of facial emotions is a stable characteristic of schizophrenia (Addington and Addington, 1998; Barkl et al., 2014), and occurs in clinically and genetically high-risk individuals (Kohler et al., 2014; Lee et al., 2015; Li et al., 2010). Schizotypy reflects an underlying predisposition for schizo phrenia (Kwapil and Barrantes-Vidal, 2015), and includes dimensions of positive and negative symptoms (Ettinger et al., 2015; Kwapil et al., 2013). Research findings on facial emotion processing among individuals with schizotypal traits are mixed. Facial emotion processing by in dividuals with schizotypal traits is significantly poorer (Brown and Cohen, 2010; Statucka and Walder, 2017) than controls (Morrison et al.,
2013; Statucka and Walder, 2017), and significant between-group dif ferences have been reported primarily for processing neutral, but not emotional expressions (Brown and Cohen, 2010; Statucka and Walder, 2017). Yet other studies have not found poor performance in recognition of facial emotions among schizotypes than controls (Jahshan and Sergi, 2007; Toomey and Schuldberg, 1995; Toomey et al., 1999). Positive schizotypy (PS) is associated with a specific type of error, namely, incorrectly labeling angry expressions as happy, unlike negative schizotypy (NS), which is associated with poor facial emotion recogni tion (Bentin et al., 1996; Caharel et al., 2007; Earls et al., 2016; Joyce and Rossion, 2005; Morrison et al., 2013). Individuals with positive schizotypal traits pay less attention in the early stage of processing social rejection (Morrison et al., 2013) than those with negative schizotypal traits (Premkumar et al., 2015), yet both groups perceive facial
* Corresponding author. School of Education, Hunan University of Science and Technology, Xiangtan, 411201, Hunan, China. ** Corresponding author. E-mail addresses: [email protected] (J. Liu), [email protected] (L. Shi). https://doi.org/10.1016/j.neuropsychologia.2019.107215 Received 29 June 2019; Received in revised form 26 September 2019; Accepted 26 September 2019 Available online 28 September 2019 0028-3932/© 2019 Elsevier Ltd. All rights reserved.
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expressions of emotion as negative (Brown and Cohen, 2010). The re sults of research on the relationship between schizotypal traits and facial emotion processing are inconsistent, which might be related to how schizotypy is defined. Among patients with schizophrenia (Fett and Maat, 2013; Kohler et al., 2003; Romero-Ferreiro et al., 2016) and their non-psychotic siblings (Fett and Maat, 2013), deficits in facial emotion recognition were notably correlated with more severe negative symptoms. Childhood maltreatment (CM) is a factor of risk for psychosis (Varese et al., 2012), but how maltreatment alters neurocognitive systems that increase vulnerability to mental-health problems is unclear (McCrory and Viding, 2015), atypical processing of emotions has been implicated. CM influences sensitivity to stress and subsequent emotional reactivity to day-to-day stressors involving the processing of potential threats (Glaser et al., 2006; Myin-Germeys et al., 2001, 2005). Children and adults who have experienced maltreatment show preferential attention to threatening information (Pollak and Tolley-Schell, 2003; Shackman et al., 2007), perceive threats despite limited information, and do not easily shift their attention away from facial expressions of threat (Pollak and Tolley-Schell, 2003). Thus, CM may determine how emotional stimuli are processed (e.g., attending to negative stimuli and ignoring positive stimuli). Heightened reactivity to stressors, especially negative cues, is an essential feature of persons with schizophrenia (Linszen et al., 1997; Melle et al., 1996). An fMRI study reported an association of CM among patients with schizophrenia with greater differentiation in brain responses to negative and positive facial emotions (Aas et al., 2017). CM might alter later connections between stress-mediating brain circuits (e. g., in the amygdala and the posterior cingulate/precuneus region), thereby affecting social cognition in schizophrenia (Cancel et al., 2017). Thus, the impact of CM on facial emotion processing in schizophrenia should be examined further. Early processing of facial emotions consists of two stages associated with two event-related potentials (ERPs): the P100 (a positive potential occurring between 80 and 120 ms after stimulus onset), and the N170 (a negative face-specific deflection occurring 165–170 ms post-stimulus). The P100, which is measured over the occipital lobe, is involved in the early processing of visual stimuli. P100 amplitudes are larger for faces than objects, and therefore, are probably modulated by emotional facial expressions (Biotti et al., 2017; van Heijnsbergen et al., 2007). The results of studies on facial emotion processing in patients with schizo phrenia are mixed. Normal processing has been reported at the P100 stage (Jung et al., 2012; Lee et al., 2010), while a meta-analysis found patients had smaller P100 amplitudes to expressions or smaller P100 amplitudes to neutral and happy expressions, but no changes in response to fearful expressions (Earls et al., 2016). The N170, a posterior tem poral negative peak, produces the largest response to facial stimuli, which is more pronounced over the right hemisphere (Heisz et al., 2006). However, whether emotional valence affects N170 amplitudes and latencies is unclear (Vuilleumier and Pourtois, 2007). Many studies have found patients with schizophrenia have attenuated N170 ERP re sponses to facial stimuli (Campanella et al., 2006; Feuerriegel et al., 2015; McCleery et al., 2015; Wynn et al., 2013), and N170 deficits have been reported in relatives of schizophrenic patients (Ibanez et al., 2012). In conclusion, the results of studies on ERP-induced processing of facial emotions in persons with schizophrenia are inconsistent, which might be caused by illness-related factors, (e.g., inpatient treatment, age at onset, antipsychotics, and symptom severity) (Kohler et al., 2010). A few studies have reported reduced N170 amplitudes in response to faces by individuals with high levels of schizotypal traits (Batty et al., 2014; Brooks and Brenner, 2017), although early sensory processing of faces (P100) appeared intact (Batty et al., 2014). Since childhood maltreatment is a factor of risk for psychosis, which affects individuals’ emotional responses, and negative schizotypy characteristics, such as anhedonia, have a strong association with defi cits in facial emotion perception. Social anhedonia is a core attribute of individuals who are vulnerable to psychosis (Horan et al., 2007; Meehl,
Table 1 Demographic characteristics and clinical information.
Age Gender(M/F) CTQ-SF scores Emotional abuse Physical abuse Sexual abuse Emotional neglect Physical neglect PAS SAS Negative schizotypy
t/χ 2
p
1.20
0.958 0.95
0.34 0.33
2.82 2.24 1.59 4.83 2.80 3.79 3.09 4.72
0.315 0.152 0.460 0.567 1.323 9.18 9.66 13.81
0.753 0.879 0.647 0.572 0.188 0.000 0.000 0.000
High NS group (n ¼ 74)
Low NS group (n ¼ 52)
Mean
SD
Mean
SD
18.85 32/42
0.77
19.02 18/34
8.18 6.51 5.95 11.11 8.64 19.00 14.53 33.53
2.70 2.35 1.94 4.46 3.27 6.08 5.78 8.19
8.02 6.58 6.10 10.63 7.90 10.27 6.04 16.10
Note: NS ¼ negative schizotypy; CTQ¼ Childhood Trauma Questionnaire; SAS ¼ the Chapman Social; Anhedonia Scale; PAS ¼ the Chapman Physical Anhedonia Scale.
2017), and it predicts the onset of schizophrenia-spectrum disorders (Kwapil, 1998), therefore, it is necessary to explore the neural mecha nisms of abnormal facial emotion perception in individuals with high negative schizotypy (NS) and examine the impact of childhood maltreatment. We hypothesized that: (1) the early visual processing deficits (reduced P100 and N170 amplitudes) found in schizophrenia can be extended to individuals with higher levels of NS; and (2) Child hood maltreatment impacts the early stage of facial emotion processing in individuals with high NS. 2. Methods and materials 2.1. Participants During 2015–2017, three cross-sectional surveys were conducted with a convenience sample of first-year college students. The total effective number of completed questionnaires was 4902. A total of 300 students were identified as potential participants, of which 126 were randomly selected as participants. Cut-off scores for assignment to groups were according to the method by Wang et al. (2018). Based on students’ scores on the revised Social Anhedonia and Physical Anhe donia scales of the Chapman Psychosis-Proneness Scales, we divided the participants into two groups: the high-NS group (NS scores �23, n ¼ 74) and low-NS group (NS scores< 23, n ¼ 52) (Wang et al., 2018). The participants reported no history of psychiatric or neurological disorders when they were assessed using the Structured Clinical Interview for the Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition. Gender, age, and the scores on the Childhood Trauma Questionnaire-Short Form were matched in the two groups. Table 1 presents participants’ demographic and clinical characteristics. All participants were right-handed with normal or corrected to normal sight. Ten participants with invalid ERP data (e.g., excessive eye and head movements) were excluded from the analysis (Huffmeijer et al., 2014). The Ethical Committee of the Second Hospital Affiliated to Hunan University of Chinese Medicine approved the study. After explaining the study, we obtained participants’ written informed consent. They received financial compensation after completing all the tasks. 2.2. Measures 2.2.1. Chapman Psychosis-Proneness Scales (CPPS) All participants completed the four scales of the CPPS: the revised Social Anhedonia scale (RSAS) captures loss of interest in social re lationships, withdrawal, and/or inability to derive pleasure from inter personal relationships (Eckblad et al., 1982); the revised Physical Anhedonia scale (RPAS) measures failure to derive pleasure from 2
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Fig. 1. A trial sequence of the visual dot-probe task.
previously enjoyable stimuli (Chapman et al., 1976); the Magical Idea tion scale (MIS) assesses sub-clinical delusions and causation beliefs in personal influence over external events (Eckblad and Chapman, 1983); and the Perceptual Aberration scale (PAS) measures abnormal bodily perceptions (Chapman et al., 1978). The first two scales measure the negative dimension of schizotypy and the latter two measure the posi tive dimension of schizotypy. Participants’ responses to the RSAS and RPAS are reported in this study.
2.2.4. Electrophysiological recordings and data analysis Continuous electroencephalogram(EEG) activity was recorded using a Net Amps 300 high-impedance EEG amplifier (NetAmps 30.0, Elec trical Geodesics Inc. [EGI], Eugene, OR), with a 64-channel HydroCel Geodesic Sensor Net and a sampling rate of 500 Hz. Impedances were maintained below 50 kΩ during data collection, as recommended for this system (Ferree et al., 2001). All electrodes were manually refer enced to the vertex sensor Cz (set by EGI) and re-referenced off-line to the average electrodes. Off-line EEG data for extracting ERPs were analyzed using MATLAB (Mathworks Inc., Natick, MA) and EEGLAB. The continuous EEG was digitally filtered using a low pass of 30 Hz and a high pass of 0.1 Hz. EEG data were segmented into 1200-ms epochs, from 200 ms prior to the stimulus to 1000 ms after the stimulus. EEG artifacts caused by eye movements and blinks were removed through independent component analysis. Recording segments with more than 10 non-functional chan nels were rejected. These channels were replaced using spherical interpolation based on the given trial’s remaining sensors. The grand averages of the ERP waveforms were computed using the epochs for each stimulus type, yielding ERP waveforms for four condi tions: happy, angry, fearful, and disgusted. The amplitude and latency of the ERP components were measured as either the most positive or most negative data point in the specified latency window: P100, at the Oz, O1, and O2 electrode positions within an 80–170-ms window post-stimulus; and N170, at the P1, P7, and P9 (left hemisphere) and P2, P8, and P10 (right hemisphere) electrode positions, within a 150–200-ms window post-stimulus.
2.2.2. The Childhood Trauma Questionnaire-Short Form (CTQ-SF) Childhood maltreatment was evaluated using the Chinese version of the CTQ-SF, which showed good internal consistency and test-retest reliability in a sample of Chinese adolescents (Zhao et al., 2005). The 28-item CTQ-SF contains five subscales assessing different types of CM: emotional abuse, physical abuse, sexual abuse, emotional neglect, and physical neglect. Each item is rated on a 5-point ordinal scale from 1 (never true) to 5 (always true); seven items are reversed scored. Each subscale score ranges from 5 to 25 points and the total score ranges from 25 to 125 points; higher scores indicate more severe maltreatment during childhood. 2.2.3. Facial stimuli for the dot-probe task The dot probe task measures attentional biases induced by emotional and non-emotional stimuli (MacLeod et al., 1986). The dot-probe task was used to examine the neural mechanisms of early processing of facial emotions by individuals with high NS using ERP. Facial stimuli were chosen from the Chinese picture collection of emotional faces from the Institute of Psychology of the Chinese Academy of Sciences. In all, 54 neutral, 54 happy, and 54 negative expressions (18 angry, 18 fearful, and 18 disgusted expressions) were selected; half of them were male faces and half were female faces. The study consisted of 648 trials with 3 blocks; each block had 216 trials. Each trial began with a 500 ms fixation in the center of a screen, followed by a pair of emotional and neutral faces for 800 ms. Immediately following the offset of the faces, a dot probe (*) was presented in the same position as one of the two faces for 2000 ms. Participants were instructed to judge the side on which the dot had appeared and to indicate the correct response using a response box. They were exposed to one of two conditions on each trial: “congruent” trial—the facial expression of emotion and probe appeared on the same side or the “incongruent” trial—the probe appeared in a different loca tion from the facial expression. The experimental paradigm diagram see Fig. 1.
2.3. Statistical analysis Demographic data and participants’ scores on the self-report mea sures are presented. Data are presented as mean � standard deviation (SD). Age distributions and scores on the scales were analyzed using independent sample t-tests, and gender was analyzed by the chi-square test. We analyzed accuracy and reaction times (RTs) with a 2 � 2 � 4 repeated-measures design using multivariate analyses of variance (MANOVA) with group (high NS vs. low NS) as a between-subjects factor. Congruency (incongruent vs. congruent) and type of emotion (disgusted, fearful, angry, and happy) were within-subject factors. Repeated-measures ANOVAs were used to analyze potential differences in the P100 amplitudes and latencies with group (low NS vs. high NS) as a between-subjects factor, and type of emotion (happy, angry, fearful, and disgusted) and electrodes (O1, Oz, and O2) as within-subject factors. 3
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Fig. 2. Grand average ERPs elicited by emotional (angry, disgust, fear and happy) expressions at O1, O2 and Oz sites in high NS group and low NS group (A), along with scalp topographies of the P100 component (80–150 ms) in high NS group and low NS group, displaying a maximum at occipital electrodes (B).
4
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Fig. 3. Grand average ERPs elicited by emotional (angry, disgust, fear and happy) expressions in bilateral occipital temporal sites in high NS group and low NS group (A), along with scalp topographies of the N170 component (120–270 ms) in high NS group and low NS group, displaying a maximum at occipital electrodes (B).
Repeated-measures ANOVAs were used to analyze group (high NS vs. low NS) as a between-subjects factor and type of emotion (happy, angry, fearful, and disgusted) and hemisphere (right vs. left) as within-subject factors to examine differences in the N170 amplitudes and latencies. The Greenhouse-Geisser epsilon value was calculated when data from the repeated-measures analyses did not pass the sphericity test. Statistical significance for all tests was set at p < 0.05. SPSS 18.0 (IBM, Armonk,
NY) was used for all statistical analyses. 3. Results 3.1. Participants’ characteristics No significant differences were found between participants’ gender, 5
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Table 2 Peak latencies and amplitudes for the P100 and N170 components for each emotional face according to group (high NS vs low NS). The amplitudes and latencies of N170 are averaged across hemisphere. Data are mean � SD values. Group High NS group
Type of emotion
P1 Amplitude
N170 Amplitude
N170 Latency
O1
Oz
O2
O1
Oz
O2
Left
Right
Left
Right
angry
2.40 (2.41) 2.61 (2.37) 2.30 (2.30) 2.41 (2.16) 3.42 (2.49) 3.44 (2.40) 3.32 (2.63) 3.34 (2.31)
2.51 (2.62) 2.74 (2.42) 2.37 (2.46) 2.58 (2.29) 3.66 (2.59) 3.64 (2.47) 3.60 (2.74) 3.58 (2.48)
2.86 (2.51) 3.03 (2.51) 2.75 (2.53) 2.85 (2.32) 4.33 (2.66) 3.98 (2.45) 3.92 (2.80) 4.04 (2.57)
134.12 (23.77) 137.83 (23.55) 134.00 (23.73) 136.12 (22.92) 141.83 (18.49) 137.25 (20.75) 141.58 (19.54) 140.75 (19.54)
132.64 (26.69) 134.76 (24.68) 130.29 (27.28) 135.47 (26.34) 141.75 (19.14) 137.92 (19.05) 142.17 (19.39) 139.25 (20.51)
134.65 (24.91) 134.35 (23.12) 136.29 (23.43) 136.29 (24.56) 140.67 (20.22) 136.00 (18.19) 141.67 (17.44) 141.92 (17.09)
5.24 (2.99) 4.70 (2.73) 5.05 (2.74) 4.87 (2.70) 4.87 (2.36) 4.77 (2.57) 4.93 (2.59) 4.74 (2.42)
5.01 (3.00) 4.66 (2.87) 4.98 (2.72) 4.76 (2.64) 4.83 (2.99) 4.71 (3.01) 4.75 (3.21) 4.62 (3.06)
196.24 (19.09) 199.24 (16.38) 196.96 (17.31) 196.63 (14.82) 196.69 (15.07) 199.39 (17.21) 196.97 (20.98) 195.22 (17.31)
193.10 (18.56) 193.31 (18.12) 192.43 (17.82) 193.22 (18.75) 198.75 (16.83) 199.19 (16.13) 198.75 (17.84) 197.39 (17.68)
disgust fear happy
Low NS group
angry disgust fear happy
P1 Latency
Note: NS ¼ negative schizotypy; Left ¼ ERP average of channels P1, P7 and P9; Right ¼ ERP average of channels P2, P8 and P10.
age, or CTQ total and subscale scores. The high-NS group’s scores were significantly higher than the low-NS group on the RSAC and RPAS of the CPPS (Table 1).
statistically significant. The P100 had a significantly larger amplitude in the low-NS group than the high-NS group. Post-hoc analysis revealed larger P100 amplitudes at the right (O2) electrode compared to the left (O1) (p ¼ 0.001) or the midline (Oz) electrodes (p ¼ 0.001). No signifi cant effects were found for P100 latencies. The results of the MANOVA for the N170 amplitude showed a main effect of type of emotion (F(3, 114) ¼ 4.007, p ¼ 0.013, η2p ¼ 0.035), but no main effect of group (F(1,114) ¼ 0.081, p ¼ 0.776, η2p ¼ 0.001) or hemi sphere (F(1,114) ¼ 0.206, p ¼ 0.651, η2p ¼ 0.002). No interactions were significant. Post-hoc analysis showed angry facial expressions elicited a larger N170 amplitude than did disgusted (p ¼ 0.022) or happy ex pressions (p ¼ 0.001). Fearful facial expressions elicited a larger N170 amplitude than disgusted (p ¼ 0.036) or happy expressions (p ¼ 0.023). A main effect of type of emotion on the N170 latency (F(3, 114) ¼ 2.617, p ¼ 0.061, η2p ¼ 0.022) and a trend toward an interaction between group and hemisphere (F(1, 114) ¼ 3.768, p ¼ 0.055, η2p ¼ 0.032) were found. No other effects were significant. Post-hoc analysis revealed that happy facial expressions elicited a shorter N170 latency than disgusted ex pressions (p ¼ 0.001). Simple effects analysis revealed that the N170 latency in the high-NS group was shorter than that of the low-NS group in the right hemisphere, with a marginal statistical difference (p ¼ 0.08).
3.2. Behavioral data There was a main effect of congruency (F(1,123) ¼ 12.16, p ¼ 0.001
η2p ¼ 0.09) on RTs. Participants reactions were significantly quicker for incongruent trials than congruent trials. No other effects were found for RTs and no significant effects were found for accuracy (Ps > 0.05). 3.3. ERP data Grand mean ERPs to facial emotion and the according scalp topog raphies were illustrated separately for the P100 component at occipital sites (O1, O2, Oz) (see Fig. 2) and N170 component at bilateral occipital temporal sites (see Fig. 3) for high- and low-NS groups. Table 2 showed the P100 and N170 latencies and amplitudes for the high- and low-NS groups. The analyses revealed main effects of group (F(1,114) ¼ 7.20, p ¼ 0.008, η2p ¼ 0.059) and electrode site (F(2, 114) ¼ 10.421, p < 0.001, η2p ¼ 0.084), but no main effect of emotion (F(3,114) ¼ 0.779, p ¼ 0.497, η2p ¼ 0.007) on the P100 amplitude. No interaction effects were
Table 3 Peak latencies and amplitudes for the P100 components for each emotional face according to group (high NS with CM, high NS without CM, low NS with CM, low NS without CM). Data are mean � SD values. Group High NS with CM group
High NS without CM group
Low NS with CM group
Low NS without CM group
Type of emotion angry disgust fear happy angry disgust fear happy angry disgust fear happy angry disgust fear happy
P1 Amplitude
P1 Latency
O2
Oz
O1
O2
Oz
O1
2.74(2.31) 2.78(2.38) 2.76(2.29) 2.95(2.27) 2.99(2.73) 3.29(2.66) 2.75(2.79) 2.75(2.41) 3.99(2.89) 3.81(2.75) 3.19(3.02) 3.68(2.94) 4.64(2.44) 4.14(2.18) 4.60(2.44) 4.38(2.19)
2.15(2.48) 2.44(2.16) 2.40(2.35) 2.68(2.25) 2.89(2.74) 3.05(2.67) 2.34(2.61) 2.75(2.41) 3.16(2.54) 3.53(2.70) 2.85(2.83) 3.11(2.70) 4.12(2.60) 3.74(2.28) 4.28(2.52) 4.02(2.23)
2.12(2.39) 2.32(2.22) 2.22(2.11) 2.38(1.92) 2.70(2.42) 2.92(2.51) 2.40(2.51) 2.47(2.36) 2.76(2.29) 2.95(2.45) 2.47(2.34) 2.75(2.36) 4.01(2.55) 3.89(2.30) 4.11(2.68) 3.89(2.16)
135.31(27.35) 138.40(23.08) 140.11(24.28) 140.00(25.19) 133.94(22.45) 130.01(22.72) 132.24(22.13) 132.36(23.63) 136.52(20.16) 133.04(20.26) 136.70(17.67) 137.91(19.81) 144.48(19.91) 138.72(15.99) 146.24(16.25) 145.60(13.52)
132.34(29.32) 140.80(23.32) 132.69(30.08) 138.40(28.25) 132.97(24.04) 128.36(24.81) 127.76(24.16) 132.36(24.19) 138.61(19.62) 132.52(20.58) 136.70(21.53) 134.26(22.33) 144.64(18.61) 142.88(16.39) 147.20(16.00) 143.84(17.91)
137.60(23.77) 141.49(21.19) 139.77(21.82) 142.51(20.90) 130.42(23.58) 133.94(25.58) 127.88(24.46) 129.33(23.32) 138.96(19.00) 132.00(22.40) 138.43(21.77) 136.35(20.11) 144.48(17.97) 142.08(18.23) 144.48(17.18) 144.80(18.48)
Notes: NS ¼ negative schizotypy; CM ¼ childhood maltreatment. 6
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individuals during a facial emotion-processing task, to confirm prior findings on facial emotion processing in patients with schizophrenia. We evaluated individuals with high NS, which yielded more narrowly focused findings, and examined the impact of childhood maltreatment on their facial emotion processing. The ERP data demonstrated that all facial expressions elicited fewer positive P100 amplitudes in the high-NS group than the low-NS group; no differences in N170 amplitudes between the two groups were found. P100 indicates early visual processing (Allison et al., 1999) and face-specific categorization (Herrmann et al., 2005a, 2005b), and N170 indicates the visual processing of facial structures (Bentin et al., 1999), therefore, our results suggest impaired fundamental visual processing in high-NS individuals, although the processing of facial figurations ap pears to be intact. The decreased P100 amplitudes in the high-NS group is similar to P100 deficits found in patients with schizophrenia (Caharel et al., 2007; Campanella et al., 2006) and persons at-risk for schizo phrenia during facial processing (Wolwer et al., 2012). These findings suggest that deficits in facial emotion processing precede the onset of the initial psychotic episode, and therefore, may be a vulnerability marker for schizophrenia. Furthermore, P100 amplitude deficits in processing facial expressions are independent of emotions (happy, angry, disgusted, or fearful), indicating these deficits are not emotion specific in high-NS individuals. N170 deficits (i.e., reduced amplitude and delayed latency) in patients with schizophrenia during facial emotion processing have been reported (Herrmann et al., 2004; Johnston et al., 2005; Turetsky et al., 2007), but we did not find this or a similar deficit among in dividuals with high NS. This is most likely because deficits in high-NS persons are typically visuo-sensory specific, as reflected by P100 dif ferences between individuals with high and low NS, and less likely to be face-specific. The main effect of emotion was significant for N170 am plitudes, with angry and fearful expressions eliciting larger amplitudes than disgusted or happy expressions. No difference was found in the magnitude of the N170 amplitude priming effect for happy and disgusted faces. These findings suggest that affect modulates N170 processing, such that responses to faces with greater affective salience are enhanced compared to faces with less affective salience, as reported in previous studies (Ashley et al., 2004; Batty and Taylor, 2003; Blau et al., 2007). When examining the effect of childhood maltreatment on the early stage of facial emotion processing, we found that, compared to the high-NS group without CM, the high-NS group with CM had a longer latency of P100. It is well known that a prolonged of P100 latency in dicates a dysfunction of the visual pathway (Cant et al., 1978). There fore, childhood maltreatment may be a factor responsible for the pathological state of the visual pathway in high NS group. This study supports hemispheric specialization of facial emotion processing. The P100 amplitude was significantly larger over the right hemisphere compared to the left hemisphere and midline electrodes. For the N170 latency, a trend was found toward an interaction between group and hemisphere, with earlier responses over the right rather than the left hemisphere in the high-NS group. With regard to the N170 amplitude, we did not find lateralization effects as reported previously (Bentin et al., 1999; Joyce and Rossion, 2005); nor did some other studies find significant differences between the left and right sides (Botzel et al., 1995; Eimer, 2000; Rossion et al., 2000). Among the study’s limitations, the first is that our sample consisted of undergraduates students, which might decrease the generalizability of the findings to populations outside university settings. Second, we used self-report questionnaires to assess schizotypy and childhood maltreatment. Ecologically valid sampling methods might be more appropriate. Third, the effect of depression on facial emotion processing should have been addressed given the evidence that individuals with depression are poor at recognizing facial expressions of emotion, and depression is common in schizotypy. Depressive symptoms, including their effects on outcomes and ways to control for them, are important issues for future research in this area. In conclusion, our findings suggest individuals with high NS have
Table 4 The amplitudes and latencies of N170 averaged across hemisphere for each emotional face according to group (high NS with CM, high NS without CM, low NS with CM, low NS without CM). Data are mean � SD values. Group
Type of emotion
N170 Amplitude
N170 Latency
Left
Right
Left
Right
High NS with CM group
angry
5.38 (2.74) 5.07 (2.56) 5.35 (2.44) 5.18 (2.65) 5.09 (3.27) 4.30 (2.89) 4.72 (3.03) 4.54 (2.75) 5.61 (2.36) 5.20 (2.59) 5.63 (2.49) 5.43 (2.41) 4.19 (2.18) 4.38 (2.53) 4.29 (2.55) 4.10 (2.28)
5.46 (3.40) 5.22 (3.16) 5.34 (2.99) 5.13 (2.99) 4.53 (2.47) 4.07 (2.45) 4.61 (2.40) 4.38 (2.20) 5.49 (3.33) 5.06 (3.18) 5.39 (3.12) 5.29 (3.19) 4.22 (2.57) 4.39 (2.86) 4.17 (3.24) 4.01 (2.87)
196.04 (21.79) 200.65 (17.36) 196.95 (20.00) 195.89 (15.74) 196.44 (16.07) 195.07 (18.80) 196.97 (14.23) 197.41 (13.98) 193.51 (14.01) 193.10 (15.29) 191.42 (20.68) 199.36 (18.78) 199.63 (15.69) 205.17 (17.12) 202.08 (20.33) 199.36 (18.78)
192.50 (18.23) 191.66 (17.56) 192.23 (16.84) 194.36 (15.89) 193.74 (19.16) 197.41 (13.98) 192.65 (19.07) 192.00 (21.57) 197.80 (13.47) 197.68 (13.58) 195.77 (15.48) 193.80 (13.87) 199.63 (19.66) 200.59 (18.33) 201.49 (19.67) 200.69 (20.29)
disgust fear happy
High NS without CM group
angry disgust fear happy
Low NS with CM group
angry disgust fear happy
Low NS without CM group
angry disgust fear happy
Notes: NS ¼ negative schizotypy; CM ¼ childhood maltreatment.
3.4. The influence of CM on P100 and N170 amplitudes and latencies In order to explore the influence of CM on the early stage of facial emotion processing, the participants were further divided into four groups: high-NS group with CM, high-NS group without CM, low-NS group with CM, low-NS group without CM. Table 3 and Table 4 shows the P100 and N170 latencies and amplitudes for the four groups. Simi larly, repeated-measures ANOVAs were used to analyze potential dif ferences in the P100/and N170 amplitudes and latencies with group (high NS with CM, high NS without CM, low NS with CM, low NS without CM) as a between-subjects factor, and type of emotion (happy, angry, fearful, and disgusted) and electrodes (O1, Oz, and O2)/and hemisphere (right vs. left) as within-subject factors, respectively. The analyses revealed only a main effect of group on the P100 latency (F(3, 2 112) ¼ 3.301, p ¼ 0.023, ηp ¼ 0.081) and amplitude (F(3, 112) ¼ 3.332, 2 p ¼ 0.022, ηp ¼ 0.082). No main effect of group on N170 latency (F(3, 2 112) ¼ 1.288, p ¼ 0.282, ηp ¼ 0.033) and amplitude (F(3, 112) ¼ 1.516, 2 p ¼ 0.214, ηp ¼ 0.039). No interaction effects were statistically signifi cant. Post hoc tests revealed that P100 amplitude was significantly larger in the low-NS group without CM compared with the high-NS group with CM (p ¼ 0.003), in the low-NS group without CM compared to the highNS group without CM (p ¼ 0.014). The P100 latency was significantly shorter in the high-NS group without CM compared to the low-NS group without CM (p ¼ 0.003). The high-NS group without CM had shorter P100 latency compared to the high-NS group with CM, with a marginal statistical difference (p ¼ 0.063). 4. Discussion This study compared the brain activity of high-NS with low-NS 7
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impaired fundamental visual processing, but intact processing of facial figurations. Childhood maltreatment may be a factor responsible for the pathological state of the visual pathway in high NS group.
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CRediT authorship contribution statement Jingbo Gong: Writing - original draft, Writing - review & editing. Jianbo Liu: Conceptualization, Methodology, Writing - review & edit ing. Lizhi Shangguan: Investigation, Data curation. Qin Zhang: Investigation, Data curation. Zhu Peng: Investigation, Data curation. Zun Li: Investigation, Data curation. Chuwen Chen: Investigation, Data curation. Lijuan Shi: Formal analysis. Acknowledgements This work was supported by grants from Humanities and Social Science Fund of Ministry of Education(18YJC190004),the Natural Sci ence Foundation of Hunan Province (2017JJ3240), and the Hunan Ed ucation Department Excellent Youth Fund (18B219). Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi. org/10.1016/j.neuropsychologia.2019.107215. References Aas, M., Kauppi, K., Brandt, C.L., Tesli, M., Kaufmann, T., Steen, N.E., Agartz, I., Westlye, L.T., Andreassen, O.A., Melle, I., 2017. Childhood trauma is associated with increased brain responses to emotionally negative as compared with positive faces in patients with psychotic disorders. Psychol. Med. 47 (4), 669–679. Addington, J., Addington, D., 1998. Facial affect recognition and information processing in schizophrenia and bipolar disorder. Schizophr. Res. 32 (3), 171–181. Allison, T., Puce, A., Spencer, D.D., McCarthy, G., 1999. Electrophysiological studies of human face perception. I: potentials generated in occipitotemporal cortex by face and non-face stimuli (New York, N.Y. : 1991). Cerebr. Cortex 9 (5), 415–430. Ashley, V., Vuilleumier, P., Swick, D., 2004. Time course and specificity of event-related potentials to emotional expressions. Neuroreport 15 (1), 211–216. Barkl, S.J., Lah, S., Harris, A.W., Williams, L.M., 2014. Facial emotion identification in early-onset and first-episode psychosis: a systematic review with meta-analysis. Schizophr. Res. 159 (1), 62–69. Batty, M., Taylor, M.J., 2003. Early processing of the six basic facial emotional expressions. Brain research. Cogn. Brain Res. 17 (3), 613–620. Batty, R.A., Francis, A.J., Innes-Brown, H., Joshua, N.R., Rossell, S.L., 2014. Neurophysiological correlates of configural face processing in schizotypy. Front. Psychiatry 5, 101. Bentin, S., Allison, T., Puce, A., Perez, E., McCarthy, G., 1996. Electrophysiological studies of face perception in humans. J. Cogn. Neurosci. 8 (6), 551–565. Bentin, S., Deouell, L.Y., Soroker, N., 1999. Selective visual streaming in face recognition: evidence from developmental prosopagnosia. Neuroreport 10 (4), 823–827. Biotti, F., Gray, K.L.H., Cook, R., 2017. Impaired body perception in developmental prosopagnosia. Cortex; a journal devoted to the study of the nervous system and behavior, vol. 93, pp. 41–49. Blau, V.C., Maurer, U., Tottenham, N., McCandliss, B.D., 2007. The face-specific N170 component is modulated by emotional facial expression. Behav. Brain Funct. : BBF 3, 7. Botzel, K., Schulze, S., Stodieck, S.R., 1995. Scalp topography and analysis of intracranial sources of face-evoked potentials. Exp. Brain Res. 104 (1), 135–143. Brooks, G.A., Brenner, C.A., 2017. Is there a common vulnerability in cannabis phenomenology and schizotypy? The role of the N170 ERP. Schizophr. Res.. Brown, L.A., Cohen, A.S., 2010. Facial emotion recognition in schizotypy: the role of accuracy and social cognitive bias. J. Int. Neuropsychol. Soc. : JINS 16 (3), 474–483. Caharel, S., Bernard, C., Thibaut, F., Haouzir, S., Di Maggio-Clozel, C., Allio, G., Fouldrin, G., Petit, M., Lalonde, R., Rebai, M., 2007. The effects of familiarity and emotional expression on face processing examined by ERPs in patients with schizophrenia. Schizophr. Res. 95 (1–3), 186–196. Campanella, S., Montedoro, C., Streel, E., Verbanck, P., Rosier, V., 2006. Early visual components (P100, N170) are disrupted in chronic schizophrenic patients: an eventrelated potentials study. Neurophysiologie clinique ¼ Clinical neurophysiologyNeurophysiol. Clinique Clin. Neurophysiol. 36 (2), 71–78. Cancel, A., Comte, M., Boutet, C., Schneider, F.C., Rousseau, P.F., Boukezzi, S., Gay, A., Sigaud, T., Massoubre, C., Berna, F., Zendjidjian, X.Y., Azorin, J.M., Blin, O., Fakra, E., 2017. Childhood trauma and emotional processing circuits in schizophrenia: a functional connectivity study. Schizophr. Res. 184, 69–72. Cant, B., Hume, A.L., Shaw, N., 1978. Effects of luminence on the pattern visual evoked potential in multiple sclerosis. Electroencephalogr. Clin. Neurophysiol. 45 (4), 496–504.
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