International Journal of Psychophysiology 116 (2017) 68–76
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Cued uncertainty modulates later recognition of emotional pictures: An ERP study Huiyan Lin a,b,1, Jing Xiang c,d,1, Saili Li d, Jiafeng Liang e, Dongmei Zhao a, Desheng Yin f, Hua Jin f,⁎ a
Institute of Applied Psychology, Guangdong University of Finance, 510521 Guangzhou, China Laboratory for Behavioral and Regional Finance, Guangdong University of Finance, Guangzhou, 510521, Guangdong, China Shaxi Primary School, 518000 Shenzhen, China d Center for Studies of Psychological Application, School of Psychology, South China Normal University, 510631 Guangzhou, China e School of Education, Guangdong University of Education, 510303 Guangzhou, China f Key Research Base of Humanities and Social Sciences of the Ministry of Education, Center of Cooperative Innovation for Assessment and Promotion of National Mental Health, Academy of Psychology and Behavior, Tianjin Normal University, 300074 Tianjin, China b c
a r t i c l e
i n f o
Article history: Received 3 October 2016 Received in revised form 4 March 2017 Accepted 15 March 2017 Available online 16 March 2017 Keywords: Uncertainty Cues Emotional pictures P2 P3 ERP
a b s t r a c t Previous studies have shown that uncertainty about the emotional content of an upcoming event modulates event-related potentials (ERPs) during the encoding of the event, and this modulation is affected by whether there are cues (i.e., cued uncertainty) or not (i.e., uncued uncertainty) prior to the encoding of the uncertain event. Recently, we showed that uncued uncertainty affected ERPs in later recognition of the emotional event. However, it is as yet unknown how the ERP effects of recognition are modulated by cued uncertainty. To address this issue, participants were asked to view emotional (negative and neutral) pictures that were presented after cues. The cues either indicated the emotional content of the pictures (the certain condition) or not (the cued uncertain condition). Subsequently, participants had to perform an unexpected old/new task in which old and novel pictures were shown without any cues. ERP data in the old/new task showed smaller P2 amplitudes for neutral pictures in the cued uncertain condition compared to the certain condition, but this uncertainty effect was not observed for negative pictures. Additionally, P3 amplitudes were generally enlarged for pictures in the cued uncertain condition. Taken together, the present findings indicate that cued uncertainty alters later recognition of emotional events in relevance to feature processing and attention allocation. © 2017 Published by Elsevier B.V.
1. Introduction Accurate anticipation about an upcoming event is of great importance to survival, as it may help individuals to avoid undesirable events. In daily life, however, there is often uncertainty about whether the upcoming event is undesirable or not. This uncertainty has been suggested to produce fear and anxiety (e.g., Grupe and Nitschke, 2013), to result in the overestimation of the upcoming threat (e.g., Dieterich et al., 2016; Grupe and Nitschke, 2011; Sarinopoulos et al., 2010) and to be at a disadvantage in preparing for the upcoming undesirable events (e.g., Lin et al., 2014a). Previous studies have investigated whether the uncertainty influences electroencephalography (EEG) for the upcoming emotional event. Regarding these studies, several researchers asked participants to view the pictures which emotional content was preceded with a ⁎ Corresponding author. E-mail address:
[email protected] (H. Jin). 1 Lin and Xiang contributed equally to the writing of this work.
http://dx.doi.org/10.1016/j.ijpsycho.2017.03.004 0167-8760/© 2017 Published by Elsevier B.V.
cue (i.e., the certain condition) or without any cues (i.e. the uncued uncertain condition; Lin et al., 2012; Onoda et al., 2006, 2007). Using this paradigm, Onoda et al. (2007) found that negative pictures evoked stronger lower-2-alpha activity in event-related desynchronization (ERD)/synchronization (ERS) in the time range of 500–1000 ms in the certain condition compared to the uncued uncertain condition. However, Onoda et al. (2006) did not observe any effects of uncued uncertainty on visual evoked magnetic fields (VEF) to emotional pictures. However, VEF and ERD/ERS may be unsuitable for investigating the effects in relevance to emotional anticipation (Lin et al., 2012, 2015a), as these techniques cannot show the effects at both early and late stages of processing. For example, when VEF and ERD/ERS were used to investigate the processing of emotion anticipation; no effects of anticipation were found in the VEF study (Onoda et al., 2006), and the anticipation effect was observed only in the late stages of processing in the ERD/ERS study (Onoda et al., 2006). Using event-related potentials (ERPs), however, our previous study observed the anticipation effects at both early and late stages (Lin et al., 2014a). When ERPs were used to further investigate the effects of uncued uncertainty on emotional pictures, we found that
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emotional (positive and negative) pictures generally elicited smaller P2, N2 and late potential potentials (LPP) amplitudes in the uncued uncertain condition compared to the certain condition (Lin et al., 2012). The P2 and N2, peaking over anterior sites at appropriately 150–200 ms and 200–300 ms following stimulus onset, are thought to be relevant to sensory encoding (e.g., Olofsson et al., 2008; Pratt et al., 2011). The LPP, which develops approximately 400 ms after the onset of a stimulus and sometimes lasts for a few seconds, is relevant to memory encoding (e.g., Azizian and Polich, 2007; Olofsson et al., 2008). The findings possibly suggest that uncued uncertainty reduces the encoding of the events independently of valence. The above-mentioned studies investigated the uncertainty effects only when participants knew nothing about the occurrence of the event or its emotional content. In some cases, however, people may realize that an event will happen, but fail to understand its emotional content (Onoda et al., 2008; Sarinopoulos et al., 2010). With respect to this issue, Onoda et al. (2006, 2007) manipulated this uncertainty with the presence of cues that signified the appearance of an upcoming event but did not indicate its emotional content (i.e., cued uncertainty). Studies have also investigated whether emotional pictures were different in the cued uncertain condition compared to the certain condition using ERD/ERS (Onoda et al., 2007) and VEF (Onoda et al., 2006). No effects of cued uncertainty were found in the ERD/ERS study (Onoda et al., 2007) and the effects were shown only at early stages of processing in the VEF study (Onoda et al., 2006). Considering that ERD/ERS and VEF may fail to reveal the related effects at both early and late stages of processing; several other studies further investigate the effects of cued uncertainty using ERPs. In the study by Gole et al. (2012), for instance, the findings showed that emotional (negative and neutral) pictures evoked larger early posterior negativity (EPN, overlapping with the N2) but smaller LPP amplitudes in the cued uncertain condition compared to the certain condition irrespective of the emotional content of the pictures. In addition, our previous study showed reduced P2 and late LPP (550–1000 ms) but enhanced N2 amplitudes for negative pictures in the cued uncertain condition. For positive pictures, the effect of cued uncertainty was observed only in early LPP (350–450 ms), with enhanced early LPP amplitudes in the cued uncertain condition (Lin et al., 2015a). In a recent study by Dieterich et al. (2016), the authors reported that emotional (negative and neutral) pictures generally evoked larger P2 and LPP amplitudes in the cued uncertain condition compared to the certain condition. The differential findings may be related to whether the anticipation period (e.g., the interval between the cues and the pictures) was long (Lin et al., 2014a, 2015a) and whether participants were asked to estimate the emotional content of the pictures during the anticipation period. Nevertheless, the findings may generally suggest that cued uncertainty modulates the encoding of emotional events, whereas the modulatory mechanisms may be different based on the stages of event processing. Encoding, which is thought to be the first stage of memory, should influence later stages, such as recognition (e.g., Erk et al., 2005; Lin et al., 2015c, 2015d; Marzi and Viggiano, 2010). As shown in the abovedescribed studies, uncertainty modulates the encoding of emotional pictures. Therefore, we primitively investigated whether uncued uncertainty about the emotional pictures affected later recognition of the pictures (Lin et al., 2015d). The results showed that recognition of negative pictures evoked reduced P2 over the right inferior temporal-parietal scalp sites and decreased P3 over parietal sites when the pictures had been encoded in the uncued uncertain condition compared to the certain condition. The P2 is a positive component that peaks appropriately 200 ms following stimulus onset. Whereas the P2 is often shown to be distributed over frontal scalp sites; in the studies investigating stimulus retrieval, the P2 was found to peak over inferior temporal-parietal scalp sites, particularly in the right hemisphere (e.g., Kaufmann et al., 2013; Lin et al., 2015d; Stahl et al., 2008; Schulz et al., 2012a, 2012b; Wiese et al., 2013, 2014). This P2 is supposed to be related to the processing of stimulus features (e.g., Kaufmann et al., 2013; Stahl et al., 2008;
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Schulz et al., 2012a, 2012b; Wiese et al., 2013, 2014). The P3, which develops appropriately 300 ms after the onset of a stimulus over parietal scalp sites, is often thought to be related to stimulus retrieval in memory research (e.g., Curran and Cleary, 2003; Marzi and Viggiano, 2010; Rugg et al., 1998; Weymar et al., 2013). This component has been shown to be associated with the allocation of attentional resources (e.g., Olofsson et al., 2008; Polich, 2007). Taken together, our previous study (Lin et al., 2015d) suggests that uncued uncertainty reduces feature processing and allocation of attentional resources in the later recognition of negative pictures. As mentioned above, cued and uncued uncertainty point to differential mechanisms; e.g., uncued uncertainty is associated with uncertainty about the occurrence and the emotional content of the event, but only the emotional content is uncertain for cued uncertainty. Previous studies have also suggested that the encoding of emotional pictures differs between cued and uncued uncertainty (Dieterich et al., 2016; Gole et al., 2012; Lin et al., 2012, 2015a; Onoda et al., 2006, 2007). Therefore, while our previous study investigated the effects of uncued uncertainty on recognition of emotional pictures (Lin et al., 2015d); more studies should be performed to investigate the effects of cued uncertainty related to recognition in order to better understand the long-term effects of uncertainty. To address this issue, participants in the present study were asked to view emotional (negative or neutral) pictures that were presented after anticipatory cues. The cues either indicated the emotional content of the following picture (i.e. the certain condition) or not (i.e. the cued uncertain condition). Subsequently, participants were asked to perform an unexpected old/new recognition task, in which no cues were presented before the pictures. EEG was recorded from the encoding phase to the recognition phase. In the encoding phase, we predicted that the effects of cued uncertainty may be shown in P2, N2 and LPP, according to previous studies (Dieterich et al., 2016; Gole et al., 2012; Lin et al., 2015a). However, as mentioned above, the effects were different due to several factors, such as the anticipation periods (Lin et al., 2014a, 2015a) and the anticipation estimation. Considering that the manipulations in the present study were similar to those in our previous one (Lin et al., 2015a); we predicted that cued uncertainty may enhance N2 but reduce the P2 and LPP for emotional pictures, particularly for negative ones. In the recognition phase, according to our previous study on uncued uncertainty (Lin et al., 2015d), we predicted that the effects of cued uncertainty on recognition of emotional pictures may be reflected in the P2 and P3. However, as the effects of cued uncertainty compared to uncued uncertainty may be different as a result of encoding (Lin et al., 2012, 2015a; Onoda et al., 2006, 2007); it is still unknown what the effects of cued uncertainty on the P2 and P3 would be.
2. Methods 2.1. Participants Twenty-four healthy undergraduate and postgraduate females2 were recruited in South China Normal University via advertisements in return for the compensation of 50 RMB. Five participants were excluded from the statistical analysis due to excessive artifacts in the EEG signals, resulting in a total of 19 participants (18–26 years old, M = 22.22, SD = 2.26). All participants were right handed, as assessed through the Edinburgh Handedness Inventory (Oldfield, 1971). Participants reported normal or corrected-to-normal vision and no history of neurological illness. All participants gave written informed consent in accordance with standard ethical guidelines as defined in the Declaration of Helsinki. The study was approved by the ethics committee of School of Psychology, South China Normal University. 2 Note that as the relationships between anticipation and recognition of emotional events are thought to be relevant to females only (Galli et al., 2011, 2014), the present study recruited females only.
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2.2. Stimuli Stimuli were the same as those used in our previous study (Lin et al., 2015d). The stimuli consisted of 240 negative and 240 neutral pictures. The pictures were obtained from various sources, such as the International Affective Picture System (IAPS; Lang et al., 2008), Chinese Affective Picture System (CPAS; Bai et al., 2005) and public pictures available on the internet. All the pictures were adjusted to 11 cm (horizontal) × 9 cm (vertical), were converted to grey-scale and were matched in luminance and contrast with the help of Adobe Photoshop CS6. These pictures were rated by another group of 109 undergraduate and postgraduate females (19–27 years, M = 21.68, SD = 1.59) on valence and arousal using a 9-point scale ranging from “1” (very unpleasant) to “9” (very pleasant) and “1” (low) to “9” (high), respectively. The ratings were lower for negative (M ± SE = 2.64 ± 0.08) compared to neutral pictures (4.94 ± 0.06) in valence, F(1, 108) = 686.23, p b 0.001, η2p = 0.86. For arousal, the ratings were higher for negative (5.09 ± 0.15) compared to neutral pictures (2.88 ± 0.13), F(1, 108) = 175.23, p b 0.001, η2p = 0.62. Half of the pictures (120 negative and 120 neutral) were used as old pictures and were presented during the encoding and the recognition phase. The other half, serving as novel pictures, were presented only during the recognition phase. Each emotion category of old pictures was pseudo-randomly separated into two sets. The four sets of old pictures were used to create four experimental conditions: certain-negative, cued uncertain-negative, certain-neutral and cued uncertain-neutral. Assignments of these sets were counterbalanced across participants. In addition, the ratings on valence and arousal were not significantly different between old and novel pictures and among different sets of old pictures, ps. N 0.05. For more details, please refer to our previous study (Lin et al., 2015d). 2.3. Procedure After informed consent had been obtained and handedness had been determined, participants were asked to sit at a viewing distance of approximately 100 cm in front of a 17-in. computer screen (screen resolution 640 × 480 pixels). Stimulus presentation was controlled and behavioral responses were recorded by E-prime 1.0 software (Psychology Software Tools, Inc., Pittsburgh, PA, USA). All stimuli were presented against a grey background. The actual experiment consisted of two phases, the encoding phase and the recognition phase. Before the encoding task, participants were told that they would be presented with pictures after anticipatory cues (i.e., “#”, “*” and “?”). Participants were told the meanings of the cues (e.g., the symbol “#” and “*” will be always followed by a negative and a neutral picture, respectively). The emotional content of the following picture will be unknown if the symbol “?” is presented. Participants were also told to view the cues and the pictures during presentation. To allow participants to concentrate on the experiment, they were also told to rate the pictures for valence on a 9-point scale (“1” = very unpleasant and “9” = very pleasant) after the presentation of the pictures using the number keypad on the keyboard without any time limit. Each trial started with a black fixation cross for 500 ms, followed by a blank screen for 600 to 1000 ms (M = 800 ms). Subsequently, a cue was presented for 200 ms. The symbol “?” served as the uncertain cue in that it was randomly followed by a negative or a neutral picture with equal conditional probabilities. For half of the participants, the symbols “#” and “*” served as certain cues for subsequent negative and neutral pictures, respectively. The meanings of the symbols were switched for the other half of the participants. After another blank screen of a random duration between 1600 and 2000 ms (M = 1800 ms), a picture was presented for 1000 ms. Following a blank screen for 200 ms, a picture rating scale was shown until the picture had been rated. The next trial started after another blank screen for 1000 ms. According to the emotional category of the pictures and the
meanings of the cues, there were four experimental conditions (certainnegative, cued uncertain-negative, certain-neutral and cued uncertainneutral). For each experimental condition, each picture (old picture) described in the Stimuli section was presented once. That is, the encoding phase consisted of 240 trials. Subsequently, participants were asked to take a short rest for approximately 10 min. After the rest, participants were informed about the recognition task. Participants did not know about the task until this point in the experiment. Participants were instructed to respond to the novelty of the pictures by pressing the “F” and the “J” key with the left and the right index finger, respectively, during the presentation of the picture or the following blank. The instructions for the task emphasized speed and accuracy. Response assignments were counterbalanced across participants. Each trial started with a black fixation cross for 500 ms. Following a blank screen that was presented for 600–1000 ms (M = 800 ms), a picture was presented for 1000 ms. The sequence between old and novel pictures was randomized across participants. The next trial started after another blank screen for 1000 ms. Each (old and novel) picture was presented once. Therefore, the recognition task consisted of 480 trials in total. The complete experiment including the encoding and the recognition phase lasted appropriately 1.5 h. 2.4. Behavioral recording In the encoding phase, the valence ratings for the pictures were recorded. In the recognition phase, hits and response times were recorded from the onset of the picture to the offset of the following blank. Response times were analyzed for correct trials only. 2.5. EEG recording EEGs were recorded using a NeuroScan Synamps 2 AC-amplifier (NeuroScan, Inc., Sterling, VA, USA). The Ag/AgCl electrodes were placed on the scalp with a 32 channel Quick-Cap according to the international extended 10–20 system (FP1/2, F7/3/z/4/8, FT7/8, FC3/z/4, T7/8, C3/z/4, CP3/z/4, TP6/7, P7/3/z/4/8, O1/z/2 and A1/2). EEG electrodes were connected to a ground and were referenced to the right mastoid online. The horizontal electrooculogram (EOG) was recorded from two electrodes at the outer canthi of both eyes, and the vertical EOG was monitored bipolarly from electrodes above and below the left eye. AC recording was performed, and the sampling rate was 1000 Hz. Band-pass filtering (0.05–100 Hz) was applied with a 50 Hz notch filter online. Impedances were below 5 kΩ. Offline, the EEG data were analyzed using the SCAN 4.3 software. Raw EEG data were re-referenced to the average of the left and right mastoids. Ocular movements were inspected and removed from the EEG signal using a regression procedure implemented with NeuroScan 4.3 software (Semlitsch et al., 1986). EEG data were then segmented into 1100 ms epochs from − 100 ms to 1000 ms relative to the onset of all pictures and old pictures in the encoding and the recognition phase, respectively, with the first 100 ms epochs for baseline correction. In the recognition phase, previous studies showed differential neural activity for the stimuli that had been remembered compared to those that were forgotten (e.g., Hsieh et al., 2009; Reber et al., 2002) and many ERP studies on stimulus recognition analyzed the stimuli that had been only remembered (e.g., Kaufmann et al., 2013; Lin et al., 2015d; Weymar et al., 2013). Therefore, we analyzed old pictures for correct responses only. Artefact rejection was performed with the amplitude threshold of 100 μV. Artefact-free trials were averaged separately for each electrode and experimental condition, and averaged ERPs were digitally low-pass filtered at 30 Hz (24 db/oct, zero phase shift, Butterworth). Finally, ERPs were re-calculated to an average reference excluding vertical and horizontal EOG channels. ERPs were quantified using mean amplitudes for all the components of interest relative to the − 100 ms baseline. In the encoding phase,
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ERPs were quantified using mean amplitudes for P2 (130–180 ms), N2 (220–330 ms) and LPP (450–850 ms). The P2 and N2 were measured at the electrodes Fz/FCz/Cz. The LPP was measured at the electrodes Fz/ FCz. In the recognition phase, the P2 was measured in the time window of 200–240 ms at the electrodes TP7/8. The P3 was measured in the time window of 300–450 ms at the electrode Pz. Electrodes of interest and the time windows were chosen according to previous studies (Dieterich et al., 2016; Gole et al., 2012; Lin et al., 2015a, 2015d; Stahl et al., 2008; Schulz et al., 2012a, 2012b; Weymar et al., 2013) and visual inspection of the grand waveforms.
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Table 2 Mean of hit rates and response times and the SD for all the experimental conditions. Emotion
Uncertainty Certain
Hit rates Neutral Negative Response times Neutral Negative
Cued uncertain
M
SE
M
SE
0.67 0.66
0.21 0.20
0.64 0.67
0.20 0.16
760.94 784.19
86.66 90.59
756.82 784.01
91.31 106.21
2.6. Data analysis For the behavioral data, including the ratings in the encoding phase and hit rates and response times in the recognition phase, we performed 2 × 2 analyses of variance (ANOVAs) with cued uncertainty (cued uncertain versus certain) and emotion (negative versus neutral) as withinsubject factors. The means and SDs of the ratings are shown in Table 1, and those of hit rates and response times are shown in Table 2. For ERP data, the above-mentioned ANOVAs were performed separately for all the components. In the encoding phase, the analysis for P2 and N2 included electrode (Fz versus FCz versus Cz) as a within-subject factor. The analysis for the LPP included electrode (Fz versus FCz) as a within-subject factor. For the recognition phase, the analysis for P2 included electrode (TP7 versus TP8) as a within-subject factor. Grandaverage waveforms of the components for the encoding phase are shown in Fig. 1, and those of the P2 and P3 are shown in Figs. 3 and 4, respectively. Topographical maps for these components in the encoding and the recognition phase are shown in Fig. 2 and Fig. 5, respectively. The means and SDs of the components across conditions for the encoding and the recognition phase are shown in Tables 3 and 4, respectively. Degrees of freedom and p-values of repeated measurements were corrected with the Greenhouse-Geisser correction, and the p-values of post-hoc tests were corrected with the Bonferroni correction. To gain a better understanding of the relationship between encoding and recognition, we also analyzed the correlations between these two phases, i.e., whether hit rates, response times and ERPs (i.e., P2 and P3) in the recognition phase are correlated with the ratings and ERPs (i.e., P2, N2 and LPP) in the encoding phase. In addition, we also calculated the correlations between behavioral responses (i.e., hit rates and response times) and ERPs (i.e., P2 and P3) in the recognition phase; as studies of memory have shown that recognition-related behaviors are correlated with ERP components (e.g., P3; Addante et al., 2012; Rugg and Curran, 2007).
to the cued uncertain condition, F(1, 18) = 5.33, p = 0.033, η2p = 0.23. For neutral pictures, however, there was no effect of cued uncertainty, ps. N 0.05. In addition, we did not find a main effect of cued uncertainty, ps. N 0.05. 3.1.2. Hit rates For hit rates, the analysis did not show any main effects or interactions, ps. N 0.05. 3.1.3. Response times The analysis only showed a main effect of emotion, F(1, 18) = 5.96, p = 0.025, η2p = 0.25. In general, response times were longer for
3. Results 3.1. Behavioral results 3.1.1. Ratings on valence The analysis showed a main effect of emotion, with higher ratings for neutral pictures compared to negative pictures, F(1, 18) = 176.94, p b 0.001, η2p = 0.91. More importantly, the interaction between cued uncertainty and emotion was also significant, F(1, 18) = 7.28, p = 0.015, η2p = 0.29. Separate analyses for each emotional category showed that negative pictures were rated higher in the certain condition compared Table 1 Mean of the ratings on valence and its SD for all the experimental conditions. Emotion
Uncertainty Certain
Neutral Negative
Cued uncertain
M
SE
M
SE
5.97 2.38
0.70 0.89
5.97 2.38
0.70 0.89
Fig. 1. Encoding-ERPs at the electrodes Fz, FCz and Cz for all the experimental conditions. Shaded areas correspond to the analysis window for the P2 (130–180 ms), N2 (220– 330 ms) and LPP (450–850 ms).
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Fig. 2. Topographical maps based on mean amplitudes of encoding-P2 (130–180 ms), -N2 (220–330 ms) and -LPP (450–850 ms) for all experimental conditions.
negative pictures compared to neutral pictures. However, we did not find a main effect of cued uncertainty or an interaction between cued uncertainty and emotion, ps. N 0.05.
3.2. ERP results 3.2.1. The encoding phase 3.2.1.1. P2 component. The analysis of the P2 component did not show any main effects or interactions, ps. N 0.05.
Table 3 Mean of the amplitude of P2, N2 and LPP in the encoding phase and their SD for all the experimental conditions. Emotion
Electrode
Uncertainty Certain
Cued uncertain
M
SD
M
SD
Fz FCz Cz Fz FCz Cz
0.97 1.25 1.24 1.16 1.51 1.60
2.98 3.01 2.98 3.50 3.33 3.09
1.01 1.34 1.45 0.80 1.31 1.38
3.57 3.48 3.29 3.45 3.29 3.10
Fz FCz Cz Fz FCz Cz
−3.37 −3.23 −2.38 −3.63 −3.29 −2.07
3.91 3.77 3.40 4.07 3.95 3.61
−3.29 −3.08 −2.18 −4.26 −3.80 −2.49
4.11 3.98 3.45 4.12 3.89 3.60
LPP component Neutral Fz FCz Negative Fz FCz
−0.52 −0.56 0.19 0.39
3.06 2.69 3.49 3.19
−0.61 −0.60 −0.75 −0.44
3.32 3.03 3.39 3.03
P2 component Neutral
Negative
N2 component Neutral
Negative
3.2.1.2. N2 component. The analysis showed a main effect of the electrode, F(1, 20) = 5.96, p = 0.025, η2p = 0.25. The N2 was more negative in the electrodes Fz, p = 0.008 and FCz, p = 0.004, compared to the electrode Cz. There was an interaction between emotion and electrode, F(1, 21) = 8.34, p = 0.007, η2p = 0.32. Separate analysis for each electrode showed that negative pictures compared to neutral pictures evoked larger N2 in the electrodes Fz, F(1, 18) = 10.15, p = 0.005, η2p = 0.36, and FCz, F(1, 18) = 4.67, p = 0.045, η2p = 0.21, but the effect of emotion was not significant in the electrode Cz, ps. N 0.05. More importantly, there was an interaction between cued uncertainty and emotion, F(1, 18) = 5.41, p = 0.032, η2p = 0.23. Further analysis showed that for negative pictures, the N2 was more negative in the uncertain condition as compared to the certain condition, F(1, 18) = 4.67, p = 0.044, η2p = 0.21. However, the effect of cued uncertainty was not significant for neutral pictures, ps. N 0.05. In addition, other main effects or interactions were not significant, ps. N 0.05. 3.2.1.3. LPP component. The analysis showed a main effect of cued anticipation, F(1, 18) = 4.54, p = 0.047, η2p = 0.20. The LPP was generally larger for pictures in the certain condition compared to the cued uncertain condition. Table 4 Mean of the amplitude of P2 and P3 in the recognition phase and their SD for all the experimental conditions. Emotion
Electrode
Uncertainty Certain
P2 component Neutral Negative P3 component Neutral Negative
Cued uncertain
M
SD
M
SD
TP7 TP8 TP7 TP8
1.16 3.31 1.32 2.92
2.91 2.84 2.73 2.50
1.61 2.68 1.28 3.29
2.71 2.51 2.99 2.95
Pz Pz
1.98 3.46
3.76 3.42
2.40 4.18
3.46 3.99
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Fig. 3. Recognition-ERPs at the electrodes TP7 and TP8 for all the experimental conditions. Shaded areas correspond to the analysis window for the P2 (200–240 ms).
In addition, there was an interaction between emotion and electrode, F(1, 18) = 12.08, p = 0.003, η2p = 0.40. However, separate analysis for each electrode showed that the effect of emotion was not significant ps. N 0.05. In addition, other main effects or interactions were not significant, ps. N 0.05.
amplitudes were larger for the pictures in the cued uncertain condition compared to the certain condition and for negative pictures as compared to neutral pictures. In addition, there was no interaction between uncertainty and emotion, ps. N 0.05. 3.3. Correlations between encoding and recognition
3.2.2. The recognition phase 3.2.2.1. P2 component. The analysis yielded significant a main effect of hemisphere, F(1, 18) = 9.01, p = 0.008, η2p = 0.33. The amplitudes were generally larger in the right hemisphere compared to the left hemisphere. More importantly, the three-way interaction among uncued uncertainty, emotion and hemisphere also reached statistical significance, F(1, 18) = 6.64, p = 0.019, η2p = 0.27. Separate analysis for each electrode showed that for the electrode TP7, there were no main effects or interactions, ps. N 0.05. For the electrode TP8, while there were no main effects of uncertainty or emotion, ps. N 0.05; the interaction between these two factors was significant, F(1, 18) = 4.60, p = 0.046, η2p = 0.20. For neutral pictures, the amplitudes were stronger in the certain condition compared to the cued uncertain condition, F(1, 18) = 5.76, p = 0.027, η2p = 0.24, but there was no significant effect of uncertainty for negative pictures, ps. N 0.05. In addition, other main effects or interactions were not significant, ps. N 0.05.
Regarding the behavioral responses in the recognition phase, the analysis showed that in the certain-negative condition, hit rates were positively correlated with LPP in the encoding phase, and response times were correlated with N2 and LPP. With regards to recognition-related ERPs, the P2 was generally negatively correlated with the ERPs (e.g., P2, N2 and LPP) in all experimental conditions. For the P3, the amplitude was also negatively correlated with the LPP in the certain- and the uncertain-neutral condition. Please refer to Table 5 for more details. 3.4. Correlations between recognition-related behaviors and ERPs The analysis showed significant correlations between hit rates and the P3 component in the uncertain-neutral condition, r = 0.46, p = 0.047, and a trend in the certain condition, r = 0.41, p = 0.084. 4. Discussion
3.2.2.2. P3 component. The analysis of the P3 amplitude showed main effects of cued uncertainty, F(1, 18) = 4.98, p = 0.039, η2p = 0.22, and emotion F(1, 18) = 27.62, p b 0.001, η2p = 0.61. In general, the
Fig. 4. Recogntion-ERPs at the electrode Pz for all the experimental conditions. Shaded areas correspond to the analysis window of the P3 (300–450 ms).
In the present study, we investigated whether cued uncertainty about the emotional content of the events affected ERPs in later recognition of the events. Different from our previous study on uncued uncertainty (Lin et al., 2015d), the findings in the present study showed that cued uncertainty reduced P2 amplitudes for neutral pictures; whereas there were no any effects of cued uncertainty for negative pictures. For the P3 component, the amplitudes were generally larger for emotional pictures in the cued uncertain condition compared to the certain condition. The findings indicated that cued uncertainty modulated ERP responses in the later recognition of emotional events in different stages of processing. It has been suggested that encoding, the first stage of memory, is an important prerequisite for later steps, such as recognition (e.g., Erk et al., 2005; Lin et al., 2015c, 2015d; Marzi and Viggiano, 2010). To have a better understanding of the recognition effects, we also investigated the effects of cued uncertainty in the encoding phase. The findings were similar to those in our previous one, particularly for negative pictures (Lin et al., 2015a). Cued uncertainty was found to elicit increased N2 for negative pictures but reduced LPP for both negative and neutral pictures; while we did not find the P2 effects of cued uncertainty observed in our previous study (Lin et al., 2015a), which is possibly in related to the gender of the sample (Jin et al., 2013; Lin et al., 2014b). Considering that the N2 and LPP are related to stimulus encoding
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Fig. 5. Topographical maps based on mean amplitudes of recognition-P2 (200–240 ms) and -P3 (300–450 ms) for all experimental conditions.
(e.g., Azizian and Polich, 2007; Olofsson et al., 2008; Pratt et al., 2011), the findings in the present study suggest that cued uncertainty reduce the encoding of neutral pictures generally, whereas the effects of cued uncertainty on the encoding of negative pictures were different according to the stages of pictorial processing. These encoding effects may influence later recognition effects, such as the P2 and P3. With respect to the P2, this component has been repeatedly suggested to be related to the processing of stimulus features in memory research (e.g., Kaufmann et al., 2013; Stahl et al., 2008; Schulz et al., 2012a, 2012b; Wiese et al., 2013, 2014). Therefore, the present study may suggest that cued uncertainty reduces the processing of features in later recognition of neutral pictures. As shown in the Results section, there were negative correlations between P2 and encoding-LPP. Given that the polarity of ERPs at the anterior scalp sites is thought to be opposite to that at the posterior scalp sites, the P2 amplitude should be positively correlated with the LPP amplitude. That is, the feature processing is positively correlated with the encoding.
As mentioned in the above paragraph, the encoding of neutral pictures in the present study is generally reduced by cued uncertainty. Therefore, it makes sense that the cued uncertainty reduces the feature processing in recognition of neutral pictures. This suggestion is in line with previous studies, which shows enhanced processing of features reflected in the P2 during recognition of deeply compared to shallowly encoded stimuli (e.g., Kaufmann et al., 2013; Stahl et al., 2008; Schulz et al., 2012a, 2012b; Wiese et al., 2013, 2014). However, the P2 effect of cued uncertainty was not observed for negative pictures, suggesting that the processing of features is similar during recognition of certain compared to uncertain negative pictures. As shown in the Results section, the P2 to both certain and uncertain negative pictures was negatively correlated with the encoding-N2 and -LPP. Therefore, the processing of features during recognition of negative pictures may also be positively correlated with the encoding, similar to neutral pictures. As mentioned above, the effects of cued uncertainty on the encoding of negative pictures are suggested to be
Table 5 Correlations between encoding and recognition. Indexes in the recognition phase
Condition
Behavior Hit rates Response times ERPs P2
Electrode TP7
Electrode
LPP N2 LPP
Fz, FCz Cz Fz, FCz
0.46, 0.49 0.46 0.46, 0.47
0.050, 0.033 0.048 0.048, 0.044
Certain-neutral Uncertain-neutral
N2 P2 N2 P2 N2 LPP N2 P2 N2 LPP P2 N2 LPP P2 N2 P2 N2 LPP LPP LPP
FCz, Cz Cz Fz, FCz, Cz Fz, FCz, Cz Fz, FCz, Cz Fz Fz, FCz, Cz Fz, FCz, Cz Fz, FCz, Cz Fz Fz, FCz, Cz Fz, FCz, Cz Fz, FCz Fz, FCz, Cz Fz, FCz, Cz FCz, Cz Fz, FCz, Cz Fz Fz, FCz Fz
−0.48, −0.53 −0.46 −0.51, −0.56, −0.60 −0.54, −0.57, −0.63 −0.65, −0.71, −0.76 −0.49 −0.53, −0.57, −0.60 −0.48, −0.49, −0.53 −0.54, −0.53, −0.59 −0.522 −0.54, −0.57, −0.57 −0.65, −0.68, −0.73 −0.55, −0.53 −0.46, −0.50, −0.51 −0.62, −0.63, −0.68 −0.47, −0.54 −0.60, −0.68, −0.78 −0.50 −0.58, −0.55 −0.48
0.038, 0.019 0.047 0.027, 0.013, 0.006 0.017, 0.011, 0.004 0.003, 0.001, b0.001 0.034 0.021, 0.011, 0.007 0.039, 0.035, 0.020 0.016, 0.020, 0.007 0.022 0.017, 0.011, 0.011 0.003, 0.001, b0.001 0.015, 0.020 0.047, 0.028, 0.026 0.004, 0.004, 0.001 0.041, 0.017 0.006, 0.001, b0.001 0.030 0.010, 0.014 0.039
Uncertain-negative Certain-neutral
Certain-negative Uncertain-negative
Pz
p
ERPs
Uncertain-neutral
P3
r
Certain-negative Certain-negative
Certain-negative
TP8
Indexes in the encoding phase
Certain-neutral Uncertain-neutral
Note that only significant effects, p b 0.05, were reported.
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altered in different stages of processing. These altered encodings may result in the reduction of the effects of cued uncertainty on feature processing. In line with the findings in the present study, our previous study on cued uncertainty also found similar P2 effects over the right inferior temporal-parietal scalp sites (Lin et al., 2015d). However, the effects in our previous study were shown for negative pictures but not for neutral pictures (Lin et al., 2015d). In our previous study, cues were shown only prior to the encoding of certain emotional pictures (Lin et al., 2015d). Studies have suggested that cues indicating an upcoming negative event increased the encoding of the event (Lin et al., 2012, 2014b; Onoda et al., 2006, 2007), whereas this may be not the case for no cues (Lin et al., 2012; Onoda et al., 2007) or cues indicating an upcoming non-negative event (Onoda et al., 2006, 2007). Therefore, uncued uncertainty may affect the encoding of negative pictures but not of neutral pictures, resulting in observing the effects of uncued uncertainty regarding feature processing only for negative pictures. In our present study, however, pictures in the encoding phase were always preceded by cues. As mentioned above, cued uncertainty was suggested to reduce the encoding of neutral pictures in general but alter that of negative pictures in different directions at different stages of pictorial processing, resulting in different results compared to those in our previous study (Lin et al., 2015d). Another finding in the present study was that pictures evoked larger P3 amplitudes in the cued uncertain compared to the certain condition, regardless of the emotional content of the pictures. Several studies have indicated that the P3 reflects the allocation of attentional resources (e.g., Olofsson et al., 2008; Polich, 2007), with increased amplitudes for attended stimuli (e.g., Langeslag et al., 2009; Lin et al., 2015b, 2015d, 2016). This component is also supposed to be associated with stimulus retrieval in memory research (e.g., Curran and Cleary, 2003; Marzi and Viggiano, 2010; Rugg et al., 1998; Weymar et al., 2013). Therefore, the findings in the present study may suggest that cued uncertainty generally enhances the attention allocation during retrieval of the pictures. As is shown in the Results section, the P3 for neutral pictures was found to be negatively correlated to the encoding-LPP, regardless of cued uncertainty. For negative pictures, there were no correlations between the P3 and ERPs in the encoding phase. These findings may suggest that the P3 effects on negative and neutral pictures resulted from different factors. For neutral pictures, the P3 effects of cued uncertainty may be closely related to the encoding. However, it may not be the case for negative pictures. Previous studies have suggested that cued uncertainty produces some other long-term effects other than the recognition effects. For example, participants reported being more worried and anxious for uncertain cues compared to certain cues even after the encoding phase (Gole et al., 2012). Participants overestimated the impact of negative pictures following uncertain cues in post-experiment questions (Sarinopoulos et al., 2010). These long-term effects elicited by cued uncertainty may re-enhance salience after the encoding, resulting in enhancing the attentional allocation during later recognition of uncertain negative pictures. However, as no studies - to the best of our knowledge - have ever investigated the effects of cued uncertainty in the intervals between encoding and recognition (e.g., the consolidation phase); our suggestions should be investigated in future studies for more details. We would like to provide some limitations of the present study and suggest outlines for future research. Firstly, we did not find any effects of cued uncertainty on behavioral responses (e.g., hit rates and response times) in recognition of emotional pictures; whereas for neutral pictures, there was a trend in hit rates. Previous studies on non-emotional stimuli have suggested that the P3 is relevant to decision making (e.g., O'connell et al., 2012; Twomey et al., 2015). In the present study, hit rates were found to be (at least slightly) correlated with recognitionP3 for neutral pictures and moreover, there was a P3 effect of cued uncertainty, possibly suggesting the effect of hit rates. The absence of the effects of hit rates may be in related to the small sample size. Future studies may enlarge the sample size to further investigate related issues.
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In addition, the dimensional model of emotion (e.g., Barrett, 1995, 1998) suggests that emotional information can be encoded in two dimensions, valence and arousal. Therefore, subsequent studies may manipulate the uncertainty of valence and arousal to further investigate related issues. 5. Conclusions The present study investigated whether cued uncertainty about the emotional content of an upcoming event modulates later recognition of the event. We found that neutral pictures evoked smaller P2 amplitudes in the cued uncertain condition compared to the certain condition, but this uncertainty effect was not shown for negative pictures. Additionally, emotional pictures generally elicited increased P3 amplitudes in the cued uncertain condition. Therefore, the findings may indicate that uncertainty modulated recognition of emotional pictures with regards to feature processing and attentional allocation. Acknowledgements This work was supported by the Project of Key Research Institute of Humanities and Social Science Department of Province Construction in China (13JJD190007). References Addante, R.J., Ranganath, C., Yonelinas, A.P., 2012. Examining ERP correlates of recognition memory: evidence of accurate source recognition without recollection. NeuroImage 62 (1), 439–450. Azizian, A., Polich, J., 2007. Evidence for attentional gradient in the serial position memory curve from event-related potentials. J. Cogn. Neurosci. 19 (12), 2071–2081. Bai, L., Ma, H., Huang, Y., Luo, Y., 2005. The development of native Chinese Affective Picture System - a pretest in 46 college students. Chin. Ment. Health J. 18, 719–722 (in Chinese). Barrett, L.F., 1995. Valence focus and arousal focus: individual differences in the structure of affective experience. J. Pers. Soc. Psychol. 69 (1), 153–166. Barrett, L.F., 1998. Discrete emotions or dimensions? The role of valence focus and arousal focus. Cognit. Emot. 12 (4), 579–599. Curran, T., Cleary, A.M., 2003. Using ERPs to dissociate recollection from familiarity in picture recognition. Cogn. Brain Res. 15 (2), 191–205. Dieterich, R., Endrass, T., Kathmann, N., 2016. Uncertainty is associated with increased selective attention and sustained stimulus processing. Cogn. Affective Behav. Neurosci. 16 (3), 447–456. Erk, S., Martin, S., Walter, H., 2005. Emotional context during encoding of neutral items modulates brain activation not only during encoding but also during recognition. NeuroImage 26 (3), 829–838. Galli, G., Wolpe, N., Otten, L.J., 2011. Sex differences in the use of anticipatory brain activity to encode emotional events. J. Neurosci. 31 (34), 12364–12370. Galli, G., Griffiths, V.A., Otten, L.J., 2014. Emotion regulation modulates anticipatory brain activity that predicts emotional memory encoding in women. Soc. Cogn. Affect. Neurosci. 9 (3), 378–384. Gole, M., Schäfer, A., Schienle, A., 2012. Event-related potentials during exposure to aversion and its anticipation: the moderating effect of intolerance of uncertainty. Neurosci. Lett. 507 (2), 112–117. Grupe, D.W., Nitschke, J.B., 2011. Uncertainty is associated with biased expectancies and heightened responses to aversion. Emotion 11 (2), 413–424. Grupe, D.W., Nitschke, J.B., 2013. Uncertainty and anticipation in anxiety: an integrated neurobiological and psychological perspective. Nat. Rev. Neurosci. 14 (7), 488–501. Hsieh, L.T., Hung, D.L., Tzeng, O.J.L., Lee, J.R., Cheng, S.K., 2009. An event-related potential investigation of the processing of Remember/Forget cues and item encoding in itemmethod directed forgetting. Brain Res. 1250, 190–201. Jin, Y., Yan, K., Zhang, Y., Jiang, Y., Tao, R., Zheng, X., 2013. Gender differences in detecting unanticipated stimuli: an ERP study. Neurosci. Lett. 538, 38–42. Kaufmann, J.M., Schulz, C., Schweinberger, S.R., 2013. High and low performers differ in the use of shape information for face recognition. Neuropsychologia 51 (7), 1310–1319. Lang, P.J., Bradley, M.M., Cuthbert, B.N., 2008. International affective picture system (IAPS): affective ratings of pictures and instruction manual. Technical Report A-8. Langeslag, S.J., Morgan, H.M., Jackson, M.C., Linden, D.E., van Strien, J.W., 2009. Electrophysiological correlates of improved short-term memory for emotional faces. Neuropsychologia 47 (3), 887–896. Lin, H., Gao, H., Wang, P., Tao, L., Ke, X., Zhou, H., Jin, H., 2012. Expectation enhances eventrelated responses to affective stimuli. Neurosci. Lett. 522 (2), 123–127. Lin, H., Gao, H., You, J., Liang, J., Ma, J., Yang, N., ... Jin, H., 2014a. Larger N2 and smaller early contingent negative variation during the processing of uncertainty about future emotional events. Int. J. Psychophysiol. 94 (3), 292–297. Lin, H., Liang, J., Xie, W., Li, S., Xiang, J., Xu, G., ... Jin, H., 2014b. Sex differences in the modulation of emotional processing by expectation. Neuroreport 25 (12), 938–942.
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