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/lp/springer-journals/expectation-modulates-the-preferential-processing-of-task-irrelevant-ITQYtsxy5q
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- Springer Journals
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- Copyright © The Author(s) 2022
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- 1744-9081
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- 10.1186/s12993-022-00203-6
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Abstract
Background: Reporting the second of the two targets is impaired when it occurs 200–500 ms after the first, the phenomenon in the study of consciousness is the attentional blink (AB). In the AB task, both the emotional salience and the expectation of the second target increase the likelihood of that target being consciously reported. Yet, little is known about how expectations modulate the prioritized processing of affective stimuli. We examined the role of expecting fearful expression when processing fear in an AB task. Participants were presented with an AB task where the 2nd target ( T2) is either a fearful face or a neutral face, and had to report the target’s gender. The frequency of fearful to neutral faces on a given block was manipulated, such that participants could either expect more or less fear- ful faces. Results: In the Experiment 1, we found that fearful faces were more likely to be recognized than neutral faces during the blink period (lag3) when participants were not expecting a fearful face (low fear-expectation); however, high fear- expectation increased the discrimination of fearful T2 than neutral T2 outside the blink period (lag8). In the Experi- ment 2, we assessed ERP brain activity in response to perceived T2 during the blink period. The results revealed that fearful faces elicited larger P300 amplitudes compared to neutral faces, but only in the low fear-expectation condition, suggesting that expecting a fearful expression can suppress the processing of task-irrelevant facial expression and unexpected fearful expression can break through this suppression. Fearful T2 elicited larger vertex positive potential ( VPP) amplitudes than neutral T2, and this affective effect was independent of fear-expectation. Since no effect of expectation was found on the VPP amplitude while P300 exhibited significant interaction between expectation and expression, this suggests that expectations modulate emotional processing at a later stage, after the fearful face has been differentially processed. Conclusions: These results provided clear evidence for the contribution of the expectation to the prioritized process- ing of second affective stimuli in the AB. Keywords: Expectation, Fear, Attentional blink, Event-related potentials Introduction Rapid and accurate identification of facial emotions is *Correspondence: zhangqin@cnu.edu.cn a very important skill during social interactions. It has Learning and Cognition Key Laboratory of Beijing, School of Psychology, been showed that fearful expression relative to neutral Capital Normal University, No.105, North Road of Western 3Rd-Ring, expression automatically attracts attention and is pref- Beijing 100048, China Full list of author information is available at the end of the article erentially processed [2, 28, 51].This was illustrated in an © The Author(s) 2022. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Sun et al. Behavioral and Brain Functions (2022) 18:16 Page 2 of 12 attentional blink (AB) paradigm in which participants of T2 [6, 23, 24, 37, 43, 55]. However, whether attentional were instructed to detect two targets (T1 and T2) among resources could be preferentially allocated to emotional a rapid serial visual presentation (RSVP) of distractors at information is controversial in the implicit emotional a rate of about 10 Hz. In this task, the detection ability of AB task in which emotional features were task-irrele- the second target (T2) is impaired when two targets are vant. On the one hand, task-irrelevant expressions were separated by a short temporal interval between 200 and found to facilitate the recognition of face identity in an 500 ms, a phenomenon called the ‘attentional blink’ [5, implicit emotional AB task [3, 7]. For instance, Engen 38]. Interestingly, some studies have reported that emo- et al. [14] showed that fearful T2 could decrease the tional T2 attenuated the AB [2, 29, 37]. For example, par- AB compared with neutral T2 even when participants ticipants were more likely to detect T2 if it was a fearful reported the gender of facial stimuli. On the other hand, face instead of a neutral face in the AB task [7, 28]. task-irrelevant expressions didn’t affect the performance Some researchers suggested that the enhanced bottom- in other implicit emotional AB tasks [44, 47]. For exam- up neural activation of coding for emotional stimuli was ple, Sun et al. [47] showed that the prioritized processing involved in the preferential attentional processing of of fearful facial expression in the AB task could only be emotional information [1, 6, 29]. The amygdala is thought observed when the facial expression had to be reported, to be involved in the early detection of emotional stim- but not when the faces’ gender was target. We speculated uli and facilitates the perception of emotional infor- that the inconsistency of these results in the implicit mation via a substantial projection to the visual region emotional tasks was likely due to the top-down regula- [2, 7]. Many event-related potential (ERP) studies have tion of emotional expectation on the prioritized emo- shown rapid enhancement of sensory-perceptual pro- tional processing, which might be suppressed when the cessing (about 200 ms after T2 onset) at posterior sen- expectation of upcoming emotional stimuli was formed. sors when participants detected an emotional T2 rather Here, we primarily focused on the mechanism of than a neutral T2 in an AB task [18, 23]. Other research- how expectation affected the emotional processing in ers proposed that in addition to this bottom-up mecha- the implicit emotional AB task, in which T2 was either nism, the top-down mechanism of expectation-driven a fearful face or a neutral face and participants were biases to emotional information may also be involved in instructed to report the gender of T2. Crucially, the the attenuation effect of emotional T2 on AB [27, 29]. probability of fearful T2 was manipulated to form emo- Participants might form expectations for the frequency tional expectation by using the block-by-block method, of emotional stimuli based on the enhanced detec- so that fearful targets (60%) occurred more often than tion of emotional T2 in the previous trials, even though neutral targets (20%) or T2-absent distractors (20%) in the frequency of the two types of stimuli was the same. the high fear-expectation block while the probability of Such emotional expectation could modify the percep- fearful and neutral faces was 20% and 60% respectively tual processing of emotional stimuli in two top-down in the low fear-expectation block. In Experiment 1, par- ways via top-down projections from higher-level brain ticipants were instructed to report the scene of T1 and regions, such as the frontal cortex [27, 46]. The first is then discriminate the gender of T2 at the end of each that the expectation could speed up the perceptual pro- stream. T2 was presented at third position (lag3; Stimuli cessing of emotional stimuli by increasing the activation Onset Asynchrony, SOA = 201 ms) or eighth position of sensory representations of emotional stimuli [12, 19, (lag8; SOA = 536 ms) after T1. The effect of emotional 21]. The other mechanism is that when the forthcom - expectation on the preferential processing of fear was ing emotional information is task-irrelevant, expecta- tested by comparing the correct reports of fearful T2 and tion could reduce the sensitivity of the brain to emotional neutral T2, given the T1 was identified correctly in the stimuli by selectively suppressing the perceptual repre- same trial. In this task, facial expression is task-irrelevant sentation of emotional information [17, 53, 54]. However, information. As one of the central cognitive functions what role emotional expectation plays in the attenuation of the human brain, expectation is generated by learn- effect of emotional T2 on attentional blink is still largely ing from prior experiences to optimize future behavioral unknown. responses [45]. The expectation of forthcoming fearful Several findings suggested that the explicit relevance face based on its probability might modulate the repre- of expression to the task was a prerequisite for prior- sentation of task-relevant facial expression. In an implicit itized processing of facial expression [14, 44]. Indeed, emotional task, Yang et al. [53] reported that fearful faces the enhanced perception of emotional T2 stimuli com- and neutral faces elicited similar ERP responses in the pared with neutral T2 stimuli has been confirmed to be expected condition, whereas unexpected fearful faces robust in the explicit emotional AB task, in which par- elicited increased P200 amplitudes than neutral faces, ticipants were instructed to attend to emotional features indicating that emotional expectation could suppress the Sun et al. Behavioral and Brain Functions (2022) 18:16 Page 3 of 12 brain susceptibility to task-irrelevant facial expression. 18–26 years, 22.8 ± 2.1 years), and twenty-seven par- u Th s, we hypothesized that emotional expectation might ticipants for Experiment 2 (15 females; age, 19–27 years, inhibit the preferential processing of task-irrelevant 22.2 ± 2.4 years). All participants signed an informed facial expression in the high fear-expectation condition, consent form before the experiment. This study was thereby reducing the attenuation effect of fear on AB, approved by the Capital Normal University Institutional while unexpected fearful faces might break out the sup- Review Board. pressive effect, and then appear greater attenuation effect of fear on AB in the low fear-expectation condition. Procedure and stimuli In Experiment 2, we used the ERP to track the neural Stimuli were presented using the Presentation software representations of T2 during the short T1-T2 interval (Neurobehavioral Systems Inc., https:// www. neuro bs. (lag3). We proposed that the modulation effect of expec -com/ prese ntati on) and displayed on a 19-inch CRT tation might be related to the later processing repre- monitor (1280 × 1024; 60 Hz) on a black (RGB:0, 0, 0) sented by the P300, a large-amplitude late positive ERP background. The viewing angle of each photograph was component that appears in the central-parietal region, 5.73 × 8.37°. The participants were seated in a quiet, peaking at 300–600 ms after stimulus presentation [10, dimly-lit room, 100 cm away from the screen, and then 35]. Numerous researchers have proposed that the P300 performed an adapted RSVP task, in which a rapid series variously implicates the encoding of stimulus salience of visual stimuli for every trial consisted of two tar- and probability [10, 13, 36], decision-making [39, 49], gets and 18 scrammed faces as distractors. We selected and context updating [34]. And in the AB task, the P300 40 copyright-released scenic photographs (half of the is considered as an index of successful consolidation for photographs depicted indoor scenes and the other half the detected T2 [20, 56]. Specifically, we hypothesized depicted outdoor scenes) from the Internet as T1 stimuli. that fearful faces would elicit enhanced P300 amplitudes The indoor scenes were photographs of drawing rooms compared to neutral faces only in the low fear-expecta- and kitchens while the outdoor scenes were photographs tion condition. By contrast, this later emotional effect of buildings, with no people or animals. might be decreased or disappeared in the high fear- T2 stimuli included 40 faces (20 fearful faces and 20 expectation condition. Previous studies have shown bet- neutral faces) taken from the NimStim face database ter performance for emotional T2 was associated with (http:// www. macbr ain. org/ resou rces. htm) [48], which early enhanced perceptual processing reflected by early consisted of half male and half female. These T2 stimuli ERP components such as the vertex positive potential were used in another study and their valence, arousal (VPP), which represented a stimulus-driven automatic and fearfulness have been described previously [47]. The attentional processing [18, 23]. And some top-down fac- distractor items included 24 scrambled faces that were tors have little influence on this early emotional effect created by another six neutral faces selected from the [22, 40]. Hence, we hypothesized that expectation did NimStim face database. For every neutral face, their facial not influence the early emotional effect reflected by VPP, features were divided into 12 × 8 squares and randomly but inhibited the later consolidation of facial expression rearranged to a scrambled face. All scrambled faces and reflected by P300. T2 faces were cropped into an oval shape to exclude hair, ears, and neck information, then converted into greyscale Methods with constant luminance using the Adobe Photoshop Participants CS5. The full-color scenic T1 stimuli were also cropped Thirty-two students participated in Experiment 1 (18 into an oval shape to control the stimuli size. The sali - females; age, 18–26 years, 22.7 ± 2.1 years). Thirty stu - ency of T1 stimuli was to make sure the identification of dents participated in Experiment 2 (17 females; age, T1 and kept consistent in the high and low expectation 19–27 years, 22.2 ± 2.3 years). All participants were right- blocks. handed and had normal or corrected-to-normal vision. Due to high false alarm rate (incorrect response to T2 Experiment 1 absent trials, ≥ 50%), two participants were excluded This was an implicit emotional expectation task and from analyses in Experiment 1 and one participant was no verbal instruction about the high or low expecta- excluded from analyses in Experiment 2. Furthermore, tion of fear was given to participants. Participants were two participants with less than sixteen remaining epochs instructed to discriminate scene (T1: indoor scene or in the high-probability fear condition (usually for neu- outdoor scene) and gender (T2: female or male) within tral faces, which had less trials) were excluded from a rapid series of scrambled faces. Each RSVP stream ERP analyses in Experiment 2. In the end, we included began with a 1 s presentation of a white fixation cross, 30 participants for Experiment 1 (17 females; age: followed by 20 sequential images that were presented Sun et al. Behavioral and Brain Functions (2022) 18:16 Page 4 of 12 for 67 ms each at the center of the screen (see Fig. 1). short rest between blocks to avoid fatigue, and the whole T1 was always presented at the sixth or eighth posi- experiment required about 40 min to complete. tion of the RSVP. In most trials (80%), T1 was followed by a second target at lag3 (SOA = 201 ms), or lag8 Experiment 2 (EEG) (SOA = 536 ms). In the remaining trials (T2-absent tri- The stimuli and procedure for Experiment 2 were identi - als, 20%), a scrambled face was presented at the time cal to Experiment 1, except that the lag8 condition was point where T2 supposed to be. At the end of each trial, absent in the Experiment 2. T2 was always presented at participants were instructed to discriminate the scene lag 3 (i.e., T2 and T1 were separated by 2 distractors) of the first target by pressing button (the D key for relative to T1. Again, Experiment 2 consisted of two high “indoor” and the F key for “outdoor”), then judge the fear-expectation blocks and two low fear-expectation gender of the second target (the J key for “male face”, blocks (400 trials over four blocks). First, participants the K key for “female face”, the L key for “face absent”). prepared for the EEG measurements and received brief The response timeout durations were 2 s and partici - instructions about the task. Then, participants performed pants were instructed to focus on accuracy rather than four blocks of 100 trials each in the AB task. response speed. EEG data were recorded by a NeuroScan Amplifier Experiment 1 included a practice block of 20 trials and (Neuroscan SynAmps) with 64 electrodes embedded in four test blocks of 100 trials each. There were two high an elastic cap using the extended 10–20 International fear-expectation blocks and two low fear-expectation System, along with one online reference electrode on the blocks. For high fear-expectation condition, 60% of tri- left mastoid and four electrodes measuring the vertical als were fearful T2 trials (60 trials per block), 20% were electrooculograms and the horizontal electrooculograms. neutral T2 trials, and 20% were T2 absent trials. For low The electroencephalogram was collected with a band - fear-expectation condition, 20% of trials were fearful pass of 0.05–100 Hz during recording. The sampling rate T2 trials, 60% were neutral T2 trials, and 20% were T2 was 500 Hz and the resistance of all electrodes was kept absent trials. The scene of T1 was balanced to the expres - below 5 kΩ. After data acquisition, the offline EEG data sion and gender of T2 stimuli. Participants practiced 20 were preprocessed with the EEGLAB toolbox (v14.1.1) trials to familiarize themselves with the procedure before for MATLAB-2015a [9]. First, data were re-referenced to the formal experiment. The order of the high fear-expec - the average of the left and right mastoids, high-pass fil - tation condition and low fear-expectation condition was tered at 0.05 Hz, low-pass filtered at 30 Hz, and epoched balanced across participants. Participants could take a from − 200 to 800 ms surrounding the onset of T2 Fig. 1 Task design of Experiment 1 and 2. Participants were instructed to judge the scene of the T1 (an outdoor or an indoor scene) and then judged the gender (female, male, or face absent) of the face in the T2 Sun et al. Behavioral and Brain Functions (2022) 18:16 Page 5 of 12 trials and correct rejections of T2-absent trials. T2 accu- stimuli. Baseline correction was applied using the aver- racy was analyzed by using a 2 × 2 × 2 repeated-measures age amplitude before T2 onset (− 200 to 0 ms). Second, analyses of variance (ANOVA) with three factors which we rejected some significant artifacts (i.e., large muscle are fear-expectation (high, low), expression (fearful, neu- activity produced by cough or swallow) not related to eye tral), and lag (Lag3, Lag8). blinks with visual inspection. As a final step, the inde - pendent component analysis (ICA) was used to identify Experiment 2 (EEG) and remove components associated with eye blinks and The method of behavioral analyses for Experiment 2 muscle tension from the EEG data [4]. In this step, we were similar to those for Experiment 1. However, Experi- used the EEGLAB’s default algorithm ‘runica’, which per- ment 2 did not conclude factor lag. T2 behavioral perfor- form ICA decomposition of input data using the logistic mance was analyzed by using a 2 × 2 repeated-measures infomax ICA algorithm with the natural gradient feature. ANOVA with the factors fear-expectation (high, low), Only trials with correct responses to both T1 and T2 and expression (fearful, neutral). All EEG analyses were targets were included for EEG analyses. The numbers of based on trials where T1 and T2 were correctly identi- epochs retained for analyses (mean, median and range) fied. The two-way repeated measures ANOVAs on the for each condition of interest were as follows: high prob- mean amplitudes of the VPP and P300 components were ability condition, fearful faces (Mean ± SD, 89.2 ± 20.7, performed with the fear-expectation (two levels: high and Median: 91, Range: 38–114), neutral faces (Mean ± SD, low), and expression (two levels: fearful and neutral), as 30.6 ± 5.6, Median: 30, Range: 19–40); low probability within-subjects factors. P values were corrected by the condition, fearful faces (Mean ± SD, 30.6 ± 6.7, Median: Greenhouse–Geisser correction. Bayesian analyses were 32, Range: 16–39), neutral faces (Mean ± SD, 92.7 ± 16.3, performed to quantify the evidences for the null hypoth- Median: 99, Range: 56–113). esis using JASP 0.10.2.0 (JASP Team, 2019, Amsterdam, In Experiment 2, we mainly focused on the VPP and The Netherlands), with default JASP Cauchy priors. We P300 components elicited by T2 stimuli. T2-locked aver- computed the Bayes Factor (BF) of each effect with BF age ERPs under different conditions were computed denoting the evidence for the alternative hypothesis and separately for each participant as the difference between BF denoting the evidence for the null hypothesis. We T1-T2 trials and T2-absent trials (i.e. the average ERP interpreted BF from 1 to 3 as weak evidence in favor of of fearful faces condition subtracts the average ERP in either hypothesis, values from 3 to 10 as moderate, and T2-absent trials). The choices about electrode sites of those above 10 as strong evidence in favor of either con- VPP and P300 components was based on previous stud- clusion [16]. ies with a similar design to the present study [23, 47]. And the choices of time window for certain ERP compo- Results nents were based on the grand-averaged ERP activity of Experiment1 the present study. We calculated mean amplitude in the First, the T1 performance was analyzed. The mean relevant time window symmetrically centered around accuracy of T1 discrimination across all conditions the peak latency for each component, with a shorter time was 92.7 ± 1.2% (M ± SE, the same below). A three- window length (40 ms) for the VPP components and a way ANOVA with factors of the fear-expectation (high, longer time window length (100 ms) for the P300 compo- low), expression (fear, neutral) and lag (lag3, lag8) nent. We calculated the VPP amplitudes at the electrode was conducted on T1 accuracy. The main effect of lag sites of FC3, FCz, FC4, C3, Cz, and C4 between 180 and was significant [F(1, 29) = 4.95, p = 0.034, η2 p = 0.15, 220 ms. The P300 amplitudes were measured with FC3, BF = 1.21], with higher T1 accuracy at the lag3 condi- FCz, FC4, C3, Cz, C4, CP3, CPz, CP4, P3, Pz, and P4 tion (93.4 ± 1.1%) than at the lag8 condition (92 ± 1.3%). from 470 to 570 ms. Other main effects [fear-expectation: F(1, 29) = 0.79, p = 0.38, BF = 5.2; expression: F(1, 29) = 0.798, p = 0.38, Statistical analysis BF = 4.99] and interactions [fear-expectation × expres- Experiment 1 sion: F(1, 29) = 2.02, p = 0.17, BF = 2.53; fear-expec- First, T1 accuracy was analyzed by using a 2 × 2 × 2 tation × lag: F(1, 29) = 0.59, p = 0.45, BF = 3.74; repeated-measures analyses of variance (ANOVA) with expression × lag: F(1, 29) = 0.32, p = 0.58, BF = 3.56; three factors which are fear-expectation (high, low), fear-expectation × expression × lag: F(1, 29) = 1.38, expression (fearful, neutral), and lag (Lag3, Lag8). Then, p = 0.25, BF = 1.97] were not significant. we analyzed the percentage of correct T2 reports from The mean accuracy of T2 discrimination across all con - trials in which T1 was accurately identified (T2|T1), con - ditions was 68.1 ± 3.1%. An ANOVA with the fear-expec- sistent with the previous study [38]. First, we calculated tation (high, low), expression (fear, neutral) and lag (lag3, T2 accuracy based on the correct reports of T2-presented Sun et al. Behavioral and Brain Functions (2022) 18:16 Page 6 of 12 lag8) as factors on T2 discrimination was performed and other interactions [fear-expectation × expression: (Fig. 2). The main effect of fear-expectation was signifi - F(1, 29) = 1.29, p = 0.27, BF = 3.46; expression × lag: cant [F(1, 29) = 8.05, p = 0.008, η2 p = 0.22, BF = 3.22]. F(1, 29) = 0.24, p = 0.63, BF = 4.28] were not significant T2 performance was significantly better in the low fear- Fig. 3. expectation condition (69.7 ± 3.1%) than that in the high We split the sample to “blinkers” (who do show an AB) fear-expectation condition (66.5 ± 3.2%). The main effect and “non-blinkers” (who do not show an AB) based on of expression was significant [F(1, 29) = 4.71, p = 0.04, η2 whether participants showed an AB effect in the neu - p = 0.14, BF = 1.96], with higher T2 accuracy for fear- tral condition or not. AB magnitude was calculated as ful T2 (69.6 ± 2.8%) than for neutral T2 (66.7 ± 3.5%). the percentage of decrement in T2 performance (given Besides, the interaction between the fear-expectation that T1 was accurately identified) relative to T1 perfor - and lag was significant [F(1, 29) = 13.96, p = 0.001, η2 mance at the lag3 condition according to the following p = 0.33, BF = 16.8]. Simple effect analysis revealed formula: (T1 -T2|T1 )/T1 × 100%. According to lag3 lag3 lag3 that there was no significant difference in mean accuracy the criteria of blinkers and non-blinkers proposed by between high fear-expectation condition (69.3 ± 3.1%) Martens and Valchev [25], six participants with an AB and low fear-expectation condition (68.7 ± 3.2%) in the magnitude of 10% or less were classified as non-blinkers lag8 condition (p = 0.605), but the accuracy in high fear- (mean = − 3.03%), another twenty-four participants as expectation condition (63.7 ± 3.7%) was lower than that blinkers (mean = 36.12%). For blinkers, an ANOVA with in the low fear-expectation condition (70.8 ± 3.3%) in the fear-expectation (high, low), expression (fear, neutral) the lag3 condition (p < 0.001). More importantly, the and lag (lag3, lag8) as factors on T2 discrimination was interaction of the fear-expectation, expression and lag performed. Still, we observed a similar pattern of results. was significant [F(1, 29) = 5.32, p = 0.03, η2 p = 0.16, The main effects of the fear-expectation [F(1, 23) = 11.93, BF = 0.56]. Further simple effect analysis revealed p = 0.002, η2 p = 0.34, BF = 5.04] and the expression that in the high fear-expectation condition, there was [F(1, 23) = 10.15, p = 0.004, η2 p = 0.31, BF = 19.93] a significant expression effect in the lag 8 condition were significant. The interaction between the fear- only, with significantly higher accuracy of fearful faces expectation and lag was significant, F(1, 23) = 15.69, than neutral faces [F(1, 29) = 4.92, p = 0.04, η2 p = 0.15, p = 0.001, η2 p = 0.41, BF = 27.17. And the interaction BF = 1.73; fear: 71.2 ± 2.7%; neutral: 67.5 ± 1.6%]. In of the fear-expectation, expression and lag was significant addition, in the low fear-expectation condition, the [F(1, 23) = 6.06, p = 0.022, η2 p = 0.21, BF = 1.19]. Fur- expression effect was significant in the lag 3 condition ther simple effect analysis revealed that in the high fear- only, with significantly higher accuracy of fearful faces expectation condition, there was a significant expression than neutral faces [F(1, 29) = 7.4, p = 0.01, η2 p = 0.2, effect in the lag 8 condition only, with significantly BF = 4.16; fear: 74.0 ± 3.3%; neutral: 67.6 ± 3.8%]. The higher accuracy of fearful faces than neutral faces (fear: main effect of lag [F(1, 29) = 0.78, p = 0.38, BF = 2.53] 68.6 ± 3.1%; neutral: 63.3 ± 4.0%, p = 0.01]. In addition, in Fig. 2 Behavioral results of Experiment 1. Mean percentage of the correct T2 identification for fearful and neutral faces in the high fear-expectation condition A and in the low fear-expectation condition B, depicted separately for the lag3 and lag8 condition Sun et al. Behavioral and Brain Functions (2022) 18:16 Page 7 of 12 Fig. 3 ERP data of the correct discrimination for the T1 and T2 in Experiment 2. Grand-average ERPs for fearful (High Fear-ex Fearful, magenta line) and neutral faces (High Fear-ex Neutral, black line) in the high fear-expectation condition, and fearful (Low Fear-ex Fearful, red line) and neutral faces (Low Fear-ex Neutral, blue line) in the low fear-expectation condition at the Fz, Cz, and Pz A; the difference waveforms and 95% confidence interval of ERPs generated by fearful faces minus neutral faces for the high fear-expectation condition (black line) and the low fear-expectation condition (blue line) at the Fz, Cz, and Pz A. The scalp topographies of difference waves between fearful faces and neutral faces in the high and low fear-expectation conditions at 180–220 ms and 470–570 ms B. The bar graphs showing the average amplitude of the four conditions (the fear-expectation × expression) for VPP and P300 C the low fear-expectation condition, the expression effect fear-expectation [F(1, 26) = 0.01, p = 0.99, BF = 3.69] was significant in the lag 3 condition only, with signifi - were not significant. cantly higher accuracy of fearful faces than neutral faces The mean accuracy of T2 across all conditions was (fear: 71.7 ± 3.7%; neutral: 62.7 ± 4.1%, p = 0.001]. The 78.9 ± 2.7%. A two-way ANOVA with factors of the fear- main effect of lag [F(1, 23) = 1.28, p = 0.27, BF = 1.19] expectation (high, low) and expression (fear, neutral) and other interactions [fear-expectation × expression: performed on T2 discrimination did not reveal signifi - F(1, 23) = 1.22, p = 0.28, BF = 3.89; expression × lag: F(1, cant main effects of the fear-expectation [F(1, 26) = 2.99, 23) = 0.85, p = 0.37, BF = 4.32] were not significant. p = 0.096, BF = 1.02] and the expression [F(1, 26) = 0.37, 01 01 p = 0.546, BF = 4.06]. The interaction effect between the fear-expectation and the expression was also not signifi - Experiment 2 cant [F(1, 26) = 0.64, p = 0.43, BF = 3.14]. Behavioral results According the AB magnitude, seven participants with The mean accuracy of T1 across all conditions was an AB magnitude of 10% or less were classified as non- 96.7 ± 0.6%. A three-way ANOVA with factors of the blinkers (mean = 4.94%) and another twenty participants fear-expectation (high, low) and expression (fear, neutral) as blinkers (mean = 22.89%). Again, a two-way ANOVA was conducted on T1 accuracy. The main effects of the with factors of the fear-expectation (high, low) and the fear-expectation [F(1, 26) = 1.64, p = 0.21, BF = 1.19] expression (fear, neutral) was performed on T2 dis- and the expression [F(1, 26) = 2.31, p = 0.14, BF = 3.27], crimination for blinkers did not reveal significant main as well as the interaction between the expression and the Sun et al. Behavioral and Brain Functions (2022) 18:16 Page 8 of 12 fear on AB. First, the experiment 1 revealed that fearful effects of the fear-expectation [F(1, 19) = 3.09, p = 0.095, expression facilitated the discrimination of gender within BF = 0.92] and the expression [F(1, 19) = 0.26, p = 0.618, the blink period only in the low fear-expectation condi- BF = 3.49], as well as the interaction effect [F(1, tion, but not in the high fear-expectation condition, sug- 19) = 0.32, p = 0.578, BF = 3.53]. gesting that unexpected fearful expression attenuated AB in the implicit emotional AB task. Secondly, the modu- ERP results lation effect of emotional expectation on emotional pro - VPP (180–220 ms) There was a significant main effect cessing during the AB task could be observed on the P300 of the expression [F(1, 26) = 4.4, p = 0.046, η2 p = 0.15, component, with larger P300 amplitudes elicited by fear- BF = 0.66], with larger VPP amplitudes elicited by fear- ful faces than neutral faces in the low fear-expectation ful faces (3.409 μV) than neutral faces (2.911 μV) (Fig. 3). condition, but not in the high fear-expectation condition. No further main effect of the fear-expectation [F(1, Furthermore, fearful faces elicited early enhancement 26) = 0.109, p = 0.744, BF = 4.593] or interaction was on VPP amplitudes than neutral faces, which was inde- significant [F(1, 26) = 0.002, p = 0.968, BF = 3.599]. pendent of the fear-expectation. However, the behavioral effects of expectation on expression were not replicated P300 (470–570 ms) There was no significant main in the experiment 2. Taken together, these results sug- effect of the fear-expectation [F(1, 26) = 2.798, p = 0.106, gested that unexpected fearful faces might attenuate AB BF = 0.7] or the expression [F(1, 26) = 1.985, p = 0.171, and get the preferential processing during the implicit BF = 2.16]. However, the interaction between the fear- emotional AB task. expectation and the expression was significant [F(1, In the implicit emotional task, whether emotional T2 26) = 8.147, p = 0.008, η2 p = 0.24, BF = 0.972] (Fig. 3). attenuated AB depended on the expectation for task- A simple effect analysis revealed that there was no sig - irrelevant emotional information. Previous studies have nificant difference between the fearful faces (2.798 μV) shown that emotional T2 could attenuate the AB in the and neutral faces (2.948 μV) in the high fear-expectation explicit emotion task [14, 23, 24, 37, 43]. Extending these condition (p = 0.758, BF = 3.594). However, fearful faces previous findings, the present study found that advantage (4.227 μV) elicited larger P300 amplitudes than neutral for fearful versus neutral faces only in the low fear-expec- faces (3.076 μV) in the low fear-expectation condition tation condition for lag 3 (i.e., within the blink period) in (p = 0.003, BF = 11.936). the implicit emotion task. The most well-supported theo - We analysis these ERP results only for blinkers. For ries of the AB [5, 32, 52] suggest that the AB reflects the the VPP, the main effects of the fear-expectation [F(1, suppression of attentional engagement during the blink 19) = 0.004, p = 0.951, BF = 4.35] and the expres- period. Thus, the advantage of unexpected fearful faces in sion [F(1, 19) = 4.01, p = 0.06, BF = 1.64] were not the lag3 condition suggested that unexpected threatening significant; and the interaction between the fear-expec - stimuli could break through the suppression that occurs tation and the expression was also not significant [F(1, during the blink. This may be an evolutionary advantage, 19) = 0.156, p = 0.697, BF = 3.11]. Again, we observed that is, the brain may be more sensitive to unexpected similar results of P300 in blinkers. The interaction threatening stimuli that could devote more attentional between the fear-expectation and the expression was engagement to process these stimuli [15, 33]. In addition, significant [F(1, 19) = 10.219, p = 0.005, η2 p = 0.35, the same advantage for fearful versus neutral faces was BF = 1.51]. A simple effect analysis revealed that there only in the lag8 condition (i.e., outside the blink period) was no significant difference between the fearful faces when fearful faces were expected, suggesting that fearful (2.91 μV) and neutral faces (3.28 μV) in the high fear- faces could capture attention again when the suppression expectation condition (p = 0.549, BF = 2.8). However, of attentional engagement was relieved in the lag8 con- fearful faces (4.96 μV) elicited larger P300 amplitudes dition. In the AB task, the available attentional resources than neutral faces (3.58 μV) in the low fear-expectation of T2 depended on its interval from T1 [5, 11]. Thus, the condition (p = 0.006, BF = 7.2). The main effect of factor of T1-T2 interval actually isolated the effects of the fear-expectation was significant [F(1, 19) = 5.023, expectation and attention. The different pattern of emo - p = 0.037, BF = 4.31], while the main effect of the tional expectation on emotional processing in two T1-T2 expression were not significant [F(1, 19) = 1.239, p = 0.28, interval condition indicated that expectation and atten- BF = 2.42]. tion might interact to produce this effect. We speculated that in the emotional implicit AB task, participants might Discussion establish an attentional template based on high anticipa- In the present study, we manipulated the probability of tion of emotional stimuli to selectively inhibit the pro- fearful T2 in an implicit emotional AB task to test how cessing of task-irrelevant emotional information, but this the expectation of fearful faces influenced the effect of Sun et al. Behavioral and Brain Functions (2022) 18:16 Page 9 of 12 attentional template might only play a role when atten- AB task, the detected T2 evoked larger P300 amplitude tional resources were relatively insufficient (lag3). Thus, compared to the missed T2, indicating that the target was the advantage of expected fearful faces in the lag3 condi- encoded into working memory [8, 20, 26, 56]. Thus, our tion was disappeared because the processing of expres- findings suggested that in the low fear-expectation condi - sion was suppressed based on the attentional template. tion, unexpected fearful faces captured more attentional When the probability of emotional stimuli was low or resources and were encoded into working memory. In the attentional resources were sufficient (lag8), the sup - Experiment 2, we observed that expectation suppressed pression of task-irrelevant emotional information based the later processing of facial expression reflecting by on attentional template would be broken, and the facial P300, but did not affect the early emotional effect. These expression would get the preferential processing again. results are consistent with a recent view that expecta- However, it should be noted that there seems to be a tion has little influence on early sensory responses and small lag effect in the high fear-expectation for both the primarily influences later elaborate stages of information neutral and fearful expression conditions, although the processing [40]. However, these explanations could only paradigm that we used was robust enough to produce be limited in the condition that the attentional resources an AB effect [29, 47]. To excluded the effect of an indi - were insufficient, because Experiment 2 only recorded vidual difference in the AB effect, we split the sample to neural activities during the short T1-T2 interval. Future “blinkers” and “non-blinkers” based on previous reported research could also focus on the neural mechanisms of method [25]. Our additional analyses excluded these expectation on emotional processing when attentional non-blinkers and found similar main effects and interac - resources were relatively sufficient. tion effects as original analyses, suggesting that the effect For the modulation effect of expectation on the later of expectation on expression cannot be explained by processing of emotional stimuli, an alternative explana- individual differences in the AB effect. tion was that the increased P300 amplitudes for unex- The neural mechanism underlying the expectation pected fearful faces compared with neutral faces might effect was measured with EEG in Experiment 2. Con - merely reflect the probability of stimuli. The P300 is sistent with a previous study [47], we found that fear- sensitive to stimuli probability, with unexpected or devi- ful faces elicited increased VPP amplitudes than neutral ant stimuli eliciting a larger P300 than high probabil- faces, and this emotional effect was independent of ity stimuli [34]. Besides, several emotional studies have expectation. Previous studies using explicit or implicit showed that negative relative to neutral facial expres- emotion tasks have found this early effect, which was sions usually induce larger amplitudes of later positive considered to reflect the rapid detection of fear by the potential (LPP), which has a similar distribution and time amygdala [2, 23, 31]. Here, since facial expression was a course as the P300, reflecting the sustained engagement task-independent feature in this study, we concluded that and elaborate processing for emotional stimuli [13, 41]. this early emotional effect was related to the bottom-up u Th s, it seems possible that the larger LPP for negative automatic attentional capture of facial expression. How- faces and the larger P300 for neutral faces (due to their ever, the significant main effect of expression on the VPP lower probability) in the high-fear-expectation condition was not supported by Bayes factors in the present study might have canceled out, while both effects would go in (BF = 0.66), whereas this effect was supported strongly the same direction (i.e., larger LPP and larger P3 for fear- by Bayes factors in our previous study with a BF of 24.22 ful faces) in the low-fear-expectation condition. If this [47]. Reporting both p-values and BF might result in alternative explanation was right, we would also observe effects falling into different categories of statistical deci - the probability effect of neutral faces, with larger P300 sion-making, especially if statistical power is low. Hence, for neutral faces in the high fear-expectation condition more studies are required to focus on this contradiction than that in the low fear-expectation condition. However, in the future. More importantly, our findings revealed this speculation was not supported by our ERP data that that expectation modulated the later working memory low-probability neutral faces did not elicit larger P300 consolidation of emotional stimuli, reflecting by the P300 amplitudes. In addition, our previous study that included component. Specifically, we found that fearful T2 trig - a condition with equal probabilities for fearful and neu- gered a larger P300 amplitudes than neutral T2 in the low tral faces in the implicit emotional AB task might help fear-expectation condition. By contrast, P300 amplitudes to quantify potential influences of fearful expressions on were similar for fearful and neutral T2 in the high fear- the P300 [47]. In that study, we found that fearful faces expectation condition. These results were consistent with elicited similar P300 as neutral faces when participants one study reported by Yang et al. [53], who proposed that reported the target’s gender. This result suggested that emotional expectation could decrease the brain sensitiv- facial expression was not processed in the later stage. ity to fearful stimuli in an implicit emotional task. In an Hence, the similar P300 of fearful and neutral faces in the Sun et al. Behavioral and Brain Functions (2022) 18:16 Page 10 of 12 high fear-expectation condition was not due to the emo- hypothesis that fearful faces might elicit enhanced later tional salience of fearful faces and the lower probability brain activity than neutral faces only in the low fear- of neutral faces. These evidences indicated that the effect expectation condition, but not in the high fear-expec- of expectation on the P300 in the implicit emotional AB tation condition. The ERP results of Experiment 2 were task did not merely reflect the stimulus probability. consistent with our hypothesis, but the lack of a behav- In the present study, the probability of fearful T2 was ioral effect of fear in the low fear-expectation condition manipulated to investigate the effect of expectation on prevented us from drawing strong conclusions. Thus, the prioritized emotional processing during the implicit further research is needed to verify this link that the emotional AB task. The data indicated that emotional ERP effects we observed in Experiment 2 are critical for expectation modulated the prioritized processing of behavior in the AB task of Experiment 1. In addition, we fear in the later working memory consolidation stage. speculated that the lack of behavioral effects might be We mentioned earlier that emotional expectation may related to the increased temporal expectation in Experi- modify the perception of emotional stimuli through two ment 2. Previous studies have indicated that temporal top-down mechanisms, enhancing or inhibiting the per- expectation also attenuated AB when the position of ceptual representation of emotional information [46]. target was predictable [42, 50]. In the present study, two Since facial expression was task-irrelevant information T1-T2 lags were used in Experiment 1, whereas only one in the present study, the later top-down mechanism of lag3 was used in Experiment 2 in which the position of inhibition was considered to involve in the effect of emo - T2 was predictable. Indeed, we observed higher T2 accu- tional expectation on emotional processing, by selec- racy in Experiment 2 (78.9 ± 2.7%) than that in Experi- tively suppressing the later neural representation of facial ment 1 (67.3 ± 3.4%) in the lag3 condition, suggesting expression. However, the present study did not find the that the implicit temporal expectation induced by fixed evidence that emotional expectation could modulate T1-T2 interval facilitated the detection of T2 in Experi- the early emotional effect, which reflected a bottom-up ment 2. Therefore, the facilitation effect of temporal automatic processing driven by the emotional salience expectation might potentially mask the attentional cap- of facial expression [23, 47]. The bottom-up process of ture effect of unexpected fearful faces. But future studies emotional stimuli may only facilitate the early detection are still needed to look at this issue. of the target, and the top-down process driven by emo- Another limitation of this study is that only fearful tional expectation may trade off the facilitation effect of and neutral faces were compared. In previous studies, expression on target discrimination. In general, two main fear and anger expressions signal threats in the envi- conclusions can be drawn from the two experiments. ronment, and these negative expressions can quickly First, expectation traded off the attenuation effect of fear capture the individual’s attention and attenuate AB [3, on AB in the implicit emotional task. By contrast, unex- 24, 28]. Some researchers believe that the effect of emo - pected fearful faces could attenuate AB compared with tion on AB is mainly related to the arousal of stimu- neutral faces in the low fear-expectation condition even lus, and positive expression can also attenuate AB [30, when facial expression was task-irrelevant. Second, emo- 37]. Therefore, we speculated that the interaction of tional expectation primarily influences the later process - expectation and fear in AB found in this study could ing of facial expression reflecting by P300, but has little be extended to expressions of anger, as well as positive influence on the early emotional effect. These results sug - expression with higher arousal. Future research should gest an important role of top-down expectation in the continue to explore this issue. preferential processing of fear under limited attentional Acknowledgements resources, that is, expectation for task-irrelevant facial This research was supported by the National Natural Science Foundation of expression and the emotional salience of stimuli can China (31470980) to Qin Zhang and the Youth Beijing Scholar Project to Ping Wei. interact to affect the perception of emotional stimuli. Our findings provide new evidence supporting the Author contributions hypothesis that task-irrelevant emotional expectation MS and QZ designed the experimental task. MS conducted the experimental task and wrote the manuscript. CS, XJ, FL, LC and PW wrote and reviewed the may modulate the prioritized processing of fear, via sup- manuscript. All authors read and approved the final manuscript. pressing the neural representation of facial expression in the later working memory consolidation stage. How- Funding This research was supported by the National Natural Science Foundation of ever, one limitation should be noted that the behavioral China (31470980) to Qin Zhang and the Youth Beijing Scholar Project to Ping results of Experiment 2 did not replicate the expectation Wei. effect as Experiment 1, indicating that the ERP results Availability of data and materials during Experiment 2 might not be driven by the behav- The data are currently not publicly available due to participant privacy. ioral effects as Experiment 1. We have made a specific Sun et al. Behavioral and Brain Functions (2022) 18:16 Page 11 of 12 13. Eimer M, Holmes A. Event-related brain potential correlates of emotional Declarations face processing. Neuropsychologia. 2007;45(1):15–31. https:// doi. org/ 10. 1016/j. neuro psych ologia. 2006. 04. 022. 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Journal
Behavioral and Brain Functions – Springer Journals
Published: Dec 14, 2022
Keywords: Expectation; Fear; Attentional blink; Event-related potentials