The effect of emotional information from eyes on empathy for pain: A subliminal ERP study

Juan Song; Yanqiu Wei; Han Ke

doi:10.1371/journal.pone.0226211

. 2019 Dec 13;14(12):e0226211. doi: 10.1371/journal.pone.0226211

The effect of emotional information from eyes on empathy for pain: A subliminal ERP study

Juan Song ^1,^*, Yanqiu Wei ¹, Han Ke ²

Editor: Kai Wang³

PMCID: PMC6910684 PMID: 31834900

Abstract

Facial expressions are deeply tied to empathy, which plays an important role during social communication. The eye region is effective at conveying facial expressions, especially fear and sadness emotions. Further, it was proved that subliminal stimuli could impact human behavior. This research aimed to explore the effect of subliminal sad, fearful and neutral emotions conveyed by the eye region on a viewer’s empathy for pain using event-related potentials (ERP). The experiment used an emotional priming paradigm of 3 (prime: subliminal neutral, sad, fear eye region information) × 2 (target: painful, nonpainful pictures) within-subject design. Participants were told to judge whether the targets were in pain or not. Results showed that the subliminal sad eye stimulus elicited a larger P2 amplitude than the subliminal fearful eye stimulus when assessing pain. For P3 and late positive component (LPC), the amplitude elicited by the painful pictures was larger than the amplitude elicited by the nonpainful pictures. The behavioral results demonstrated that people reacted to targets depicting pain more slowly after the sad emotion priming. Moreover, the subjective ratings of Personal Distress (PD) (one of the dimensions in Chinese version of Interpersonal Reactivity Index scale) predicted the pain effect in empathic neural responses in the N1 and N2 time window. The current study showed that subliminal eye emotion affected the viewer’s empathy for pain. Compared with the subliminal fearful eye stimulus, the subliminal sad eye stimulus had a greater impact on empathy for pain. The perceptual level of pain was deeper in the late controlled processing stage.

Introduction

Empathy refers to the process of an individual sharing and understanding another person's emotions, feelings and thoughts. It plays an important role in communication and interaction in human society [1]. Gladstein proposed two major types of empathy: affective empathy (responding with the same emotion to another person’s emotion) and cognitive empathy (intellectually taking the role or perspective of another person) [2]. Further, Davis divided empathy into 4 parts: perspective-taking (tendency to spontaneously adopt the psychological point of view of others), empathy concern (“other-oriented” feelings of sympathy and concern for unfortunate others), fantasy (tendency to transpose themselves imaginatively into the feelings and actions of fictitious characters in books, movies, and plays) and personal distress (“self-oriented” feelings of personal anxiety and unease in tense interpersonal settings) [3]. Modern accounts of empathy decompose empathy into these three components: experience-sharing involves vicariously resonating with others’ experiences, mentalizing involves actively inferring others’ thoughts and intentions, and compassion involves motivation to alleviate others’ suffering [4, 5]. Empathy is regarded as a suitable explanation for prosocial behavior [6], such as taking care of offspring and cooperating with others.

Empathy for pain has been the major focus of research devoted to empathy in social neuroscience and other related fields, making it the most dominant neuroscientific domain in the study of empathy [7]. A review paper summarized research in this field for the past twenty years, it was found that the theme of empathy research gradually shifted from early personality traits, attitudes, and emotions to social cognition [8]. With the development of technology, research on the cognitive neuroscience of empathy became a hot topic. On one hand, some researchers thought that the medial prefrontal cortex (mPFC), superior temporal sulcus (STS), temporal poles (TP), and ventromedial cortex (VM cortex) were involved in cognitive empathy, and the amygdala, insula and inferior frontal gyrus (IFG) were involved in affective empathy. On the other hand, the right temporoparietal junction (rTPJ), the insula and the anterior midcingulate cortex (aMCC) were thought to be related to empathy for pain [9]. The aMCC and the insula were the “shared neural circuit” of empathy for pain [10]. In other research, the prefrontal cortex (PFC) and the anterior cingulate cortex (ACC) were closely related to empathy for pain [11]. Some new research found that the fusiform face area (FFA) was involved in empathy tasks [12]. The mirror neuron, “neural bridge” in social communication, occupies an important place in empathy [13].

As we know, the face can provide important social information and reflect potential changes in the environment [14, 15]. People can infer and understand others’ inner state immediately by observing facial expressions. A study found that individuals with high empathy paid attention to various negative facial expressions (angry and afraid faces) more than those with low empathy from very-early stage (reflected in the N170) to late-stage (reflected in the LPP) processing of faces [16]. N170 is a negative component elicited by face’s feature and is sensitive to eye information. For example, isolated eye regions elicit N170 amplitudes and delayed latencies compared to faces. Hence, there is a close relationship between empathy and facial expression.

Moreover, there is special processing of eyes in facial perception. For instance, research found that the adults had obvious attentional bias for the eyes [17] using an eye movement technique. When recognizing sad emotions, the eye cues had greater significance than other cues. People first notice the eyebrow area, and the eyebrow area captured more attentional resources than the mouth area [18]. In addition, threat information conveyed by eyes was the same as that conveyed by the face when distinguishing facial expressions, but the effect of the mouth area was quite different from that of the whole face [19]. Qiao drew a similar conclusion [20]. The eye was the most expressive part of the face, especially for fearful and sad emotions. The eyes have an advantage in facial processing, and eye region information plays an important role in people’s processing of negative emotion. These conclusions provided strong evidence that sad and fearful information from eye region can accurately represent facial expression.

Therefore, eye region emotional information, as a unique part of facial expression, is inseparable from empathy for pain. People can infer others’ current mental state just through observing the eyebrow area of the face, and adjust their social behaviors accordingly. Empathy can also be measured by the “Reading the Mind in the Eyes” test [21], which was created by Baron-Cohen [22]. The test reflects the ability to interpret people’s complex emotional states in some situations when other information is limited. Furthermore, one study found that participants made more cooperative decisions after supraliminal eye contact than they did with no eye contact, and the effect only existed for the prosocial but not for the pro-self [23]. To date, research using eye stimuli alone to study face processing is still in an initial stage [24]. Additionally, emotions conveyed by eye region information become more important and a necessary way for people to read others’ mind when expressions of the others’ whole face is not available, such as in medical situations or hijacking. The study of eye emotions has many practical applications.

In summary, the eye region was found to be the important area for conveying facial expression [25]. In previous research, the ERP research concerning empathy for pain mostly used pictures and videos describing hands or feet in painful situations, or they used a painful facial expression to explore the subjects’ index of brain activity and behavioral changes when observing others’ pain [26, 27, 28, 29, 30]. To date, there have been a few ERP studies comparing the effect of negative emotions on empathy for pain [26, 27, 31]. For example, one supraliminal ERP study looking at the effect of eye emotional information on empathy for pain found a significant difference on P3 component induced by different eye conditions. The amplitude in neutral eyes condition was greater than that in sad eyes condition and fear eyes condition. Different supraliminal emotional information expressed by eye region affects late processing of empathy for pain [31]. Further, negative emotions have a profound influence on human survival and are important for social adaption from an evolutionary perspective [32]. Additionally, subliminal stimuli can also have impact on human behavior [33, 34, 35, 36, 37, 38]. In some situations, unconsciously processed stimuli could affect behavioral performance more profoundly than consciously processed stimuli [39]. For instance, a study found that unconsciously processed stimuli could enhance emotional memory after both short and long delays. This result indicated that emotion could enhance memory processing even when the stimuli was encoded unconsciously[36]. Another study found that people’s response to painful stimuli was more likely to be affected by unconscious negative emotions than the conscious negative emotions [14, 40]. Therefore, it’s imperative to study the processing of subliminal negative stimuli.

In this study, we aimed to compare the neural response to subliminal sad and fearful negative emotions conveyed by eyes on empathy for pain with an ERP technique. We used a typically subliminal affective priming paradigm with an empathy task, which is similar to some previous studies [26, 27, 40], to investigate which negative emotion was highly correlated with empathy for pain automatically. The theory of emotion-sharing indicated that emotion-sharing between the self and others was the base of empathic behavior [41]. When individuals perceived others’ emotion, they automatically imitated others’ emotions and share the same representation. As we know, the fear emotion means danger and a crisis [42]. It can cause avoidance behaviors. In contrast, sadness can give rise to prosocial behaviors [43]. Furthermore, the priming pictures in one of the previous studies were situational pictures that stimulate participants’ own emotions [26]. While our procedure was different in term of that we used different eye emotions as cues to prime empathy for pain. The eye cues were external emotion sources. Hence, we could supply some evidence of finding the suitable emotion from others when empathy for pain occurred to explain the subsequent social behaviors such as helping others or escaping.

As we know, N1 and N2 components reflect early, automatic, affective-sharing processes, people automatically share fearful emotion information rather than sad emotion information when they show empathy for pain [9]. Hence, our hypothesis was that the empathy for pain task with fearful emotion would elicit larger N1 and N2 components than the task with sad emotion. Some studies showed that the P2 was an index of perceptual processing [44]. Also, humans are sensitive to negative novelty stimuli [45], which captures much more attention and can be reflected by brain activity. Therefore, the negative novelty stimuli would elicit larger amplitudes of ERP components. We therefore hypothesized that the P2 amplitude elicited by sad emotion priming in an empathy task would be larger than that elicited by fear. It meant that people would pay more attention to the empathy task with a sad emotion rather than a fearful emotion. The LPC (late positive component) and P3 component have been shown to index the amount of attentional resources allocated to the stimulus [28], and they indicate top-down processing and elaborate evaluation [16]. The more adequately people evaluate targets, the larger the amplitudes of the P3 and LPC. We hypothesized that the amplitudes of P3 and LPC elicited by painful stimuli were larger than nonpainful stimuli, which meant that processing painful stimuli took more mental resources.

Materials and methods

Participants

Nineteen participants with no history of brain injury or mental disorder participated in the experiment. All participants had normal or corrected-to-normal vision, signed the informed consent form and received compensation after the experiment. Four of the participants’ data (no obvious classical ERP components for one of them, and valid trials in each condition were 51.8% for the other three) were rejected due to artifacts during electroencephalographic (EEG) recording. Data of 15 participants were retained (6 men, 9 women; 22.33 ± 1.91 years (M ± SD)). This study was approved by the Ethics Committee of the Academy of Psychology and Behavior, Tianjin Normal university.

Experimental design and stimuli

This study used an affective priming paradigm with a 3 priming type (subliminal neutral, sad, fear eye region information) × 2 target type (painful, nonpainful pictures) within-subject design. Therefore, there were 6 conditions in total: Neutral/ Painful, Neutral/ Non-Painful, Sad/ Painful, Sad/ Non-Painful, Fear/ Painful, Fear/ Non-Painful. The priming stimuli used in the experiment were 42 facial black and white pictures (comprising 14 subliminal sad, 14 subliminal fear, and 14 subliminal neutral pictures) selected from the Chinese Affective Face Picture System (CAFPS) [46]. As the total eye region from the CAFPS was not large enough, as well as that some eye region emotions were rated poorly (i.e. some sad eyes did not convey sad emotions sufficiently), a minority of them (7 pictures) were taken from the internet with only remaining the eye region. The gender of the characters in the images for each emotion type was equal. The targets were pictures showing a person’s hands in painful or nonpainful situations [47, 48]. The size of eye region pictures was adjusted to 260 pixels in width and 115 pixels in height. The size of masks was 255 × 105 pixels. They were obtained by randomly scrambling 10 × 10-pixel squares on every cropped face with MATLAB2016b. The size of targets was 369 × 287 pixels. The distance between the participants and the computer monitor was approximately 65 cm. The pictures were normalized for size, global contrast and luminance.

Thirty participants assessed the priming pictures prior to the experiment (rated on a 9-point scale). For the level of arousal, both sad (M ± SD: 6.71 ± .56) and fearful eye regions (6.84 ± .38) differed significantly in priming from neutral eye regions (3.52 ± .20, p < .001), but the difference between the sad and fearful eye regions was not significant (p = .40). For level of valence, the sad (2.37 ± .43) and fearful eye regions (2.31 ± .73) differed dramatically from neutral eye regions (4.30 ± .56, p < .001), but the difference between the sad and fearful eye regions was not significant (p = .79). Another 29 participants assessed the target pictures (rated on a 4-point scale). The pain intensity of the painful pictures (M ± SD: 2.16 ± .22) and the nonpainful pictures (.30 ± .19) were significantly different (p < .001).

Experimental procedure

The experimental procedure in each trial was as follows. A fixation was presented in the center of the screen for 500 ms, followed by a random blank screen for 400~600 ms. The priming pictures were then presented for 16 ms. Subsequently, the scrambled mask pictures were presented for 184 ms follow by a blank screen of 200 ms [40]. After which, the target pictures were displayed for 1500 ms until a response was given. Participants were told to judge whether the targets were in pain or not. There was a blank interval presented for 1000 ms between each trial (see Fig 1). Simultaneously, the brain activity was recorded using Curry8 (Neuroscan, USA). The priming reached a subliminal effect through a series of operations consisting of short-term presentation of the priming pictures with masks subsequently. After the EEG session, participants were asked whether they saw the priming pictures or their type clearly before the mask. They all reported that they were not aware of the emotion type. Therefore, the priming pictures were at an unconscious level according to their subjective reports [40]. Consequently, this operation ensured that the priming was subliminal.

Fig 1 — Panel A showed the target illustrated a non-painful scene. Panel B showed the target illustrated a painful scene. Participants were asked to judge whether the target was painful or not.

The procedure was divided into 4 blocks. Each block consisted of 126 trials, hence 84 trials in each condition. Each type of eye region pictures repeated 12 times, and each of the target pictures repeated 6 times. The stimuli in every block were pseudorandomly presented. The response buttons were counterbalanced across participants, and the button press model was also counterbalanced across different participants using F for painful targets and J for nonpainful targets or J for painful targets and F for nonpainful targets.

After the EEG session, all participants were asked to complete the Chinese version of Interpersonal Reactivity Index scale (IRI-C scale) [3, 49], which contained 22 items. A 5-point Likert scale was used for responses, ranging from inappropriate (0 point) to very appropriate (4 points). 5 items were scored in reverse. In this questionnaire, empathy was divided into 4 parts: perspective-taking (tendency to spontaneously adopt the psychological point of view of others), empathy concern (“other-oriented” feelings of sympathy and concern for unfortunate others), fantasy (tendency to transpose themselves imaginatively into the feelings and actions of fictitious characters in books, movies, and plays) and personal distress (“self-oriented” feelings of personal anxiety and unease in tense interpersonal settings). Correlations between the personal distress subscale and ERP components was conducted in order to find out the relationship between state empathy in task and trait empathy [30].

Devices and recording

The EEG was continuously recorded from 64 scalp electrodes mounted on an elastic cap in accordance to the extended 10–20 system, with the addition of two mastoid electrodes. The electrode at the left mastoid was used as the recording reference and transformed to the average of the two mastoids offline. The electrode impedance was kept at less than 5 kΩ. Eye blinks and vertical eye movements were monitored with electrodes located above and below the left eye. The horizontal electro-oculogram was recorded from electrodes placed 1.5 cm lateral to the left and right external canthi. The EEG was amplified (bandpass: 0.05–400 Hz) and digitized at a sampling rate of 1000 Hz.

Data analysis

EEG data were preprocessed and analyzed using the functions in Curry8 software. To achieve more valid trials, some frontal electrodes (FP1 FPz FP2 AF3 AF4) were excluded for drifting and some electrodes over the ears (F7 FT7 T7 TP7 F8 FT8 T8 TP8) were excluded due to low signal quality. Additionally, the ineffective channel CP5 was deleted. The EEG data were re-referenced to linked offline mastoids. A digital filter at a low-pass of 30 Hz was then applied. Trials exceeding 100 μv at any electrode were excluded from the average. Time windows of 600 ms before and 1000 ms after the onset of the painful and nonpainful target pictures were segmented from EEG data. The time of target onset was the zero point. All epochs were baseline-corrected with respect to the mean voltage over the 600 ms to 400 ms preceding the onset of painful and nonpainful targets. Baseline correction was performed prior to fixation to avoid distortion of the baseline by visually evoked potentials to the mask [50, 51]. An additional ANOVA in the time interval between -400 ms and -200 ms was performed to exclude any physical difference in the stimuli that may have compromised possible priming effects [50, 51]. This analysis did not reveal any significant effects (ps > .09).

According to the grand-averaged ERP pictures, the topographical distribution and the literature [9, 30, 52, 53], five regions of interest from the frontal (the mean amplitudes of F3, Fz and F4), frontal-central (the mean amplitudes of FC3, FCz and FC4), central (the mean amplitudes of C3, Cz and C4), central-parietal (the mean amplitudes of CP3, CPz and CP4) and parietal (the mean amplitudes of P3, Pz and P4) regions were chosen. Analyses were conducted using the peak amplitudes of N1 (100~180 ms), P2 (180~240 ms), N2 (240~300 ms) and P3 (300~430 ms) and the mean amplitude of the LPC (430~650 ms) after the onset of the painful or nonpainful pictures [9, 16, 28]. A three-way, repeated-measures ANOVA with priming type (subliminal neutral, sad, fear eye region information), target type (painful, nonpainful pictures) and regions of interest was performed. Specifically, five electrodes from the midline (Fz, FCz, Cz, CPz and Pz) were chosen for LPC [40]. Degrees of freedom for the F-ratio were corrected using the Greenhouse-Geisser method. Statistical differences were corrected according LSD post hoc correction.

Moreover, we conducted the correlations between PD ratings and pain effect (subtracting ERP elicited in the nonpainful condition from ERP elicited in the painful condition) to investigate whether the pain effect was correlated with the PD subscale of the IRI-C [30].

Results

Behavioral results

A three-way repeated measures ANOVA was conducted to examine the reaction time (RT) differences between the experimental conditions. The results are depicted in Fig 2.

Fig 2 — The error bars representing standard errors of the mean. The symbol of “**” means p < .01. “***” means p ≤ .001.

The main effect of priming type was significant (F(2,28) = 28.21, p < .001, η²_p = .67). The RT for the neutral eye emotion (M = 800 ms, SE = 20) was faster than the fearful eye emotion (M = 816 ms, SE = 22) (p < .01) and the sad eye emotion (M = 827 ms, SE = 21) (p < .001), and the RT for the fearful eye emotion was faster than the sad eye emotion (p < .01). The main effect of target type was significant (F(1,14) = 7.20, p = .02, η²_p = .34). The RT for the painful pictures (M = 797 ms, SE = 19) was faster than for nonpainful pictures (M = 832 ms, SE = 24). There was an interaction between priming type and target type (F(2,28) = 7.99, p < .01, η²_p = .36), suggesting that the RT for the neutral eye emotion (M = 776 ms, SE = 18) was faster than the fearful eye emotion (M = 795 ms, SE = 20) (p < .01) in the painful situation, and there was also a significant difference between the neutral and sad eye emotions (M = 820 ms, SE = 20) (p < .001) and the fearful and sad eye emotions (p = .001) in the painful situation. Other interactions were not significant (ps > .07).

ERP results

N1

Only one significant main effect of region was observed (F(4,56) = 48.06, p < .001, η²_p = .77). N1 was mainly distributed in the frontal and frontal-central regions (M ± SE: -6.24 ± .71μV, -5.76 ± .65μV, -3.60 ± .38μV, -.31 ± .21μV and 2.08 ± .53μV). The main effect of priming type was insignificant (F(2,28) = 1.12, p = .34). The main effect of target type was not significant (F(1,14) = .36, p = .56). All the interactions were not significant (ps > .16).

P2

The main effect of region was significant (F(4,56) = 33.02, p < .001, η²_p = .70). P2 was mainly distributed in the parietal regions (M ± SE: -2.16 ± .63μV, -2.00 ± .56μV, -.78 ± .31μV, 1.56 ± .20μV and 4.70 ± .59μV). The main effect of priming type was insignificant (F(2,28) = .54, p = .59). The main effect of target type was insignificant (F(1,14) = .22, p = .65). A significant interaction of priming type × target type (F(2,28) = 3.85, p = .03, η²_p = .22) was observed, suggesting that the sad eye emotion(M ± SE: .33 ± .18μV) elicited a larger P2 amplitude than the fear (.15 ± .21μV) under the painful situation(p = .02), but there was no significant difference between the neutral(.28 ± .21μV) and the fear eye emotion (p = .08) as well as the sad and the neutral eye emotion (p = .52). Other interactions were not significant (ps > .61) (see Fig 3 and Fig 4).

Fig 4 — Left panel represented P2 peak amplitudes. Middle panel represented P3 peak amplitudes. Right panel represented LPC mean amplitudes.

N2

There was only one significant main effect of region (F(4,56) = 60.86, p < .001, η²_p = .81), suggesting that N2 was mainly distributed in the frontal and frontal-central regions (M ± SE: -6.59 ± .67μV, -6.04 ± .57μV, -3.49 ± .35μV, .07 ± .30μV and 3.12 ± .59μV). The main effect of priming type was insignificant (F(2,28) = .54, p = .59). The main effect of target type was also insignificant (F(1,14) = .08, p = .78). All the interactions were not significant (ps > .47)

P3

The significant main effect of region was observed (F(4,56) = 73.86, p < .001, η²_p = .84), suggesting that P3 was mainly distributed in the parietal regions (M ± SE: -4.68 ± .76μV, -3.82 ± .64μV, -1.32 ± .34μV, 2.77 ± .31μV and 6.80 ± .51μV). The main effect of priming type was insignificant (F(2,28) = .77, p = .47). The main effect of target type was significant (F(1,14) = 7.46, p = .02, η²_p = .35), suggesting that comparing to nonpainful stimuli(M ± SE: -.11 ± .21μV), a larger amplitude was elicited by painful pictures (.01 ± .20μV). All the interactions were not significant (ps > .29) (Figs 3 and 4).

LPC

The main effect of the electrode was significant (F(4,56) = 52.95, p < .001, η²_p = .79), suggesting that LPC was largest at P_Z (M = 4.35 μV, SE = .54). The main effect of priming type was not significant (F(2,28) = 1.18, p = .32). The main effect of target type was significant (F(1,14) = 10.52, p = .01, η²_p = .43) with painful pictures eliciting a larger amplitude (M ± SE: -.63 ± .34 μV) than nonpainful pictures (-.98 ± .28 μV). No interactions were significant (ps > .13) (Figs 3 and 4).

Correlations between the IRI-C and ERP

To investigate whether the pain effect (subtracting ERP elicited in the nonpainful condition from ERP elicited in the painful condition) was correlated with the PD subscales of the IRI, we calculated the correlations between PD ratings (M ± SD: 1.40 ± .77) and the pain effect from the frontal, frontal-central and the central electrodes (i.e., F3, Fz, F4, FC3, FCz, FC4, C3, Cz and C4) based on the distributions of N1 and N2. These analyses revealed significant correlations in the N1 time window (Cz: r(15) = .51, p = .05 for PD) and N2 time window (F3: r(15) = .61, p = .02 for PD).

Discussion

Previous studies showed the significance of subliminal stimuli. For instance, subliminal stimuli that failed to reach awareness may affect performance more effectively than stimuli that do reach awareness [54]. Invisible stimuli that are irrelevant to task are more disturbing than visible distractors because of failed communication in regions of the brain that normally suppress such responses [54]. Meanwhile, a study found that the affectively significant visual stimuli had privileged access to consciousness [55]. Our research initially used subliminal eye region information as the experimental stimulus to explore its effect on empathy for pain. The eye region was found to be an important area for conveying facial expression [25]. The subliminal paradigm in the present study was used to highlight the automatic processing of eye cues. Furthermore, unlike previous studies that roughly divided the experimental materials into positive, neutral, and negative emotion types, the current research divided the types of negative emotions more elaborate. We chose neutral, sad and fearful emotions because sad and fearful emotions have great significance for human survival. Sadness can give rise to prosocial behaviors [43] and fear can cause avoidance behaviors. Therefore, in this study, we compared the neural response to subliminal sad and fearful negative emotions conveyed by eye cues on empathy for pain by measuring the ERP responses.

The behavioral results showed that people reacted to the painful scene more slowly with the subliminal sad eye emotion than with the other two emotions. This finding indicated that people were more affected by sad eye emotion and sad eye emotion information required more attention. It seemed that people could not extract their attention from the sad emotion immediately during the empathy task. The sad emotion interfered with their responses to pain judgements [56]. Consequently, participants reacted more slowly to painful scenes while viewing the subliminal sad eye region information. On the other hand, explanation of negative priming effect supposed that during the process of subliminal priming, when the primes and the targets were related, automatic spreading activation from primes did happen and it might interfere with the process and comparison of the subsequent targets owing to the short interval in subliminal paradigms. When the primes and the targets were unrelated, they rarely matched and interfered with each other, so that the response was quicker [57].

The ERP results demonstrated that the P2 amplitude was less positive for the fear condition relative to the sadness condition for painful scenes. Neither sad nor fearful conditions were significantly different from neutral conditions for painful scenes. First of all, the P2 component is an index of extraction of emotional salience from stimuli [58]. It seemed that sad emotion from the eye regions stood out from the other two emotions during the empathy for pain task. Further, the P2 is also an index of attention [59]. Attentional bias happens automatically. Comparing to subliminal fearful eye regions, the empathy task was modulated and attracted more by subliminal sad eye regions. This meant people focused more on the empathy task primed by subliminal sad eye regions than that primed by fearful eye regions. Furthermore, sad eye emotions induce human’s prosocial behaviors to some extent [43]. However, fear emotion often implies a crisis [42]. Hence, there will be more costs involved in human’s exploration [60]. As a result, more attentional resources were diverted to aid in processing the sad eye emotion, and a larger P2 amplitude during empathy for pain was evoked.

Moreover, the task setting might cause participants some psychological stress and emotional burden [61]. Participants were asked to make a pain judgement within a certain period of time. They might imagine that they were experiencing the situation of the protagonist in a social scene. In this way, participants might have experienced negative impression and evaluation of the neutral eye emotions, which initially represented calm emotions. Consequently, the neutral emotion, to some extent, was more threatening and dominant rather than purely neutral [62]. Furthermore, the degree of threat was a little weaker than the fearful eye emotion. There was no significant difference between them accordingly. There was also no significant difference between the prosocial mental state [43, 63] elicited by the sad eye emotion and the dominant mental state induced by the neutral eye emotion. Maybe, the brain activities of the two emotions on empathy for pain were at a similar level under our task setting.

Additionally, this study found the amplitude elicited by painful pictures was larger than nonpainful pictures for late-controlled P3 and LPC. These two components were related to cognitive evaluation and involved elaborate processing based on previous results [9, 16, 26, 64]. The behavioral results demonstrated that people reacted more quickly than with the nonpainful situation. This finding may be related to the allocation of human attentional resources [26]. Human attentional resources are limited, and they have attentional bias. The painful scenes were more novel and important for human survival. Also, due to the task setting, participants were asked to judge whether the stimuli were in pain or not. Painful scenes were much more varied than nonpainful scenes. They therefore captured more attentional resources [65], and received more cognitive resources [26]. It might be the reason why the amplitude elicited by the painful stimuli was significantly larger than that elicited by the nonpainful stimuli.

Lastly, we explored the relationship between IRI-C and ERP components. According to a previous study, PD ratings were used to reflect automatic affective sharing of others’ emotional experience [30, 66, 67, 68]. The N1 and N2 have been suggested to be markers of early automatic emotional sharing [9, 30]. Therefore, we calculated the correlations between them. We found that the different waves (subtracting ERP elicited in the nonpainful condition from ERP elicited in the painful condition) of N1 and N2 were significantly correlated with PD sub-scale ratings. The larger the difference between painful and nonpainful conditions, the higher the PD score elicited. This significant correlation suggested that N1 and N2 reflected the level of discomfort induced by affective sharing of another’s pain [30]. The correlation between the PD rating and the early ERP reaction to the pain effect suggested that the empathic behavioral response had a neural basis.

Limitations

There are some possible directions for further study, such as the influence of different arousal levels from the same emotional priming on empathy for pain. Additionally, the source of the priming type (eye region emotion from different interpersonal distances) could be another influential factor in empathy for pain. There is still more space for exploration.

Conclusions

Together, these findings demonstrated that subliminal eye emotions significantly affected empathy for pain. Compared with the subliminal fearful eye stimulus, the subliminal sad eye stimulus had a greater impact on empathy for pain, which supported the theory of emotional sharing. The perceptual level of pain was deeper in the late controlled processing stage.

Acknowledgments

The authors would like to acknowledge all the participants in this study and Tianjin Philosophy and Social Science Projects in China. (TJJX17-010).

Data Availability

All data underlying our findings described in the manuscript can be fully available without restriction within the manuscript. Figures were the supporting information for our research. Our original data is available upon request (including the ERP waveforms, AVG and original data). All the means and SD are included in the manuscript. Our data did not extract any points from images. The images are the reflection of our data. The ERP waveforms' figures' making were based on the mean data of our subjects. If it is really needed, we can supply our grand mean AVG file for ERP waveforms.

Funding Statement

The research in the manuscript was funded by Tianjin Philosophy and Social Science Projects (China) Number: TJJX17-010 to JS. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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PLoS One. doi: 10.1371/journal.pone.0226211.r001

Decision Letter 0

Kai Wang

14 Aug 2019

PONE-D-19-16381

The effect of emotional information from eyes on empathy for pain A subliminal ERP Study

PLOS ONE

Dear Dr. Song,

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Reviewer #2: Yes

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Reviewer #2: Yes

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Reviewer #2: Yes

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Reviewer #1: The research article by Song and co-authors addresses the very interesting question if there is an association between eye region information and empathy for pain. This study demonstrated that subliminally conveyed eye emotion affected the viewer’s empathy for pain. Compared with the subliminal fearful eye stimulus, the subliminal sad eye stimulus had a greater impact on empathy for pain. The perceptual level of pain was deeper in the late controlled processing stage. Nevertheless I have some important points that I believe should be changed to make the manuscript clearer.

Specific comments:

ABSTRACT

a. In the body text the authors report the relationship between IRI-C and ERP components. However, this is not expressed in the abstract. This point should be added to make this paper more preciseness in the abstract.

b. Some abbreviations in the abstract should be clearly indicated.

Introduction

a. Some abbreviations are not given, such as “temporal poles” and “ inferior frontal gyrus”.

b. What is the meaning of “N170”? I noticed that this is explained in your 16th reference. Maybe you can explain what it means in your article.

c. In the third sentence of the sixth paragraph in your introduction, the conjunction “Nevertheless” may not be appropriate.

d. In the sixth paragraph in your introduction, we should start by writing about what others have investigated, and then write something about what research is fully investigated and what we can do in the present study.

e. The two sentences “Then, how do humans perceive others’ pain in completely different situations? It is still unknown and needs to be further explored.” may be better expressed in a declarative sentence.

Methods

a. The authors write "Nineteen participants with no history of brain injury or mental disorder participated in the experiment." Then, we can see “Thirty participants” and “another 29 participants”coming up in the Experimental Design and Stimuli part. Did the authors make some writing mistakes or some other reasons?

b. What is “IRI-C scale”? I did not find the full name of this abbreviation, which should be indicated in the text. There exists other improper abbreviation, for example the “PD”.

c. Why only make a correlation analysis between the pain effect and the Personal Distress (PD) subscales of the IRI-C? How about other scales of the IRI-C?

Results

- The abbreviation “RT” is not clear.

Discussion

a. The authors write “Fear indicates danger and a crisis, which can cause avoidance behaviors.”“ This finding might be caused by people being more affected by sad eye emotion and sad eye emotion information requiring more attention.” Is there any grammatical error here?

b. The authors write “How do humans automatically perceive others’ pain in these different situations? We still need to explore this question”. This point may be not appreciated. I think it can be replaced by your goal and hypothesis of your research.

c. “Additionally, P2 is an index of attention [55]. It is enhanced with greater attention.” These two sentences have the same meaning, change the expression of a subordinate clause or delete one sentence.

d. Psychology is very gender-biased. Whether gender influences the results in this study is worth further discussion. All participants have no history of brain injury or mental disorder in the study, does this phenomenon still exist in other groups or in other age groups?

Reviewer #2: This paper explored the effect of subliminal sad and fearful information conveyed by eyes on pain empathy by ERPs, and found that sad lead to slower response and greater P2 amplitude. The focus of the paper are interesting, the methods and used and the logic are reasonable, the structure of the article is clear. The following problems need further addressed.

Major points:

1. This article should focus on the modulation of subliminal emotional primes on pain empathy, so authors need to pay more attention to the interactions between the primes and targets. For example, authors only report P3 and LPC are affected by painful / nonpainful targets, can subliminal emotion be modified this effect? The results and discussion are less concerned about interactions, the reported interactions in the results are also poorly explained.

2. The author used the subliminal stimuli as primes, but in the introduction part, they did not present enough reasons about the significance of subliminal emotion and the difference between subliminal and supraliminal stimuli. The discussion part also lack the related explanation.

3. Methods and Results: the number of subjects (only 15 subjects’ results) was relatively small. In addition to arousal and valence, did the emotional types (sad, fearful or neutral?) be evaluated by subjects? Authors report interactions in the results, but do not report clearly how they interact in subsequent analyses from the view of two independent variables, so that readers can understand.

4. In view of the current results, there is a suggestion for data analysis. When analyzing ERP data, the author conducted repeated measurement analysis of brain region×primes (sad, fearful and neutral)× target type (painful or nonpainful), and the main results focused on the main effect of the region, while other results were not good enough. The ERP components differed in different brain regions, which is natural an easily understood results. Therefore, the analysis of specific ERP component can be conducted by analyzing the differences in brain regions first, and then analyze the electrodes of the most obvious region with prime types× target types measurements, which can more effectively reflect the author's intention.

Minor points:

Figure 1: It is suggested to replace the eyes, mask and target of the actual material samples

Figure 2: To add SE as error bar to the bar of reaction time. The unit and description should be added on the axis. The vertical axis should start from 0, and statistics significance is suggested to be added.

Figure 3：The ERP figure is not clear enough to see the detail including time axis. There are six lines in the ERP figure. It is recommended to take the peaks and draw a bar chart to express the results more clearly.

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Reviewer #1: No

Reviewer #2: Yes: Bin Xuan

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PLoS One. 2019 Dec 13;14(12):e0226211. doi: 10.1371/journal.pone.0226211.r002

Author response to Decision Letter 0

23 Oct 2019

Response to Editor and Reviewers(Please see the file "Response to Editor and Reviewers"in the final PDF. The colored part of revision can be seen in the file.)

Response to Editor and Reviewers

Dear editor and reviewers,

Thank you very much for inviting us to revise and resubmit our manuscript “The effect of emotional information from eyes on empathy for pain: A subliminal ERP Study”. We appreciate this opportunity. The comments raised by the reviewers were very thoughtful and constructive. Based on these comments, we have revised our manuscript and we believe that this revision is a substantially stronger contribution accordingly. We have prepared this cover letter to summarize how we have addressed these comments in our revision. Please see below for detailed responses. The issues raised in your editorial letter is reproduced in italics, followed by our response in each case.

We look forward to your reply. We have already sent our manuscript to AJE for language editing before our submitting. Also, for this revision, we accepted suggestions from one native speaker of English and one professional visitor study abroad about our language again. However, if needs, please give us another chance to edit it. See the revision of language in words highlighted in grey and some red words.

We are confident about our results and we also tried the methods the review suggested. If there is any thing you think we should revise or do more, please give us another chance to do it. We think our work is quiet creative and new in empathy study field. So it has its own value to be published. And it will really be our great pleasure if we can have it published in your journal with the help and suggestions of our editor and reviewers.

Thank you so much for your work and patience. Every details we revised were highlighted in the revised version of manuscript.

And we also revised the figures according to the advice.

If there is anything we did not revise or understand, please contact us and give us another chance, We will really appreciate.

Sincerely,

Juan Song on behalf of all authors

Reviewer #1: The research article by Song and co-authors addresses the very interesting question if there is an association between eye region information and empathy for pain. This study demonstrated that subliminally conveyed eye emotion affected the viewer’s empathy for pain. Compared with the subliminal fearful eye stimulus, the subliminal sad eye stimulus had a greater impact on empathy for pain. The perceptual level of pain was deeper in the late controlled processing stage. Nevertheless, I have some important points that I believe should be changed to make the manuscript clearer.

Specific comments:

Thank you so much for your suggestions.Please see the revised version of manuscript and manuscript with track changes. We also have Figure1,2,3,4(revised) version.

ABSTRACT

We really thank the Reviewer’s advice on the preciseness of the abstract. We have revised it: Moreover, the subjective ratings of Personal Distress (PD) (one of the dimensions in Chinese version of Interpersonal Reactivity Index scale) predicted the pain effect in empathic neural responses in the N1 and N2 time window.

“Abstract

b. Some abbreviations in the abstract should be clearly indicated.

Thanks for your nice advice. The abbreviations (ERP, LPC) in our abstract has been clearly indicated in our manuscript.

“Abstract

Introduction

a. Some abbreviations are not given, such as “temporal poles” and “inferior frontal gyrus”.

Really thanks a lot for your clear advice. We revised it clearly in our new manuscript.

Please see in the second paragraph of Introduction:

“Empathy for pain has been the major focus of research devoted to empathy in social neuroscience and other related fields, making it the most dominant neuroscientific domain in the study of empathy [7]. A review paper summarized research in this field for the past twenty years, it was found that the theme of empathy research gradually shifted from early personality traits, attitudes, and emotions to social cognition [8]. With the development of technology, research on the cognitive neuroscience of empathy became a hot topic. On one hand, some researchers thought that the medial prefrontal cortex (mPFC), superior temporal sulcus (STS), temporal poles (TP), and ventromedial cortex (VM cortex) were involved in cognitive empathy, and the amygdala, insula and inferior frontal gyrus (IFG) were involved in affective empathy. On the other hand, the right temporoparietal junction (rTPJ), the insula and the anterior midcingulate cortex (aMCC) were thought to be related to empathy for pain [9]. The aMCC and the insula were the “shared neural circuit” of empathy for pain [10]. In other research, the prefrontal cortex (PFC) and the anterior cingulate cortex (ACC) were closely related to empathy for pain [11]. Some new research found that the fusiform face area (FFA) was involved in empathy tasks [12]. The mirror neuron, “neural bridge” in social communication, occupies an important place in empathy [13].”

b. What is the meaning of “N170”? I noticed that this is explained in your 16th reference. Maybe you can explain what it means in your article.

That’s a creative question. But we did not explore N170 ERP component in this research. So we did not describe it more. But we also add some of its function as you suggested. As we know, N170 is sensitive to eye information. For example, isolated eye regions elicit N170 amplitudes and delayed latencies compared to faces (Parkington & Itier, 2018). Maybe, our future research can mainly explore whether the eye region information as a priming cue could elicit the N170.

Please see the third paragraph of Introduction.

“As we know, the face can provide important social information and reflect potential changes in the environment [14, 15]. People can infer and understand others’ inner state immediately by observing facial expressions. A study found that individuals with high empathy paid attention to various negative facial expressions (angry and afraid faces) more than those with low empathy from very-early stage (reflected in the N170) to late-stage (reflected in the LPP) processing of faces [16]. N170 is a negative component elicited by face’s feature and is sensitive to eye information. For example, isolated eye regions elicit N170 amplitudes and delayed latencies compared to faces. Hence, there is a close relationship between empathy and facial expression.”

c. In the third sentence of the sixth paragraph in your introduction, the conjunction “Nevertheless” may not be appropriate.

We appreciate that the reviewer’s spirit of preciseness. We have replaced it with “Further”.

“In summary, the eye region was found to be the important area for conveying facial expression [25]. In previous research, the ERP research concerning empathy for pain mostly used pictures and videos describing hands or feet in painful situations, or they used a painful facial expression to explore the subjects’ index of brain activity and behavioral changes when observing others’ pain [26, 27, 28, 29, 30]. To date, there have been a few ERP studies comparing the effect of negative emotions on empathy for pain [26, 27, 31]. For example, one supraliminal ERP study looking at the effect of eye emotional information on empathy for pain found a significant difference on P3 component induced by different eye conditions. The amplitude in neutral eyes condition was greater than that in sad eyes condition and fear eyes condition. Different supraliminal emotional information expressed by eye region affects late processing of empathy for pain [31]. Further, negative emotions have a profound influence on human survival and are important for social adaption from an evolutionary perspective [32]. Additionally, subliminal stimuli can also have impact on human behavior [33, 34, 35, 36, 37, 38]. In some situations, unconsciously processed stimuli could affect behavioral performance more profoundly than consciously processed stimuli [39]. For instance, a study found that unconsciously processed stimuli could enhance emotional memory after both short and long delays. This result indicated that emotion could enhance memory processing even when the stimuli was encoded unconsciously [40]. Another study found that people’s response to painful stimuli was more likely to be affected by unconscious negative emotions than the conscious negative emotions [14, 41]. Therefore, it’s imperative to study the processing of subliminal negative stimuli.”

We really thank the Reviewer for this suggestion. We have revised it according to your advice.

Please see the sixth and seventh paragraph.

In this study, we aimed to compare the neural response to subliminal sad and fearful negative emotions conveyed by eyes on empathy for pain with an ERP technique. We used a typically subliminal affective priming paradigm with an empathy task, which is similar to some previous studies [26, 27, 41], to investigate which negative emotion was highly correlated with empathy for pain automatically. The theory of emotion-sharing indicated that emotion-sharing between the self and others was the base of empathic behavior [42]. When individuals perceived others’ emotion, they automatically imitated others’ emotions and share the same representation. As we know, the fear emotion means danger and a crisis [43]. It can cause avoidance behaviors. In contrast, sadness can give rise to prosocial behaviors [44]. Furthermore, the priming pictures in one of the previous studies were situational pictures that stimulate participants’ own emotions [26]. While our procedure was different in term of that we used different eye emotions as cues to prime empathy for pain. The eye cues were external emotion sources. Hence, we could supply some evidence of finding the suitable emotion from others when empathy for pain occurred to explain the subsequent social behaviors such as helping others or escaping. ”

Thanks for the reviewer’s advice. We have expressed it in declarative sentence.

Please see the revised part of it:the seventh paragraph.

“In this study, we aimed to compare the neural response to subliminal sad and fearful negative emotions conveyed by eyes on empathy for pain with an ERP technique. We used a typically subliminal affective priming paradigm with an empathy task, which is similar to some previous studies [26, 27, 41], to investigate which negative emotion was highly correlated with empathy for pain automatically. The theory of emotion-sharing indicated that emotion-sharing between the self and others was the base of empathic behavior [42]. When individuals perceived others’ emotion, they automatically imitated others’ emotions and share the same representation. As we know, the fear emotion means danger and a crisis [43]. It can cause avoidance behaviors. In contrast, sadness can give rise to prosocial behaviors [44]. Furthermore, the priming pictures in one of the previous studies were situational pictures that stimulate participants’ own emotions [26]. While our procedure was different in term of that we used different eye emotions as cues to prime empathy for pain. The eye cues were external emotion sources. Hence, we could supply some evidence of finding the suitable emotion from others when empathy for pain occurred to explain the subsequent social behaviors such as helping others or escaping. ”

Methods

a. The authors write "Nineteen participants with no history of brain injury or mental disorder participated in the experiment." Then, we can see “Thirty participants” and “another 29 participants’ coming up in the Experimental Design and Stimuli part. Did the authors make some writing mistakes or some other reasons?

Thanks a lot for your question. Because we have two kinds of stimuli. One is the priming stimuli, the other is the target stimuli. As a result, we asked two groups to evaluate the stimuli. The thirty participants assessed the priming pictures. Another 29 participants assessed the target pictures. The nineteen new participants just took part in the ERP experiment. They have been highlighted in light blue in the new manuscript.

“Participants

“Experimental Design and Stimuli

This study used an affective priming paradigm with a 3 priming type (subliminal neutral, sad, fear eye region information) × 2 target type (painful, nonpainful pictures) within-subject design. Therefore, there were 6 conditions in total: Neutral/ Painful, Neutral/ Non-Painful, Sad/ Painful, Sad/ Non-Painful, Fear/ Painful, Fear/ Non-Painful. The priming stimuli used in the experiment were 42 facial black and white pictures (comprising 14 subliminal sad, 14 subliminal fear, and 14 subliminal neutral pictures) selected from the Chinese Affective Face Picture System (CAFPS) [47]. As the total eye region from the CAFPS was not large enough, as well as that some eye region emotions were rated poorly (i.e. some sad eyes did not convey sad emotions sufficiently), a minority of them (7 pictures) were taken from the internet with only remaining the eye region. The gender of the characters in the images for each emotion type was equal. The targets were pictures showing a person’s hands in painful or nonpainful situations [48, 49]. The size of eye region pictures was adjusted to 260 pixels in width and 115 pixels in height. The size of masks was 255 × 105 pixels. They were obtained by randomly scrambling 10 × 10-pixel squares on every cropped face with MATLAB2016b. The size of targets was 369 × 287 pixels. The distance between the participants and the computer monitor was approximately 65 cm. The pictures were normalized for size, global contrast and luminance.

b. What is “IRI-C scale”? I did not find the full name of this abbreviation, which should be indicated in the text. There exists other improper abbreviation, for example the “PD”.

Thanks for the Reviewer’s advice. The IRI-C scale we used is the Chinese version of the “Interpersonal Reactivity Index-Chinese”. The PD scale, a subscale of the IRI-C, is short for the Personal Distress. We have revised it in the new manuscript.

We have given a brief description of IRI at the third paragraph of the “Experimental Procedure” section. Please see it in the new manuscript. This part has been highlighted in yellow in the new manuscript.

“After the EEG session, all participants were asked to complete the Chinese version of Interpersonal Reactivity Index scale (IRI-C scale) [3, 52], which contained 22 items. A 5-point Likert scale was used for responses, ranging from inappropriate (0 point) to very appropriate (4 points). 5 items were scored in reverse. In this questionnaire, empathy was divided into 4 parts: perspective-taking (tendency to spontaneously adopt the psychological point of view of others), empathy concern (“other-oriented” feelings of sympathy and concern for unfortunate others), fantasy (tendency to transpose themselves imaginatively into the feelings and actions of fictitious characters in books, movies, and plays) and personal distress (“self-oriented” feelings of personal anxiety and unease in tense interpersonal settings). Correlations between the personal distress subscale and ERP components was conducted in order to find out the relationship between state empathy in task and trait empathy [30]. ”

c. Why only make a correlation analysis between the pain effect and the Personal Distress (PD) subscales of the IRI-C? How about other scales of the IRI-C?

We referred to previous research about the correlation between the pain effect and the PD subscales of the IRI-C (Jiao, Wang, Peng, & Cui, 2017). And at the last paragraph of discussion, we have explained the reason in detail. What’s more, we also calculated the other scales of the IRI-C, but the correlations were not significant.

Results

The abbreviation “RT” is not clear.

We have revised it.

“Behavioral Results

A three-way repeated measures ANOVA was conducted to examine the reaction time (RT) differences between the experimental conditions. The results are depicted in Fig 2.”

Discussion

a. The authors write “Fear indicates danger and a crisis, which can cause avoidance behaviors.” This finding might be caused by people being more affected by sad eye emotion and sad eye emotion information requiring more attention.” Is there any grammatical error here?

Thank you very much. We have asked the expert who were good at English to revise it. It has been highlighted in yellow in the new manuscript.The first paragraph of Discussion:

“Previous studies showed the significance of subliminal stimuli. For instance, subliminal stimuli that failed to reach awareness may affect performance more effectively than stimuli that do reach awareness [55]. Invisible stimuli that are irrelevant to task are more disturbing than visible distractors because of failed communication in regions of the brain that normally suppress such responses [55]. Meanwhile, a study found that the affectively significant visual stimuli had privileged access to consciousness [56]. Our research initially used subliminal eye region information as the experimental stimulus to explore its effect on empathy for pain. The eye region was found to be an important area for conveying facial expression [25]. The subliminal paradigm in the present study was used to highlight the automatic processing of eye cues. Furthermore, unlike previous studies that roughly divided the experimental materials into positive, neutral, and negative emotion types, the current research divided the types of negative emotions more elaborate. We chose neutral, sad and fearful emotions because sad and fearful emotions have great significance for human survival. Sadness can give rise to prosocial behaviors [44] and fear can cause avoidance behaviors. Therefore, in this study, we compared the neural response to subliminal sad and fearful negative emotions conveyed by eye cues on empathy for pain by measuring the ERP responses.”

Thanks for your advice. We have replaced it with the goal of our research. It has been highlighted in yellow in the new manuscript.The fisrt paragraph of Discussion as above.

Thanks a lot. We deleted it.

We definitely appreciate the Reviewer’s suggestion. With the ERP technique, this study initially explored the effect of emotional information from eyes on empathy for pain. We discussed this question preliminarily. Therefore, the effect of gender difference in this phenomenon was not the major question. Similar to previous study (Fan & Han, 2008), what we studied was pervasive features of emotional information from eyes on empathy for pain. Besides, as we know, Han, Fan and Mao (2008) have studied the gender difference in empathy for pain. And we would explore whether this phenomenon in our study exists in different gender, age groups and even in some special subjects in future research.

Reviewer #2: This paper explored the effect of subliminal sad and fearful information conveyed by eyes on pain empathy by ERPs, and found that sad lead to slower response and greater P2 amplitude. The focus of the paper is interesting, the methods and used and the logic are reasonable, the structure of the article is clear. The following problems need further addressed.

Thank you so much for your suggestions.Please see the revised version of manuscript and manuscript with track changes. We also have Figure1,2,3,4(revised) version.

Major points:

We appreciate the Reviewer’s suggestion. But for the reason that we did not get interaction results between the primes and targets about P3 and LPC. Therefore, we did not explain it in the discussion.

On the other hand, we found an interaction between emotional primes and targets about the P2 component. In detail, the subliminal sad eye stimulus elicited a larger P2 amplitude than the subliminal fearful eye stimulus when participants were doing empathy for pain.

We appreciate the reviewer’s suggestion and we fully agree that we should present enough reasons about the significance of subliminal emotion and the difference between subliminal and supraliminal stimuli. We have added these parts highlighted in yellow in both the “Introduction and discussion” parts.

“Introduction

In summary, the eye region was found to be the important area for conveying facial expression [25]. In previous research, the ERP research concerning empathy for pain mostly used pictures and videos describing hands or feet in painful situations, or they used a painful facial expression to explore the subjects’ index of brain activity and behavioral changes when observing others’ pain [26, 27, 28, 29, 30]. To date, there have been a few ERP studies comparing the effect of negative emotions on empathy for pain [26, 27, 31]. For example, one supraliminal ERP study looking at the effect of eye emotional information on empathy for pain found a significant difference on P3 component induced by different eye conditions. The amplitude in neutral eyes condition was greater than that in sad eyes condition and fear eyes condition. Different supraliminal emotional information expressed by eye region affects late processing of empathy for pain [31]. Further, negative emotions have a profound influence on human survival and are important for social adaption from an evolutionary perspective [32]. Additionally, subliminal stimuli can also have impact on human behavior [33, 34, 35, 36, 37, 38]. In some situations, unconsciously processed stimuli could affect behavioral performance more profoundly than consciously processed stimuli [39]. For instance, a study found that unconsciously processed stimuli could enhance emotional memory after both short and long delays. This result indicated that emotion could enhance memory processing even when the stimuli was encoded unconsciously [40]. Another study found that people’s response to painful stimuli was more likely to be affected by unconscious negative emotions than the conscious negative emotions [14, 41]. Therefore, it’s imperative to study the processing of subliminal negative stimuli.

In this study, we aimed to compare the neural response to subliminal sad and fearful negative emotions conveyed by eyes on empathy for pain with an ERP technique. We used a typically subliminal affective priming paradigm with an empathy task, which is similar to some previous studies [26, 27, 41], to investigate which negative emotion was highly correlated with empathy for pain automatically. The theory of emotion-sharing indicated that emotion-sharing between the self and others was the base of empathic behavior [42]. When individuals perceived others’ emotion, they automatically imitated others’ emotions and share the same representation. As we know, the fear emotion means danger and a crisis [43]. It can cause avoidance behaviors. In contrast, sadness can give rise to prosocial behaviors [44]. Furthermore, the priming pictures in one of the previous studies were situational pictures that stimulate participants’ own emotions [26]. While our procedure was different in term of that we used different eye emotions as cues to prime empathy for pain. The eye cues were external emotion sources. Hence, we could supply some evidence of finding the suitable emotion from others when empathy for pain occurred to explain the subsequent social behaviors such as helping others or escaping.

Discussion

Previous studies showed the significance of subliminal stimuli. For instance, subliminal stimuli that failed to reach awareness may affect performance more effectively than stimuli that do reach awareness [55]. Invisible stimuli that are irrelevant to task are more disturbing than visible distractors because of failed communication in regions of the brain that normally suppress such responses [55]. Meanwhile, a study found that the affectively significant visual stimuli had privileged access to consciousness [56]. Our research initially used subliminal eye region information as the experimental stimulus to explore its effect on empathy for pain. The eye region was found to be an important area for conveying facial expression [25]. The subliminal paradigm in the present study was used to highlight the automatic processing of eye cues. Furthermore, unlike previous studies that roughly divided the experimental materials into positive, neutral, and negative emotion types, the current research divided the types of negative emotions more elaborate. We chose neutral, sad and fearful emotions because sad and fearful emotions have great significance for human survival. Sadness can give rise to prosocial behaviors [44] and fear can cause avoidance behaviors. Therefore, in this study, we compared the neural response to subliminal sad and fearful negative emotions conveyed by eye cues on empathy for pain by measuring the ERP responses.

”

Thanks for your advice. Firstly, we have already assessed both the priming and target stimuli. We have written it in the second paragraph of the “Experimental Design and Stimuli” part.

Secondly, although we only have 15 valid participants, the results of our effect size (η2p) (Please check the value in the manuscript) was larger enough to indicate our results were stable. Moreover, the number of participants in some empathy research with ERP technique published also had less than 20 people (Jiao, Wang, Peng & Cui, 2017; Suzuki, Galli, Ikeda, Itakura & Kitazaki, 2015; Jiang, Varnum, Hou & Han, 2013; Mu, Fan, Mao & Han, 2008; Fan & Han, 2008). So, we think that our result was a sound one.

Thirdly, we also have reported interactions and the simple effect of the two independent variables’ interactions in subsequent analyses. Please see the detailed parts in the manuscript.

4. In view of the current results, there is a suggestion for data analysis. When analyzing ERP data, the author conducted repeated measurement analysis of brain region × primes (sad, fearful and neutral) × target type (painful or nonpainful), and the main results focused on the main effect of the region, while other results were not good enough. The ERP components differed in different brain regions, which is natural and easily understood results. Therefore, the analysis of specific ERP component can be conducted by analyzing the differences in brain regions first, and then analyze the electrodes of the most obvious region with prime types× target types measurements, which can more effectively reflect the author's intention.

Thanks a lot for your brilliant advice. The statistical method we used referred to previous studies (Cheng, Jiao, Luo, & Cui, 2017; Jiao, Wang, Peng, & Cui, 2017; Luo, Feng, He, Wang, & Luo, 2010; Mu & Han, 2013) and our own topographical distribution. So, we have such confidence to believe that our statistical method is authentic.

Especially for P2, the classical regions about empathy involved the frontal and central regions (Han, Luo & Han, 2015; Luo, Han, Du & Han, 2018). However, P2 involved the centro-parietal regions (Xu, Li, Ding, Zhang, Fan, Diao et al., 2015; Pesciarelli, Leo & Sarlo, 2016) and the parieto-occipital regions (Liu, Pinheiro, Zhao, Nestor, McCarley & Niznikiewicz, 2012) when the research was about emotion. In this study, P2 was calculated via the frontal, frontal-central, central, centro-parietal and parietal regions on account of this study contained empathy and emotion (Cheng, Jiao, Luo & Cui, 2017). Because of the uncertainty in the studies about P2 until now, we chose wide regions to study the feature for P2 in empathy field, especially in our subliminal design.

We did consider your advice thoroughly. Our work was the first one to detect the eye region effect on pain empathy with subliminal paradigm which might have less effect than that in supraliminal paradigm, so we wanted to study the difference through wide brain regions to find out the changing tendency in our experimental design in order not to miss some vital findings. And it might be provide some evidence for further study which might be focused on special region for special effect. It did have some creative value in empathy field. And we really did the analysis on the basis of a series of references in this field. The region we chose was from frontal to parietal, which can make our analysis more consistent among different components. We just followed the main clue. If there was interaction, we reported it. If there was none, we did not further analyse it.

If you have more opinions, we really appreciate you can instruct us, discuss with us and please give us another chance to revise it. Thank you so much again.

Minor points:

Figure 1: It is suggested to replace the eyes, mask and target of the actual material samples.

Thanks for your suggestion. We have revised it.

Please see the Figure1 (revised).

Really thanks for your detailed suggestion. We have repainted the pictures. It looks nice now.

Please see the Figure2 (revised).

Figure 3: The ERP figure is not clear enough to see the detail including time axis. There are six lines in the ERP figure. It is recommended to take the peaks and draw a bar chart to express the results more clearly.

Thanks a lot. We have repainted according to your advice.

Please see the Figure3 (revised).

References

Cheng, J., Jiao, C., Luo, Y., & Cui, F. (2017). Music induced happy mood suppresses the neural responses to other's pain: Evidences from an ERP study. Scientific Reports, 7(1).

Fan, Y., & Han, S. (2008). Temporal dynamic of neural mechanisms involved in empathy for pain: An event-related brain potential study. Neuropsychologia, 46(1),160-173.

Han, S., Fan, Y., & Mao, L. (2008). Gender difference in empathy for pain: An electrophysiological investigation. Brain Research, 1196, 85-93.

Han, X. C., Luo, S. Y., & Han, S. H. (2015). Embodied neural responses to others’ suffering. Cognitive Neuroscience, 7(1–4), 114–127.

Jiang, C., Varnum, M. E. W., Hou, Y., & Han, S. (2013). Distinct effects of self-construal priming on empathic neural responses in Chinese and Westerners. Social Neuroscience, 9(2),130-138.

Jiao, C., Wang, T., Peng, X., & Cui, F. (2017). Impaired empathy processing in individuals with internet addiction disorder: An Event-Related Potential study. Frontiers in Human Neuroscience, 11, 498.

Liu, T., Pinheiro, A., Zhao, Z., Nestor, P., McCarley, R., & Niznikiewicz, M. (2012). Emotional cues during simultaneous face and voice processing: Electrophysiological insights. PLoS ONE, 7(2), e31001.

Luo, W., Feng, W., He, W., Wang, N., & Luo, Y. (2010). Three stages of facial expression processing: ERP study with rapid serial visual presentation. NeuroImage, 49(2), 1857-1867.

Luo, S., Han, X., Du, N., & Han, S. (2018). Physical coldness enhances racial in-group bias in empathy: Electrophysiological evidence. Neuropsychologia, 116, 117-125.

Mu, Y., Fan, Y., Mao, L., & Han, S. (2008). Event-related theta and alpha oscillations mediate empathy for pain. Brain Research, 1234, 128-136.

Mu, Y., Han, S. (2013). Neural oscillations dissociate between self-related attentional orientation versus evaluation. NeuroImage, 67, 247-256.

Parkington K.B., Itier R. J. (2018). One versus two eyes makes a difference! Early face perception is modulated by featural fixation and feature context, CORTEX.

Pesciarelli, F., Leo, I., & Sarlo, M. (2016). Implicit Processing of the Eyes and Mouth: Evidence from Human Electrophysiology. PLOS ONE, 11(1), e0147415.

Suzuki, Y., Galli, L., Ikeda, A., Itakura, S., & Kitazaki, M. (2015). Measuring empathy for human and robot hand pain using electroencephalography. Scientific Reports, 5(1).

Xu, M., Li, Z., Ding, C., Zhang, J., Fan, L., Diao, L., & Yang, D. (2015). The divergent effects of fear and disgust on inhibitory control: An ERP study. PLoS ONE, 10(6), e0128932.

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PLoS One. doi: 10.1371/journal.pone.0226211.r003

Decision Letter 1

Kai Wang

22 Nov 2019

The effect of emotional information from eyes on empathy for pain: A subliminal ERP Study

PONE-D-19-16381R1

Dear Dr. Song,

We are pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it complies with all outstanding technical requirements.

Within one week, you will receive an e-mail containing information on the amendments required prior to publication. When all required modifications have been addressed, you will receive a formal acceptance letter and your manuscript will proceed to our production department and be scheduled for publication.

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With kind regards,

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PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

PLoS One. doi: 10.1371/journal.pone.0226211.r004

Acceptance letter

Kai Wang

6 Dec 2019

PONE-D-19-16381R1

The effect of emotional information from eyes on empathy for pain: A subliminal ERP Study

Dear Dr. Song:

I am pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please notify them about your upcoming paper at this point, to enable them to help maximize its impact. If they will be preparing press materials for this manuscript, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

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With kind regards,

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on behalf of

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Data Availability Statement

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PERMALINK

The effect of emotional information from eyes on empathy for pain: A subliminal ERP study

Juan Song

Yanqiu Wei

Han Ke

Roles

Abstract

Introduction

Materials and methods

Participants

Experimental design and stimuli

Experimental procedure

Fig 1. The procedure of the effect of subliminal emotional information from eyes on empathy for pain.

Devices and recording

Data analysis

Results

Behavioral results

Fig 2. Behavioral results under six experimental conditions.

ERP results

N1

P2

Fig 3. Illustration of ERP results at representative electrodes.

Fig 4. Topographical maps of P2, P3 and LPC for the painful conditions.

N2

P3

LPC

Correlations between the IRI-C and ERP

Discussion

Limitations

Conclusions

Acknowledgments

Data Availability

Funding Statement

References

Decision Letter 0

Kai Wang

Roles

Author response to Decision Letter 0

Decision Letter 1

Kai Wang

Roles

Acceptance letter

Kai Wang

Roles

Associated Data

Supplementary Materials

Data Availability Statement

ACTIONS

PERMALINK

RESOURCES

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