Neural mechanisms of modulations of empathy and altruism by beliefs of others’ pain

Aesop’s fable ‘The boy who cried wolf’ tells a story that villagers run or do not run to help a shepherd boy who cries wolf depending on whether or not they believe that the boy’s crying indicates his actual emotion and need. This story illustrates an important character of human altruistic behavior, that is, perceived cues signaling others’ suffering drives us to do them a favor only when we believe that their suffering is true. Although this character of human altruism was documented over 2000 years ago in Aesop’s fable and is widely observed in current human societies, its psychological and neural underpinnings have not been fully understood. The present study investigated how beliefs of others’ pain (BOP) modulate human altruistic behavior independently of perceived cues signaling others’ suffering and whether the modulation effect, if any, is mediated by changes in empathy for others’ pain and relevant brain underpinnings.

Empathy refers to understanding and sharing of others’ emotional states (Decety and Jackson, 2004) and has been proposed to provide a key motivation for altruistic behavior in both humans and animals (Batson et al., 2015; de Waal, 2008; Decety et al., 2016). Empathy can be induced by perceived cues signaling others’ pain that activate neural responses in brain regions underlying sensorimotor resonance (e.g., the sensorimotor cortex), affective sharing (e.g., the anterior insula [AI] and anterior cingulate cortex [ACC]), and mental state inference/perspective-taking (e.g., the medial prefrontal cortex [mPFC] and temporoparietal junction [TPJ]) (Singer et al., 2004; Jackson et al., 2005; Avenanti et al., 2005; Saarela et al., 2007; Fan and Han, 2008; Shamay-Tsoory et al., 2009; Han et al., 2009; Sheng and Han, 2012; Fan et al., 2011; Lamm et al., 2011; Zhou and Han, 2021). Neural responses to others’ pain in the empathy network and functional connectivity between its key hubs can predict motives for subsequent altruistic actions (e.g., Hein et al., 2010; Hein et al., 2016; Mathur et al., 2010; Luo et al., 2015). These brain imaging findings revealed neural mechanisms underlying the perception-emotion-behavior reactivity (e.g., perceived pain-empathy-help) that occurs often in everyday lives (Eisenberg et al., 2010; Hofman, 2008; Penner et al., 2005). However, empathic neural responses are influenced by multiple factors such as perceptual features depicting others’ pain (Gu and Han, 2007; Li and Han, 2019), observers’ perspectives and attention (Gu and Han, 2007; Li and Han, 2010; Jauniaux et al., 2019), and perceived social relationships between observers and empathy targets (Xu et al., 2009; Avenanti et al., 2010; Hein et al., 2010; Mathur et al., 2010; Sheng and Han, 2012; Azevedo et al., 2013; Sheng et al., 2014; Sheng et al., 2016; Han, 2018; Zhou and Han, 2021). What remains unclear is whether and how BOP modulates empathic brain activity through which to further influence altruistic behavior. To address these issues is crucial for understanding variations of empathy and altruism during complicated social interactions as illustrated in Aesop’s fable.

Beliefs refer to mental representations of something that are not immediately present to the scenes but allow people to think beyond what is here and now (Fuentes, 2019). Beliefs reflect an organism’s endorsement of a particular state of affairs as actual (McKay and Dennett, 2009). Beliefs that best approximate reality enable the believers to act effectively and maximize their survival (Fodor, 1985; Millikan, 1995). Previous research has shown that beliefs affect multiple mental processes such as visual awareness (Sterzer et al., 2008) and processing of emotions (Petrovic et al., 2005) including experiences of pain (Wager et al., 2004; Colloca and Benedetti, 2005). The function of beliefs is also manifested in increasing the efficiency of neural processes involved in decision-making and goal setting (Garcés and Finkel, 2019; Régner et al., 2019). Potential effects of beliefs on empathic neural responses were tested by presenting participants with photographs showing pain inflicted by needle injections into a hand that was believed to be or not to be anesthetized (Lamm et al., 2007). Functional magnetic resonance imaging (fMRI) of brain activity suggested modulations of insular responses to perceived pain by beliefs of anesthetization. However, the results cannot be interpreted exclusively by BOP because the stimuli (i.e., needles) used to induce beliefs of numbed and non-numbed hands were different. An ideal paradigm for testing modulations of empathy by BOP independently of perceived cues signaling others’ pain should compare brain activities in response to identical stimuli under different beliefs and enable researchers to test how BOP influences altruistic behavior.

In six behavioral, electroencephalography (EEG), and fMRI experiments, the current study tested the hypothesis that BOP affects empathy and altruistic behavior by modulating brain activity in response to others’ pain. Specifically, we predicted that lack of BOP may result in the inhibition of altruistic behavior by decreasing empathy and its underlying brain activity. Our behavioral, EEG, and fMRI experiments were designed based on the common beliefs that patients show pain expressions to manifest their actual feelings of pain whereas pain expressions performed by actors/actresses do not indicate their actual emotional states. To examine BOP effects on empathy, we experimentally manipulated BOP by asking participants to learn and remember different identities (i.e., patient or actor/actress) of a set of neutral faces during a learning procedure. Thereafter, we measured self-reports of others’ pain and own unpleasantness from the participants when they viewed learned faces with pain or neutral expressions. During EEG/fMRI recording, the participants were asked to discriminate patient or actor/actress identities of faces with pain or neutral expressions. We compared self-reports of others’ feelings and brain activities related to pain (vs. neutral) expressions of patients’ faces with those related to actors/actresses’ faces. If the perception of patients’ pain expressions implicitly activates BOP whereas perception of actors/actresses’ pain expressions does not activate BOP, we expected that lack of BOP (i.e., to compare actors/actresses vs. patients) would reduce self-report of empathy, empathic brain activity, and altruistic behavior. We further predicted that BOP effects on altruistic behavior might be mediated by decreased empathy and empathic brain activity due to lack of BOP.

Similar to previous research (Jackson et al., 2005; Fan and Han, 2008; Hein et al., 2010; Mathur et al., 2010; Sheng and Han, 2012), we adopted both subjective and objective estimations of empathy for others’ pain. Subjective estimation of empathy for pain depends on the collection of self-reports of others’ painful feelings and one’s own unpleasantness when viewing others’ suffering (e.g., Bieri et al., 1990; Jackson et al., 2005; Lamm et al., 2007; Fan and Han, 2008; Sheng and Han, 2012). Objective estimation of empathy for pain relies on recording of brain activities, using fMRI or EEG, that differentially respond to painful versus non-painful stimuli applied to others (e.g., Singer et al., 2004; Jackson et al., 2005; Gu and Han, 2007; Fan and Han, 2008; Hein et al., 2010) or to others’ faces with pain versus neutral expressions (Botvinick et al., 2005; Saarela et al., 2007; Han et al., 2009; Sheng and Han, 2012). Brain responses to perceived non-painful stimuli applied to others or neutral expressions were also collected to control empathy-unrelated perceptual or motor processes. fMRI studies revealed greater activations in the ACC, AI, and sensorimotor cortices in response to painful compared to non-painful stimuli applied to others (e.g., Singer et al., 2004; Jackson et al., 2005; Gu and Han, 2007; Hein et al., 2010; see Lamm et al., 2011; Fan et al., 2011 for review). EEG studies showed that event-related potentials (ERPs) in response to perceived painful stimulations applied to others’ body parts elicited neural responses that differentiated between painful and neutral stimuli over the frontal region as early as 140 ms after stimulus onset (Fan and Han, 2008; see Coll, 2018 for review). Moreover, the mean ERP amplitudes at 140–180 ms predicted self-report of others’ pain and one’s own unpleasantness (Fan and Han, 2008).

Particularly related to the current work are neuroimaging findings that compared brain responses to pain versus neutral expressions. fMRI studies found that viewing video clips (Botvinick et al., 2005) or pictures (Sheng et al., 2014) showing faces with pain versus neutral expressions or viewing photos of faces of patients who were suffering from provoked pain versus chronic pain (Saarela et al., 2007) induced activations in the ACC, AI, and inferior parietal cortex. Moreover, the cortical areas activated by facial expressions of pain were also engaged by the first-hand experience of pain evoked by thermal stimulation (Botvinick et al., 2005). Moreover, the strengths of AI activations during observation of others’ pain were correlated with subjective feelings of others’ pain (Saarela et al., 2007). ERP studies found that neural responses to pain expressions occurred as early as 130 ms after face onset over the frontal/central regions as indexed by the increased amplitude of a positive component at 128–188 ms (P2) in response to pain compared neutral expressions (Sheng and Han, 2012; Sheng et al., 2013; Sheng et al., 2016; Han et al., 2016; Li and Han, 2019). In addition, the P2 amplitudes in response to others’ pain expressions positively predicted subjective feelings of own unpleasantness induced by others’ pain and self-reports of one’s own empathy traits (Sheng and Han, 2012). In addition, source estimation of the P2 component in response to others’ pain expressions suggested a possible origin in the ACC. Taken together, these brain imaging findings suggest effective subjective and objective measures of empathy (i.e., understanding and sharing of others’ pain) that are suitable for the investigation of neural mechanisms underlying modulations of empathy and altruism by BOP.

In Experiment 1, we randomly assigned patient or actor/actress identities to faces to test how experimentally manipulated BOP associated with face identities caused changes in empathy (i.e., subjective evaluation of others’ pain) and altruistic behavior (i.e., monetary donations). We predicted that lack of BOP related to actors/actresses (vs. patients) would result in reduced empathy and altruistic behavior. In Experiment 2, based on the common belief that an effective medical treatment reduces a patient’s pain, we tested whether decreasing BOP due to knowledge of effective medical treatments of patients also reduced empathy and altruistic behavior.

In Experiments 3 and 4, we investigated whether BOP modulates empathic brain activity by recording EEG signals in response to pain or neutral expressions of faces with patient or actor/actress identities. Brain activities related to empathy were quantified by comparing neural responses to pain versus neutral expressions to exclude neural processes of facial structures, social attributes (e.g., gender), and other empathy-unrelated information. Given previous findings that the P2 amplitude increased to pain compared to neutral expressions and was associated with self-report of sharing of others’ pain (Sheng and Han, 2012; Sheng et al., 2013; Sheng et al., 2016; Han et al., 2016; Li and Han, 2019), we focused on how the P2 amplitude in response to pain (vs. neutral) expressions was modulated by facial identities (i.e., patient or actor/actress) that link to different beliefs (i.e., patients’ pain expressions manifest their actual feelings whereas actors/actresses’ pain expressions do not). Our ERP results showed evidence that actor/actress compared to patient identities of faces decreased the empathic neural responses (i.e., P2 amplitudes in response to pain [vs. neutral] expressions) within 200 ms post-stimulus. In Experiment 5, we further revealed behavioral and EEG evidence that neural responses to pain expressions of faces mediate BOP effects on empathy and monetary donations.

In Experiment 6, we employed fMRI to examine brain regions in which blood oxygen level-dependent (BOLD) signals are modulated by BOP. We examined BOLD responses to faces that had either patient or actor/actress identities, received painful/non-painful stimulations, and showed pain or neutral expressions. fMRI results allowed us to test whether empathic neural responses in the cognitive (i.e., the dorsal mPFC and TPJ; Völlm et al., 2006; Schnell et al., 2011; also see Lamm et al., 2011; Fan et al., 2011; Shamay-Tsoory, 2011), sensorimotor/affective (i.e., the ACC, insula, and sensorimotor cortex; Jackson et al., 2005; Singer et al., 2004; Avenanti et al., 2005), or both nodes of the empathic neural network would be modulated by BOP that was manipulated by assigning different identities (i.e., patient or actor/actress) to empathy targets. In addition, we examined whether neural responses in the empathic network would be able to predict variations of subjective feelings of others’ pain due to lack of BOP.

Taken together, our behavioral and brain imaging results showed consistent evidence that lack of BOP or decreasing BOP resulted in reduced empathy and altruistic behavior. Our findings suggest that BOP may provide a cognitive basis for human empathy and altruism and uncover intermediate brain mechanisms by which BOP influences empathy and altruistic behavior.

We conducted six experiments to investigate psychological and neural mechanisms underlying BOP impacts on empathy and altruistic behavior in humans. We manipulated individuals’ BOP by randomly assigning patient or actor/actress identities to faces as there was a lack of BOP for actors/actresses’ faces but not for patients’ faces. We also estimated individuals’ intrinsic BOP by asking the participants to estimate the effectiveness of medical treatments of patients to trigger BOP as an effective medical treatment reduces a patient’s pain. We further measured brain activity using EEG and fMRI to examine BOP effects on empathic neural responses with high temporal and spatial resolutions, respectively. Our behavioral and neuroimaging findings showed evidence for a functional role of BOP in modulations of the perception-emotion-behavior reactivity by illustrating how BOP predicted and affected self-reports of empathy, empathic brain activities, and monetary donations. Our findings suggest that BOP may provide a cognitive basis for empathy and altruistic behavior in humans.

Experiments 1 and 2 showed behavioral evidence that manipulated changes in BOP caused subsequent variations of self-report of empathy and altruistic behavior along the directions as predicted. Specifically, decreasing BOP concomitant with changes in face identities (from patient to actor/actress) or changes in effective medical treatments (from suffering due to a disease to recovery due to medical treatment) significantly reduced self-report of both cognitive (perceived intensity of others’ pain) and affective (own unpleasantness induced by perceived pain in others) components of empathy. Decreasing BOP also inhibited following altruistic behavior that was quantified by the amount of monetary donations to those who showed pain expressions. By contrast, reassuring patient identities in Experiment 1 or by noting the failure of medical treatment related to target faces in Experiment 2 increased subjective feelings of others’ pain and own unpleasantness and prompted more monetary donations to target faces. The increased monetary donations might be due to repeatedly confirming patient identity or knowing the failure of medical treatment increased the belief of authenticity of targets’ pain and thus enhanced cognitive and affective components of empathy. Alternatively, repeatedly confirming patient identity or knowing the failure of medical treatment might activate other emotional responses to target faces such as pity or helplessness, which might also influence altruistic decisions. The increased empathy rating scores and monetary donations might also reflect a contrast effect due to rating patient and actor/actress targets alternately. These possible accounts can be clarified in future work by asking participants to report their emotions and performing rating tasks on patient and actor/actress targets in separate blocks of trials. In consistent with the effects of manipulated BOP on empathy and altruism across the participants, the results of Experiment 2 showed that individuals’ intrinsic BOP related to each target face predicted their self-report of empathy and altruistic behavior across different target faces. Moreover, decreased (or increased) intrinsic BOP also predicted changes in empathy/altruistic behavior across different target faces. These converging behavioral findings across different participants and across different target faces provide evidence for causal relationships between BOP and empathy/altruism.

Our results showed that self-reports of others’ pain intensity and own unpleasantness elicited by perception of others’ pain were able to positively predict altruistic behavior across individuals. Previous research using questionnaire measures of empathy ability found that empathy as a trait is positively correlated with the amount of money shared with others in economic games (Edele et al., 2013; Li et al., 2019). Taken together, these findings are consistent with the proposition that empathy, as either an instant emotional response to others’ suffering (e.g., estimated in our study) or a personality trait (e.g., estimated in Edele et al., 2013 and Li et al., 2019), plays a key role in driving altruistic behavior (Batson, 1987; Batson et al., 2015; Eisenberg et al., 2010; Hofman, 2008; Penner et al., 2005). Our mediation analyses of the behavioral data in both Experiments 1 and 2 further revealed that the effects of decreased BOP on monetary donations were mediated by self-report of others’ pain intensity. These results further suggest empathy as an intermediate mechanism of the BOP effects on altruistic behavior.

Our neuroimaging experiments went beyond the subjective estimation of the relationships between BOP and empathy/altruism by investigating neural mechanisms underlying BOP effects on empathy for others’ pain. It is necessary to conduct the objective estimation of empathy to examine BOP effects because self-report measures of empathy can be influenced by social contexts and are unable to unravel brain mechanisms underlying BOP effects on empathy (e.g., Sheng and Han, 2012). Our EEG results in Experiments 3 and 5 repeatedly showed that neural responses to pain (vs. neutral) expressions over the frontal regions within 200 ms after face onset (indexed by the P2 amplitude over the frontal/central electrodes) were significantly reduced to faces with actor/actress identities compared to those with patient identities. The results in Experiments 3 and 4 indicate that BOP concomitant with face identity (i.e., patients’ pain expressions manifest their actual painful emotional states whereas actors/actresses’ pain expressions do not) rather than face identity (e.g., Tiger or Lion team identities) alone resulted in modulations of the P2 amplitudes to pain expressions in the direction as expected. Numerous EEG studies have shown that the frontal P2 component responds with enlarged amplitudes to various facial expressions such as fear, anger, happy (Williams et al., 2006; Luo et al., 2010; Calvo et al., 2013), and pain (Sheng and Han, 2012; Sheng et al., 2013; Sheng et al., 2016) expressions compared to neutral faces. These findings uncovered early affective processing by differentiating emotional and neutral expressions. ERPs to others’ pain within 200 ms post-stimulus occur regardless of task demands and are associated with spontaneous empathy for pain (Fan and Han, 2008). Our ERP results indicate that BOP may provide a cognitive basis for early spontaneous neural responses to others’ suffering reflected in pain expressions. Moreover, the results in Experiment five showed that the early spontaneous empathic neural responses in the P2 time window mediated the BOP effect on self-report of others’ pain intensity, which further mediated the relationship between the P2 empathic responses and the amount of monetary donations. These results highlight both early spontaneous neural responses to others’ pain and subjective feelings of others’ pain as intermediate mechanisms by which BOP influences altruistic behavior.

To identify neural architectures underlying BOP effects on empathy, we recorded BOLD responses, using fMRI, to perceived painful and non-painful stimuli applied to individuals with patient or actor/actress identities in Experiment 6. We showed that the contrast of perceived painful (vs. non-painful) stimulations activated the sensory (i.e., post-central gyrus), affective (i.e., insula), and cognitive (i.e., mPFC) nodes of the empathy network, similar to the findings of previous studies (Singer et al., 2004; Jackson et al., 2005; Saarela et al., 2007; Shamay-Tsoory et al., 2009; Han et al., 2009; Fan et al., 2011; Lamm et al., 2011; Zhou and Han, 2021; Luo et al., 2014). Viewing non-painful stimulations applied to neutral faces with patient versus actor/actress identities revealed increased activity in the mPFC and bilateral TPJ, suggesting the possible neural representation of facial identities in the brain regions. Most importantly, the results of searchlight RSA that was sensitive to both stimuli and subjective feelings evoked by the stimuli revealed significant variations of activities in the insula, post-central gyrus, and lateral frontal cortex in correspondence with the patterns of self-reports of empathy for patients and actors/actresses’ pain. In other words, the patterns of the activities in the insula, post-central gyrus, and lateral frontal cortex were able to predict distinct subjective feelings of patients’ and actors/actresses’ pain. Moreover, the results of our VPS analyses showed consistent evidence for decreased neural activities in the empathy-related neural network due to lack of BOP. These fMRI results together suggest that activities in the brain regions supporting affective sharing (e.g., insula; Shamay-Tsoory et al., 2009; Fan et al., 2011; Lamm et al., 2019), empathic sensorimotor resonance (e.g., post-central gyrus; Avenanti et al., 2005; Zhou and Han, 2021), and emotion regulation (e.g., lateral frontal cortex; Ochsner and Gross, 2005; Etkin et al., 2015) may provide intermediate mechanisms underlying variations of subjective feelings of others’ pain intensity due to lack of BOP.

Numerous studies have shown evidence for modulations of empathy by social contexts. Contextual variables that influence the perception of others’ pain and empathy include empathy targets’ posture (Martel et al., 2008), identifiable pain pathology (Twigg and Byrne, 2015), moral valence (Cui et al., 2016; Nicolardi et al., 2020), and so on. Empathizers’ prior exposure to pain (Prkachin and Rocha, 2010), socioeconomic status (Varnum et al., 2015), and cultural experiences (Wang et al., 2015; Hampton and Varnum, 2018) also influence empathy and its underlying brain activities. Perceived information about social relationships between observers and empathy targets also modulates empathic neural responses such that, relative to viewing own-race or own-team individuals’ pain, viewing other-race or opponent-team individuals’ pain decreased empathic neural responses in the affective (e.g., ACC and AI), cognitive (e.g., mPFC and TPJ), and sensorimotor (e.g., motor cortex) nodes of the empathy network (Xu et al., 2009; Avenanti et al., 2010; Hein et al., 2010; Mathur et al., 2010; Sheng and Han, 2012; Sheng et al., 2014; Sheng et al., 2016; Han, 2018; Zhou and Han, 2021). The perceived intergroup (racial) relationships between empathizers and empathy targets also influenced altruistic behavior such as medical treatment (Drwecki et al., 2011). These findings uncovered how social information perceived from stimuli and social experience modulate empathic neural responses to others’ suffering and subsequent social behavior. The results of our current work complemented the findings of previous studies by uncovering how beliefs, as preexisting internal mental representations of something that is not immediately present to the scenes (Fuentes, 2019), also modulate people’s empathy and following altruistic behavior. Specifically, in the current study, participants’ beliefs (i.e., pain expressions of patients manifest their actual feelings whereas pain expressions performed by actors/actresses do not) weakened the participants’ empathy for others’ pain and reduced their monetary donations to those who appeared suffering. BOP effects on empathy and altruistic behavior can be understood as modulations of empathy by preexisting internal information (e.g., beliefs) whereas previous findings revealed modulations of empathy by instantly perceived social information in a specific social context. These findings together help to construct neurocognitive models of empathy that take into consideration of both perceived social information and preexisting internal information and their interactions that lead to modulations of empathy and altruistic behavior during real-life social interactions.

It should be noted that our experimental manipulations changed the participants’ minds about the models’ identities (e.g., patient vs. actor/actress) rather than explicitly asking them to alter their BOP. BOP altered implicitly with target persons’ identities due to observers’ knowledge about individuals with different identities (e.g., painful stimuli applied to actors/actresses do not really hurt them and they show facial expressions to pretend a specific emotional state). Therefore, the BOP effects on empathy and altruistic behavior identified in our study might take place implicitly. This is different from the placebo effects on first-hand pain experiences that are produced by explicitly perceived verbal, conditioned, and observational cues that induce expectations of effective analgesic treatments (Meissner et al., 2011). Similar explicit manipulations of making individuals believe receiving oxytocin also promote social trust and preference for close social distances (Yan et al., 2018). Moreover, the placebo treatment relative to a control condition significantly attenuated activations in the ACC, AI, and subcortical structures (e.g., the thalamus) in response to painful electric shocks but increased the prefrontal activity during anticipation of painful stimulations possibly to inhibit activity in pain processing regions (Wager et al., 2004; Wager and Atlas, 2015). The brain regions in which empathic neural responses altered due to BOP (e.g., the lateral frontal cortex) as unraveled in the current study do not overlap with those in which activities are modulated by placebo analgesia (Atlas and Wager, 2014). These results suggest that there may be distinct neural underpinnings of BOP effects on empathic brain activity and placebo effects on brain responses to first-hand pain experiences.

Do beliefs also provide a cognitive basis for the widely documented ingroup bias in empathy for pain? Previous studies suggest that multiple neurocognitive mechanisms are involved in ingroup bias in empathy for pain such as lack of attention (Sheng and Han, 2012) and early group-based categorization of outgroup faces (Zhou et al., 2020b, see Han, 2018 for review). There have been behavioral evidence that White individuals who more strongly endorsed false beliefs about biological differences between Blacks and Whites (e.g., ‘Black people’s skin is thicker than White people’s skin’) reported lower pain ratings for a Black (vs. White) target and suggested less accurate treatment recommendations (Hoffman et al., 2016). These behavioral findings suggest that other beliefs may also provide a basis for modulations of empathy for others’ pain and relevant altruistic behavior. The underlying brain mechanisms, however, remain unknown. The paradigms developed in the current study may be considered in future research to examine neural underpinnings of the effects of false beliefs on empathy for pain.

Another question arising from the findings of the current study is whether the belief effect is specific to neural underpinnings of empathy for pain or is also evident for neural responses to other facial expressions. To address this issue, we conducted an additional EEG experiment in which we tested (1) whether beliefs of authenticity of others’ happiness influence brain responses to perceived happy expressions, and (2) whether lack of beliefs of others’ happiness also modulates neural responses to happy expressions in the P2 time window, similar to the BOP effect on ERPs to pain expressions (see Appendix 1 for methods). Similar to the paradigm used in Experiment 3, participants in the additional experiment had to first remember face identities (awardees or actors/actresses). Thereafter these faces with happy or neutral faces were presented with contextual information that the awardees showed happy expressions when receiving awards whereas actors/actresses imitated others’ happy expressions. The participants also performed identity judgments on the faces while EEG was recorded. Behavioral results in this experiment showed that participants reported less feelings of actors’ happiness compared to awardees’ happiness. ERP results in this experiment showed that lack of beliefs of authenticity of others’ happiness (e.g., actors simulating others’ happy expressions vs. awardees smiling when receiving awards) reduced the amplitudes of a long-latency positive component (i.e., P570) over the frontal region in response to happy expressions. However, the face identities did not affect the P2 amplitudes in response to happy (vs. neutral) expressions (see Appendix 1 for statistical details). These findings suggest that belief effects are evident for subjective feelings and brain activities in response to happy expressions. However, BOP or happiness affect neural responses to facial expressions in different time windows after face onset. Future research should examine neural mechanisms underlying belief effects on neural responses to other emotions to deepen our understanding of general belief effects on neural processes of others’ emotional states.

Our behavioral and neuroimaging findings have implications for how we understand the general functional role of beliefs in social cognition and interaction. Empathy is supposed to originate from an evolved adaptation to quickly and automatically respond to others’ emotional states during parental care that is necessary for offspring survival in humans and other species (de Waal, 2008; Decety, 2011). In most cases of interactions among family members (i.e., between parents and offspring or between siblings) perceived cues signaling pain in a person manifest his/her actual emotional states that urge help from other family members. Such life experiences may set up a default belief that perceived painful stimulation to others and their facial expressions reflect individuals’ actual emotional states. This default belief provides a fundamental cognitive basis of reflexive and automatic empathy and empathic brain activity that further generates autonomic and somatic responses, as suggested by the perception-action model of empathy (Preston and de Waal, 2002). Nevertheless, when social interactions expand beyond family members to non-kin members and even strangers, perceived pain expressions or painful stimuli applied to others may not always manifest others’ actual emotional states because perceived painful cues may be fake in some cases. BOP in such situations may function as cognitive gate-control to modulate neural responses to perceived pain in others. This is necessary for monitoring social interactions to determine whether to help or to coordinate with those who appear suffering. Our findings illustrate how the perception-emotion-behavior reactivity occurs under the cognitive constraint of BOP to keep empathy and altruistic decision/behavior for the right target who is really in need of help. In this sense, BOP also provides an important cognitive basis for survival and social adaption during social interactions.

Some limitations of the current work create future research opportunities. For example, a recent approach to hierarchical Bayesian models of cognition assumes that the brain represents information probabilistically and people represent a state or feature of the world not using a single computed value but a conditional probability density function (Knill and Pouget, 2004; Friston, 2005; Clark, 2013; Tappin and Gadsby, 2019). Our manipulations of BOP, however, had only two conditions (patient vs. actor/actress) and thus lack a model of effects of probability-based belief-updating on empathy and relevant altruistic behavior. Future research should examine how empathy and relevant altruistic behavior vary as a function of the degree of BOP. Other interesting research questions arising from our work include how the brain represents BOP. It has been proposed that different types of beliefs (e.g., empirical beliefs, conceptual beliefs, and relational beliefs) exist in the human mind and may have distinct neural underpinnings (Harris et al., 2009; Seitz and Angel, 2020). To address neural representations of BOP will allow researchers to further explore and construct neural models of the interaction between beliefs and empathic brain activity in the key nodes of the empathy network. Another interesting issue related to our findings is individual differences in BOP and BOP effects on empathy and altruism. Since specific degrees of beliefs differ widely across individuals (Ais et al., 2016), it is crucial to examine what personality/psychopathic traits or biological factors make individuals hold strong or weak BOP and exhibit large or small BOP effects on empathy and altruistic behavior. It is also important to clarify what environmental factors modify individuals’ default BOP and consequently change their motivations to help those who appear suffering. To clarify these issues will advance our understanding of individual and contextual factors that shape the functional role of BOP in modulations of empathy and altruistic behavior. Finally, a general issue arising from the current work is whether beliefs affect the processing of other emotions such as fear, sad, and happy, and, if yes, whether there are common underlying psychological and neural mechanisms.

Our results in Experiments 1–6 showed consistent evidence for modulations of both subjective (self-report) and objective (EEG/fMRI) measures of empathy for others’ suffering. An interesting question arising from these findings is whether the belief effects are specific to neural underpinnings of empathy for pain. We addressed this issue by examining belief effects on neural responses to other facial expressions in an additional experiment. Specifically, in this experiment, we sought to test (1) whether beliefs of authenticity of others’ happiness influence brain responses to perceived happy expressions and (2) whether beliefs also modulate neural responses to happy expressions in the P2 time window, similar to the BOP effect on ERPs to pain expressions. The paradigm used in the additional experiment was the same as that used in Experiment 3 except the following. We asked an independent sample of participants to remember identities (awardees or actors/actresses) of neutral faces. Thereafter, EEG signals to happy and neutral expressions of awardees or actors/actresses were recorded after informing the participants that photos of happy faces were taken from awardees who were smiling when receiving awards whereas actors/actresses imitated others’ smiling and showed happy expressions. We predicted that beliefs that actors/actresses’ expressions do not reflect their actual emotional states would decrease brain response to happy expressions. We tested this prediction by comparing ERPs to happy/neutral faces with awardee or actor/actress identities.

We recorded EEG signals from an independent sample of healthy young adults (N=30 males, mean age±s.d.=22.30±2.73 years). Face stimuli with happy or neutral expressions were adopted from the previous study (Wang and Han, 2021). There were photos of 16 Chinese models (half males) and each model contributed one photo with happy expression and one with neutral expression.

The participants were first presented with the faces with neutral expressions and were informed that these photos were taken from eight awardees who recently obtained awards and from eight actors/actresses. After the identity memory task, in which the participants were able to correctly recognize all faces with awardee or actor/actress identities, they were asked to perform identity judgments on faces with neutral or happy expressions by pressing one of two buttons while EEG was recorded. After EEG recording, the participants were presented with each happy face again and had to rate how happy the person is feeling (i.e., happiness intensity) by rating on a Likert-type scale (1=not happy at all, 7=extremely happy).

An ANOVA of the mean rating scores of happiness intensity with Identity (awardee vs. actor/actress) and Expression (happy vs. neutral) as within-subject variables revealed significant main effects of Identity (F(1,29)=19.512, p<0.001, η_p²=0.402, 90% CI=[0.166, 0.560]) and Expression (F(1,29)=422.774, p<0.001, η_p²=0.936, 90% CI=[0.889, 0.953]), and a significant Identity×Expression interaction (F(1,29)=6.610, p=0.016, η_p²=0.186, 90% CI=[0.021, 0.372], see Appendix 1—figure 1a, and Appendix 1—table 1 for details). The results suggest weaker subjective feelings of happiness intensity for faces with actor/actress identities compared to awardee identities.

Appendix 1—figure 1

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Appendix 1—figure 1—source data 1

Happy intensity rating scores and Mean differential P570 amplitudes.

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The participants responded to face identities with high accuracies during EEG recording (>88% across all conditions, see Appendix 1—table 1 for details). Similarly, ERPs to face stimuli in this experiment were characterized by an early negative activity at 90–120 ms (N1) and a positive activity at 175–195 ms (P2) at the frontal/central regions, which were followed by two positive activities at 280–340 ms (P310) over the parietal region and 500–700 ms (P570) over the frontal area (Appendix 1—figure 1b). ANOVAs of the P2 amplitudes with Identity (awardee vs. actor/actress) and Expression (happy vs. neutral) as within-subject variables did not reveal a significant Identity×Expression interaction (F(1,29)=0.441, p=0.512, η_p²=0.015, 90% CI=[0, 0.145], Bayes factors=0.303).

Importantly, ANOVAs of the later P570 amplitudes showed a significant Identity×Expression interaction (F(1,29)=4.832, p=0.036, η_p²=0.143, 90% CI=[0.005, 0.328], Appendix 1—figure 1b and 1c, see Appendix 1—table 1 for statistical details). Simple effect analyses indicated significantly larger P570 amplitudes in response to happy versus neutral expressions of awardees’ faces (F(1,29)=20.880, p<0.001, η_p²=0.419, 90% CI=[0.181, 0.573]), but not of actors/actresses’ faces (F(1,29)=3.375, p=0.076, η_p²=0.104, 90% CI=[0, 0.285], Bayes factor=0.858).

Our behavioral and ERP results in this experiment suggest reduced subjective feelings and brain responses to happy (vs. neutral) expressions of actors/actresses’ faces compared to awardees’ faces. These results support the prediction that beliefs that actors/actresses’ expressions do not reflect their actual emotional states decrease brain response to happy expressions. However, belief effects on brain responses to happy expressions were observed on the P570 amplitudes but not on the P2 amplitudes. This is different from our ERP results in Experiments 3–5, in which we showed evidence that BOP modulated the P2 amplitudes. These results suggest general belief modulation effects on brain activities involved in processing of facial expressions. In addition, our results suggest that the time window in which beliefs modulate brain responses to facial expressions depends on the nature of facial expressions (e.g., pain or happiness expressions).

Source data files have been provided for Figures 1-6 and Appdendix 1 Figure 1.

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Author details

1. Taoyu Wu

   School of Psychological and Cognitive Sciences, PKU-IDG/MGovern Institute for Brain Research, Beijing Key Laboratory of Behavior and Mental Health, Peking University, Beijing, China

   Contribution

   Data curation, Software, Formal analysis, Validation, Visualization, Methodology, Writing - original draft, Writing - review and editing

   Competing interests

   No competing interests declared

2. Shihui Han

   School of Psychological and Cognitive Sciences, PKU-IDG/MGovern Institute for Brain Research, Beijing Key Laboratory of Behavior and Mental Health, Peking University, Beijing, China

   Contribution

   Conceptualization, Formal analysis, Supervision, Funding acquisition, Investigation, Visualization, Methodology, Writing - original draft, Project administration, Writing - review and editing

   For correspondence

   shan@pku.edu.cn

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-3350-5104

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