Are there sex differences in ERPs related to processing empathy-evoking pictures?
Highlights
► IAPS pictures with positive human emotions elicit enhanced N1 and anterior N2. ► IAPS pictures with negative human emotions elicit enhanced LPP. ► No sex differences in ERPs to IAPS pictures with positive or negative human emotions. ► Females prioritize socially relevant and negative emotional information.
Introduction
In general, empathy has been defined as the capacity to share and understand other people’s feelings. The common view is that women are more empathic than men. Indeed, numerous studies confirmed that females compared to males have an advantage in social-cognitive and affective functions that are related to experiencing and expressing empathy. For example studies focusing on emotion recognition and expression, such as affective facial expressions, prosody in the voice, body postures and social gestures have shown a female advantage, although this depends on the type of emotion and the situation (see for a review: Kret & De Gelder, 2012; see for a meta-analysis: McClure, 2000). Concerning the experience of empathy, however, most studies on this female advantage are based on self-reports, which have been shown susceptible to normative responding reflecting a bias to confirm the sex-role stereotypes (e.g., Eisenberg and Miller, 1987, Gerdes et al., 2010, Grossman and Wood, 1993). The present study makes use of brain potentials to objectify sex differences in the experience of empathy.
Most definitions of empathy agree that the capacity to feel, understand and respond to the affective experiences of other persons depends on two components, an affective and a cognitive one (Blair, 2005, Chakrabarti and Baron Cohen, 2006, Derntl et al., 2010, Eisenberg and Miller, 1987, Gerdes et al., 2010, Lamm et al., 2007, Shamay-Tsoory et al., 2009). The affective component of empathy is the tendency to feel similar emotions when observing other persons’ emotions, implicating emotional contagion or affective sharing (Blair, 2005, Shamay-Tsoory et al., 2009, Shamay-Tsoory, 2011). The cognitive component refers to higher order cognitive functions that allow a person to adopt another’s point of view or having a theory of (the other’s) mind (Baron-Cohen, Leslie, & Frith, 1985; ToM Baron-Cohen and Wheelwright, 2004, Baron-Cohen, 2009). This comprises the understanding of the other’s thoughts, desires and beliefs. i.e., cognitive mentalizing, as well as the other’s feelings, i.e., affective mentalizing (Decety and Meyer, 2008, Shamay-Tsoory, 2011). It is important to distinguish affective mentalizing from affective empathy, with affective mentalizing meaning to have an imagination of another person’s feelings, and affective empathy meaning to feel what the other feels, i.e., emotional contagion.
Current research supports the existence of distinguishable neural systems sub-serving affective and cognitive empathy. During emotional contagion, emotion recognition and pain sharing, phylogenetically older structures are activated, which form part of the affective empathy system (de Waal, 2008, Shamay-Tsoory, 2011). The involved structures are the inferior frontal gyrus (IFG), the inferior parietal lobule (IFL), both these regions forming part of the mirror neuron system (MNS) involved in imitation and emotional contagion, as well as the anterior cingulate cortex (ACC), insula, and amygdala, the latter two being especially involved in feeling pain empathy and compassion (Decety and Michalska, 2010, Decety et al., 2010, Keysers and Gazzola, 2006, Rizzolatti et al., 2009, Shamay-Tsoory, 2011). During mentalizing, evolutionarily more recently developed structures are involved (Shamay-Tsoory, 2011). The brain regions suggested to be involved in cognitive empathy are the medial prefrontal cortex (mPFC), superior temporal sulcus (STS), the temporoparietal junction (TPJ) and the temporal poles (TP) (Carrington and Bailey, 2009, Frith and Singer, 2008, Van Overwalle and Baetens, 2009). While the affective empathy system is suggested to support early automatic, bottom-up processes of empathy, the cognitive empathy system is related to later consciously controlled evaluative processes of empathy, including affective mentalizing (Decety and Michalska, 2010, Shamay-Tsoory, 2011).
Consideration of this distinction may lead to a more complete understanding of sex differences in empathic abilities and their underlying neural mechanisms. Self-report and performance measures appear not to be sufficient; additional measures derived from neuroimaging and physiological recordings are warranted (see for a review: Gerdes et al., 2010). Yet, neuroimaging studies have only begun to unravel sex differences in brain systems supporting empathy. The few fMRI studies available on sex differences in empathic brain responses, however, primarily focused on aspects of cognitive empathy assessing identification, inference and imagination (affective mentalizing) of another person’s feeling (Derntl et al., 2010) or the evaluation of the observer’s own feeling when looking at the expression of a target face (Schulte-Rüther, Markowitsch, Shah, Fink, & Piefke, 2008). Another study required female and male participants to indicate to what extent they felt compassion when viewing pictures showing human suffering in different contexts compared to emotionally neutral pictures showing objects or landscapes and non-compassion-evoking social scenes (Mercadillo, Luis Diaz, Pasaye, & Barrios, 2011). All these studies showed that females, when observing or identifying emotions in others, show more activation in brain regions related to the cognitive as well as the affective empathy system. However, all these studies have in common that they placed a demand on the participant’s cognition, because the participant was asked to make a decision. Moreover, from the relatively slow changes in the BOLD signal of fMRI, it cannot be discerned what processes are subsequently engaged when observing emotional expressions or suffering in others.
The temporal dynamics of empathic processing have been revealed by EEG event-related potential (ERP) studies by Fan and Han (2008) and Decety, Yang, and Cheng (2010). These authors demonstrated that empathy for pain can be divided into an early automatic process of emotional sharing and a later controlled cognitive evaluation process. In the study by Fan and Han, the ERPs showed an early positive shift for painful compared to neutral stimuli at frontocentral sites (140–380 ms: including P180 and N240) that was unaffected by top-down processing (a positive shift for painful stimuli) and a long-latency empathic response (380–500 ms: P320) at posterior parietal sites that was suppressed by top-down processing, i.e., by the task demand of counting the stimuli instead of just judging them as being painful or not. The later pain effect was found to be more salient for the left hemisphere. A re-analysis on sex differences by Han, Fan, and Mao (2008) demonstrated a stronger top-down influence on only the long-latency controlled process of pain empathy (340–540 ms: P320) in females compared to males, i.e. a smaller pain effect when counting was required. Although no sex differences were found in the early automatic processing of pain stimuli (140–320 ms: P180 and N240), only the females’ mean amplitudes of the early components correlated significantly with subjective evaluations of others’ pain and self-unpleasantness.
Another ERP study conducted by Proverbio, Adorni, Zani, and Trestianu (2009) investigated sex differences in empathic brain responses during the passive viewing of both positive and negative affective pictures with and without humans selected from the International affective picture system (IAPS) (Lang, Bradley, & Cuthbert, 2005). Compared to males, an enhanced early anterior negativity (210–270 ms: anterior N2), was found in females in response to human pictures with positive emotions compared to negative emotions as well as an enhanced late positivity (500–700 ms: LPP) in response to human pictures with negative emotions compared to negative scenes without humans. The effects of positive human emotions were stronger over the left hemisphere, whereas the effects of negative human emotions were stronger over the right hemisphere supporting the hemispheric asymmetry hypothesis of emotions (Davidson, 1984). In the light of the automatic-controlled model of empathy by Fan and Han the findings of Proverbio and colleagues suggest that sex differences in affective empathy and cognitive evaluation of the emotion (affective mentalizing) are dependent on the valence of emotion.
In the present study we used EEG event-related potentials (ERPs) in combination with self-report measures of empathy to investigate sex differences regarding the temporal dynamics of brain activation during the processing of empathy-evoking pictures with humans depicting negative emotions (pain, anger, fear, suffering) as well as positive emotions (happiness, love, tenderness). To this end we adopted the paradigm of Proverbio et al. (2009) in which participants passively view human and nonhuman emotional pictures from the IAPS. The use of a passive viewing task allows for capturing the participants’ unbiased empathic brain activations, because no response or decision is required. The study design was however adjusted on several aspects: (1) An emotionally neutral condition was added, because contrasting emotional to neutral pictures allows for measuring the ‘pure’ affective response and controls for between subject (sex) differences in ERP morphology of non-emotional stimulus processing. (2) The most disgusting pictures were removed from the selection to diminish confounding feelings of disgust. (3) Self-reported empathic traits were assessed to explore relationships between the unbiased brain activations and subjectively judged empathic experiences in daily life. (4) The number of participants was more than doubled.
The main aim of the present study was to gain insight into sex differences in the temporal dynamics of early automatic emotional sharing and late controlled affective mentalizing of both negative and positive emotions in humans. To this end, we replicated the study of Proverbio et al. (2009) on sex differences in ERPs to empathy-evoking pictures with the adjusted task design. The current theories of empathy predict that early-latency ERP components reflect the experience of affective empathy without the influence of cognitive evaluation (affective empathy or emotional sharing) and that late-latency components reflect cognitive evaluation aspects of empathy (affective mentalizing). We therefore expect that early-latency empathy effects correlate with self-report measures of affective empathy, while the late-latency empathy effects correlate with self-report measures of cognitive empathy.
Section snippets
Participants
The present study included 52 participants aged 18–26 years old (M=20.7 years), of which 25 were female. The males were slightly older than the females (males: mean 21.3/SD 2.1 years; females: mean 20.1/SD 1.6 years; F(1,51)=5.1, p=.028). The original sample consisted of 70 participants, but 12 participants (4 females) had to be removed because of a technical failure of the earlobe recordings for the reference, five because of excessive EEG artifacts (2 females) and 1 female participant because
Self-reported empathy
The females in our sample scored significantly higher than males on the IRI PD scale, but not on the other scales of the IRI (see Table 2). However, when taking into account the direction of our hypothesis expecting females to be more empathic, testing one-sided revealed that females also reported significantly higher IRI fantasizing (FS) and empathic concern (EC) scores than males. Females scored significantly higher than males on the empathy quotient (EQ) (see Table 2).
P1
The P1 was larger over
Discussion
The main aim of the present study was to gain insight into sex differences in the temporal dynamics of processing empathy-evoking pictures. To this end ERPs were measured during a passive viewing task using IAPS pictures with and without humans evoking positive and negative emotions that were contrasted with pictures of neutral emotional valence. Both short-latency (N1 and anterior N2) and long-latency (LPP) ERP components appeared more sensitive to pictures with humans showing emotions
Acknowledgments
We give our special thanks to the following people who helped in collecting the data for this study: Dorien Bangma, Lotte Fidder, Sem van Heijningen, Nicky Klaassen, Annechien Prins, Mark Smellink, Nikita van der Vinne, and Marlies van der Wijk.
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2021, NeuroImageCitation Excerpt :Higher self-reported empathy has also been associated with more positive LPP amplitudes to target facial expressions amongst other expressions during an oddball task (Choi and Watanuki, 2014). Finally, LPP amplitudes were found to be more positive in response to negative human stimuli relative to negative scenes, and the magnitude of this difference was correlated with self-reported empathy (Groen et al., 2013). These findings would suggest that these ERP components reflect processes that may also be active during our affective empathy task, which is important to confirm to further develop our understanding of what processes these components reflect.