The Neural Networks Underlying Reappraisal of Empathy for Pain

Navot Naor; Christiane Rohr; Lina H Schaare; Chirag Limbachia; Simone Shamay-Tsoory; Hadas Okon-Singer

Disclosures

Soc Cogn Affect Neurosci. 2020;15(7):733-744. 

In This Article

Abstract and Introduction

Abstract

Emotion regulation plays a central role in empathy. Only by successfully regulating our own emotions can we reliably use them in order to interpret the content and valence of others' emotions correctly. In an functional magnetic resonance imaging (fMRI)-based experiment, we show that regulating one's emotion via reappraisal modulated biased emotional intensity ratings following an empathy for pain manipulation. Task-based analysis revealed increased activity in the right inferior frontal gyrus (IFG) when painful emotions were regulated using reappraisal, whereas empathic feelings that were not regulated resulted in increased activity bilaterally in the precuneus, supramarginal gyrus and middle frontal gyrus (MFG), as well as the right parahippocampal gyrus. Functional connectivity analysis indicated that the right IFG plays a role in the regulation of empathy for pain, through its connections with regions in the empathy for pain network. Furthermore, these connections were further modulated as a function of the type of regulation used: in sum, our results suggest that accurate empathic judgment (i.e. empathy that is unbiased) relies on a complex interaction between neural regions involved in emotion regulation and regions associated with empathy for pain. Thus, demonstrating the importance of emotion regulation in the formulation of complex social systems and sheds light on the intricate network implicated in this complex process.

Introduction

Our emotions can help us respond effectively and adaptively to the complex world that surrounds us. They can also, however, become destructive and unhelpful, making us more confused rather than providing us more clarity (Gross, 2013). For this reason, being able to regulate our emotions by amplifying those that encourage adaptive responses and diminishing those that do not is central to our wellbeing. A common strategy that individuals use to regulate their emotions is cognitive reappraisal—a process through which individuals reconstruct an emotional situation in a way that alters its emotional impact, for example by reconstructing a horror film as a parody (McRae et al., 2012).

Traditionally, the study of emotion regulation focused on intrinsic and basic emotions (e.g. fear, anger or disgust; Gross, 2013). Recently, however, growing research interest is being directed toward more complex emotional situations provoked during interpersonal interactions. One such complex emotional situation is the experience of empathy, which is the focus of this paper. Empathy is generally defined as an individual's ability to vicariously experience the thoughts and feelings of another person, thus generating connections between individuals. As part of the empathic process, individuals use their own emotions and experiences as a reference point for understanding the mental states of others. Thus, it follows that empathy is influenced by the control individuals exert over their own emotional experiences (Decety, 2010, Naor et al. 2018).

The tendency to use one's own emotions while at the same time regulating them is even more relevant in the context of empathy for pain, i.e. the ability to partake of the pain felt by others (Fitzgibbon et al., 2010). Empathy for pain has been the major focus of empathy research in social neuroscience and other related fields (Singer and Lamm, 2009), highlighting the importance of empathy for pain in daily life. For example, we recently demonstrated that the use of reappraisal to regulate emotions can influence the empathic process and eliminate biases in judging emotional facial intensity (Naor et al. 2018). The ability to accurately judge the intensity of emotional facial expressions can be considered to be one type of empathic accuracy (Ickes et al., 1990). The ability to identify others' emotions based on the observation of facial expressions has been linked to the ability to share such feelings (Enticott et al., 2008), a key concept in empathy (Blais et al., 2012; Singer, 2006). Judgment of morphed faces has been used as a measure of empathic accuracy in previous works, for example in studies that showed participants dynamic facial expressions and asked them to continuously judge the intensity of the emotional expressions (e.g. Hall and Schmid Mast, 2007; Zaki et al., 2008, 2009). Furthermore, reduction in the ability to make accurate emotional intensity inferences from morphed static face images has been associated with conditions marked by impairments in empathy, such as cocaine users (Kuypers et al., 2015), patients with ventromedical prefrontal cortex lesions (Jenkins et al., 2014) and individuals with autistic spectrum disorder (Smith et al., 2010). A recent study demonstrated a cognitive bias for judgments of pain only when these judgments were made after the participant experienced empathy for pain, yielding exaggerated assessment of emotional intensity compared to the presented intensity. Nevertheless, that bias disappeared when participants used reappraisal to regulate their empathy (Naor et al. 2018).

The neural networks underlying the process of modulating empathy for pain in the context of emotion regulation have yet to be explored. Empathy relies heavily on areas of the salience network, namely the anterior insula (AI) and the anterior cingulate cortex (ACC) (Menon and Uddin 2010; Seeley et al., 2007). Conversely, emotion regulation, and mainly reappraisal-based downward regulation, is associated with executive control and limbic networks, namely the prefrontal cortex and the amygdala (Seeley et al., 2007, Menon and Uddin 2010). An accumulating body of research highlights the utility of examining functional connectivity when assessing the relationships between cognitive and affective processes, as well as their corresponding brain processes.

Hence, the current study aimed at exploring the functional connectivity among the neural networks involved both in upregulating and in downregulating empathy for pain. To this end, we employed the task developed by Naor et al. (2018) in an functional magnetic resonance imaging (fMRI) setting. In short, participants observed scenarios of painful or non-painful situations. They were then asked to rate the degree of affect in faces that depicted either a painful or a happy expression. In half of the trials, participants were asked to empathize with the scenario, while in the other half they were asked to reappraise their empathy. Empathic engagement with the painful scenario is hypothesized to lead to empathy, which will affect the participants' emotional state and lead them to judge other people's levels of pain inaccurately but will not affect the accuracy of their valence judgment of other emotions. Conversely, the use of reappraisal will downregulate the participant's own emotional state, resulting in more accurate empathic judgment.

In addition, we hypothesized that (i) the experience of empathy for pain would result in increased activity in the salience network, mainly the AI and the ACC; (ii) downregulation of empathy for pain via reappraisal would result in increased activity in regions associated with executive control and decreased activity in limbic networks; and (iii) the degree of activity in the prefrontal-limbic network would affect the degree of cognitive bias, such that the greater the functional connectivity between regions related to emotion regulation and those related to empathy, the lesser the bias would be. To this end, in addition to a GLM-based fMRI data analysis, we also conducted a generalized psychophysiological interaction (gPPI) analysis to explore the functional networks underlying the differences between bias scores after observation of painful scenarios under reappraise and watch conditions. This analysis enabled us to pinpoint the brain regions that exhibit higher functional coupling during the process of downward regulation of empathy.

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