Who caused the pain? An fMRI investigation of empathy and intentionality in children

Abstract

When we attend to other people in pain, the neural circuits underpinning the processing of first-hand experience of pain are activated in the observer. This basic somatic sensorimotor resonance plays a critical role in the primitive building block of empathy and moral reasoning that relies on the sharing of others’ distress. However, the full-blown capacity of human empathy is more sophisticated than the mere simulation of the target's affective state. Indeed, empathy is about both sharing and understanding the emotional state of others in relation to oneself. In this functional magnetic resonance imaging (fMRI) study, 17 typically developing children (range 7–12 yr) were scanned while presented with short animated visual stimuli depicting painful and non-painful situations. These situations involved either a person whose pain was accidentally caused or a person whose pain was intentionally inflicted by another individual. After scanning, children rated how painful these situations appeared. Consistent with previous fMRI studies of pain empathy with adults, the perception of other people in pain in children was associated with increased hemodynamic activity in the neural circuits involved in the processing of first-hand experience of pain, including the insula, somatosensory cortex, anterior midcingulate cortex, periaqueductal gray, and supplementary motor area. Interestingly, when watching another person inflicting pain onto another, regions that are consistently engaged in representing social interaction and moral behavior (the temporo-parietal junction, the paracingulate, orbital medial frontal cortices, amygdala) were additionally recruited, and increased their connectivity with the fronto-parietal attention network. These results are important to set the standard for future studies with children who exhibit social cognitive disorders (e.g., antisocial personality disorder, conduct disorder) and are often deficient in experiencing empathy or guilt.

Introduction

Our understanding of the neural mechanisms underpinning the experience of empathy has increased significantly during the past decade. This is mainly due to the application of cognitive neuroscience and neuroimaging tools that have expanded to study interpersonal sensitivity, i.e., the ability to perceive and respond with care to the internal states (e.g., cognitive, affective, motivational) of another, understand the antecedents of those states, and predict the subsequent events that will result (Decety & Batson, 2007).

Notably, a growing number of functional neuroimaging studies have demonstrated striking similarities (as well as differences) in the neural circuits involved in the processing of both the first-hand experience of pain and the second-hand experience of observing other individuals in pain (Jackson, Rainville, & Decety, 2006 for a review). These studies have consistently shown that the perception of pain in others elicits activation of the neural circuit subserving the processing of the affective and motivational dimension of pain (Botvinick et al., 2005, Cheng et al., 2007, Gu and Han, 2007; Jackson, Meltzoff, & Decety, 2005; Jackson, Brunet, Meltzoff, & Decety, 2006; Lamm, Batson, & Decety, 2007; Moriguchi et al., 2007; Morrison, Lloyd, di Pellegrino, & Roberts, 2004; Morrison, Peelen, & Downing, 2006; Ogino et al., 2007, Saarela et al., 2007, Singer et al., 2004; Zaki, Ochsner, Hanelin, Wager, & Mackey, 2007). This neural circuit includes the dorsal anterior cingulate cortex (ACC), the anterior midcingulate cortex (aMCC) and anterior insula (Derbyshire, 2000, Price, 2000). In addition, transcranial magnetic stimulation (Avenanti, Bueti, Galati, & Aglioti, 2005), somatosensory-evoked potentials (Bufalari, Aprile, Avenanti, Di Russo, & Aglioti, 2007), magenoencephalography (Cheng, Yang, Lin, Lee, & Decety, 2008), and functional magnetic resonance imaging (fMRI) studies (Benuzzi, Lui, Duzzi, Nichelli, & Porro, 2008; Cheng et al., 2007, Lamm et al., 2007b; Moriguchi et al., 2007) have also demonstrated that areas processing the sensory dimension of pain (somatosensory cortices/posterior insula) may also be elicited by the mere visual perception of pain in others.

Altogether, there is strong evidence to suggest that perceiving the pain of others triggers an automatic somatic sensorimotor-mirroring mechanism between other and self, which activates almost the entire neural pain matrix including the periaqueductal gray (PAG), a major site in pain transmission and for processing of fear and anxiety, the supplementary motor area (SMA) that programs defensive movements in the context of nociceptive information, and thalamus. Such a resonance mechanism provides a functional bridge between first-person information and third-person information, grounded in self–other equivalence, which allows for analogical reasoning, and offers a possible, yet partial, route to understanding others (Decety & Sommerville, 2003; Decety & Grèzes, 2006; Gallese, 2001). In the case of pain, individuals are predisposed to find distress of others aversive and learn to avoid actions associated with this distress. This is even the case in many mammalian species including rodents. For instance, rats that had learned to press a lever to obtain food would stop doing so if their response was paired with the delivery of an electric shock to a visible neighboring rat (Church, 1959). This example illustrates the functional connection between the first-hand experience of pain, its perception in others, and empathic concern, which draws on the encephalization of pain evaluation (Tucker, Luu, & Derryberry, 2005).

However, the full-blown capacity of human empathy is more sophisticated than the mere automatic resonance of the target's affective state. Indeed, empathy is both about sharing the emotional state of others and understanding it in relation to oneself (Decety & Moriguchi, 2007; Eisenberg, Spinrad, & Sadovsky, 2006). The capacity for two people to resonate with each other emotionally, prior to any cognitive understanding, is the basis for developing shared emotional meanings, but is not enough for empathic understanding. Such an understanding goes beyond this reflex-like response. Indeed, although affective resonance contributes to empathy, it is not sufficient for grasping another's distinct emotional perspective. This requires forming an explicit representation of the feelings of another person, an intentional agent, which necessitates additional computational mechanisms beyond the shared representation level, as well as self-regulation to modulate negative arousal in the observer (Decety & Jackson, 2004). In order to understand the emotions and feelings of others in relation to oneself, second-order representations of the other need to be available to awareness (a decoupling computational mechanism between first-person information and second-person information: theory of mind), for which the medial prefrontal cortex, especially the paracingulate cortex (PCC) and the temporo-parietal junction (TPJ) play a special role (Decety & Jackson, 2004; Frith & Frith, 2003; Saxe & Kanwisher, 2003). The importance of the medial prefrontal cortex in self-awareness and self-conscious emotions is also supported by studies with neurological patients suffering from fronto-temporal lobar degeneration. For instance, Sturm, Rosen, Allison, Miller, and Levenson (2006) found preserved peripheral physiological response and negative emotional reactivity, but diminished self-conscious emotional behavior such as empathic concern.

To our knowledge there is no functional MRI study that has investigated the neural underpinnings in empathy for pain and theory of mind in school-aged children. We believe that such investigations are critical to set the standard for future studies with children who exhibit social cognitive disorders (e.g., antisocial personality disorder, conduct disorder) and are often deficient in experiencing empathy or guilt. Given the age of the children included in our experiment, we posited that the different components of empathy (i.e., emotion sharing, self–other distinction, self-regulation) are already in place. This reasoning is based on behavioral and physiological studies by developmental psychologists (e.g., Eisenberg & Eggum, in press; Eisenberg & Miller, 1987; Zahn-Waxler & Radke-Yarrow, 1990) that have documented that by the age of 4–5 yr, typically developing children exhibit mature empathic ability and prosocial behaviors (see Decety & Jackson, 2004; Decety & Meyer, 2008 for reviews). By the same age, children are equipped with cognitive mechanisms that subserve theory of mind capabilities (Baron-Cohen, Tager-Flusberg, & Cohen, 2000). In support of this view, one functional MRI study with children of a similar age (mean age 10 yr, range 7–13) as our participants, found the same neural network activated by a theory of mind task as in adult participants, including the medial prefrontal cortex and right TPJ (Ohnishi et al., 2004).

The goals of our study were twofold: (1) to map the brain response in typically developing children associated with the perception of pain in others; (2) to examine the respective contribution of mechanisms that contribute to theory of mind and implicit moral reasoning in the context of pain perception. In this experiment, children in middle childhood were shown dynamic visual animations depicting body parts in painful situations. These situations involved one person whose pain was either ostensibly caused by accident or inflicted by another individual. It was predicted that when children watched the painful situations involving one person, the neural circuits engaged in pain processing (e.g., the aMCC, insula, SMA, somatosensory cortex, PAG) would be activated. When the situations involved another individual inflicting pain on another, we hypothesized that, in addition to areas that belong to the pain matrix, significant signal increase would be detected in the neural regions associated with mentalizing and self-regulation such as the PCC, the TPJ and the orbital medial frontal cortex (oMFC). The PCC and oMFC have been implicated in social behavior, such as making inferences about others’ thoughts and the monitoring of outcomes that relate to punishments and rewards (Amodio & Frith, 2006; Anderson, Bechara, Damasio, Tranel, & Damasio, 1999), which are critical processes in moral reasoning. Individuals with damage to the orbital medial prefrontal cortex show little control over their emotions as well as limited awareness of the moral implications of their actions (Damasio, 1994, Grafman et al., 1996). Further, it is possible that perceiving another individual intentionally inflicting pain upon another person recruits the amygdala, which plays a critical role in fear-related behaviors, such as the evaluation of actual or potential threats (e.g., LeDoux, 2000, Phelps et al., 2001). It is generally acknowledged that the amygdala is necessary for normal processing of negative emotional stimuli, and its damage most often leads to impairments in recognizing threat and/or arousal-related information from visual stimuli (Adolphs, 2002). Of particular interest, individuals who lack empathy, such as in psychopathy, exhibit dysfunction in a circuit that includes the amygdala and oMFC (Blair, 1995, Kiehl, 2006). This anomaly precludes learning the basics of care-based morality, that is, learning that some actions harm others and because of this are to be avoided (Blair, 2007). The amygdala and oMFC are both anatomically and functionally connected (Amaral & Price, 1984) and their effective interactions are critical for decoding emotionally salient information and guiding social behavior (Saddoris, Gallagher, & Schoenbaum, 2005).