The study of empathy

In the past few years, the study of the social and emotional brain has captured the interest of many researchers from a diverse range of disciplines. A new interdisciplinary field, social cognitive neuroscience, has emerged. There have been several special issues of science devoted to this topic and a number of review articles (e.g. Adolphs 2003, Ochsner & Lieberman 2001, Frith & Wolpert 2004).

The study of empathy has become the focus of recent investigation in social neuroscience and can be contrasted with research on a related topic, Theory of Mind (ToM). In contrast to ToM, which refers to the process of attributing propo-sitional attitudes to another person (e.g. desires, beliefs and intentions), the ability to empathize refers to the process which allows us to experience what it feels like for another person to experience a certain emotion or sensation (e.g. qualia). The capacity to understand another person's emotions by sharing their affective states, such as sharing the grief of a close friend, is fundamentally different in nature from the capacity to understand their thoughts and intentions, the latter lacking a bodily sensation.

How can we understand what someone else feels when he or she experiences emotions or bodily sensations such as pain, touch or tickling, in the absence of any emotional or sensory stimulation to our own body? Influenced by perception—action models of motor behaviour and imitation (Prinz 1998), Preston & de Waal (2002) proposed a neuroscientific model of empathy, suggesting that observation or imagination of another person in a particular emotional state automatically activates a representation of that state in the observer with its associated autonomic and somatic responses. The term 'automatic' in this case refers to a process that does not require conscious and effortful processing but which can nevertheless be inhibited or controlled.

In the last three years, several imaging studies have revealed brain networks associated with different empathic responses in the domain of touch, smell and pain (Blakemore et al 2005, Jackson et al 2005, Keysers et al 2004, Morrison et al 2004, Singer et al 2004b, 2006, Wicker et al 2003). Wicker et al (2003) showed activity in the anterior insula (AI) and anterior cingulate cortex (ACC) both when experiencing disgust, and to the observation of another's disgusted facial expression. Accordingly, lesions of the insula result in impairment in experiencing disgust in the self, and in the recognition of disgust in others. (Calder 2000, Adolphs et al 2003). Similarly, two studies indicate the recruitment of somato-sensory areas when volunteers were touched on different parts of their body, and when they watched someone else being touched in a video (Blakemore et al 2005, Keysers et al 2004).

Singer et al (2004b, 2006) expanded these approaches by measuring empathy for pain in vivo and identified both shared and unique networks involved in the vicarious experience of pain. To measure empathic responses in vivo she brought couples into the same scanner environment and compared the brain activity of the female partner while receiving painful stimulation of her own hand or watching cues indicating that her husband sitting next to the scanner was receiving painful stimulation. The results suggest that parts, but not the whole, of the 'pain matrix' were activated when empathizing with the pain of others. Activity in the primary and secondary somatosensory cortex/posterior insula contralateral to the stimulated hand was only observed when receiving pain (but see Avenanti et al 2005 and discussion of Singer & Frith 2005). In contrast, bilateral AI, the rostral ACC, brainstem, and cerebellum were activated when volunteers either received pain or a signal that a loved one was experiencing pain. These areas have been shown to be involved in the processing of the affective component of pain, that is, how unpleasant the pain feels. Interestingly, individual differences in empathy revealed by a standard empathy questionnaire were highly correlated with activity in these empathy-related areas. In summary, both the experience of pain to oneself and the knowledge that a loved-one is experiencing pain activates the same affective pain circuits. This suggests that we use representations of our own emotional response to pain in order to understand how the other feels when in pain.

The results of three recent independent studies indicate that empathie responses extend to unfamiliar people and that they are modulated by the affective link between people. Activity in ACC and AI has been also observed when volunteers watched still pictures depicting only body parts in painful situations (Jackson et al 2005) or videos showing a needle pricking the back of a hand (Morrison et al 2004). The findings of a recent study by Singer et al (2006) indicate that the magnitude of empathic responses in ACC and AI is modulated by the degree of familiarity between two persons and by whether the 'object of empathy' is liked or disliked. In this study actors pretended to be naïve volunteers participating with a real volunteer in two independent experiments; one on 'social exchange', the other on 'processing of pain'. In the first experiment, the two confederates repeatedly played a sequential Prisoner's Dilemma Game in the position of the second mover with the volunteer. One actor played fairly; they reciprocated cooperative moves by the volunteer with cooperative moves of their own; the other actor played unfairly and defected in response to cooperative moves by the volunteer. Post-experimental questionnaires showed that volunteers rated the fair actor to be a person they liked and found attractive and agreeable whereas the unfair actor was rated as unpleasant, dislike-able and unattractive. Moreover, most of the men (but not the women) indicated that they were angry with the unfair player, and they expressed the view that unfair player deserved to receive pain. These results are consistent with findings of a previous imaging study which revealed emotion-related brain activation in responses to faces of people who had previously cooperated or defected (Singer et al 2004a).

In the second part of the experiment, all three players participated in a pain study that expanded on the approach by Singer et al (2004b). One actor sat on each side of the scanner, enabling the scanned volunteer to observe coloured cues indicating high or low pain stimulation to their hand or to those of the fair or unfair players. Both men and women showed increased activation in ACC and AI when observing the unfamiliar but likeable person receiving painful stimulation. Interestingly, however, men but not women showed reduced activation in ACC and AI when they were informed that the player who previously played unfairly in the Prisoner's Dilemma game received painful shocks. Instead of empathy-related activity, men showed enhanced activity in the nucleus accumbens, an area known to play a key role in reward processing (e.g. O'Doherty 2004, Schultz 2000). Moreover, the magnitude of this reward-related activity increased with the strength of the subjectively expressed desire for revenge as elicited in post-scan questionnaires. These results suggest that both women and men show empathic responses towards unfamiliar people who had previously acted fairly, while men inhibit their empathic response towards an unfair player who they dislike. In fact, men seem to have engaged in reward-related processing—as indicated by the activation of the nucleus accumbens—when the unfair player received pain. This finding is in agreement with the results of a recent imaging study that reports similar reward-related activity when players could punish defectors in a sequential Prisoner's Dilemma game by delivering punishment points at personal costs (DeQuervain et al 2004). Further experiments are necessary to confirm the gender specificity of this effect; however, it could explain a predominant role of males in the maintenance of justice and punishment of norm violation in human societies.

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