New Voices: I feel your pain!

The ability to function successfully within a social environment is crucial to human survival. Pivotal to effective social interaction is the ability to empathise with others (Gallese, 2003). Empathy is commonly defined as the ability to share the emotion of another individual: for example, their pain. For the majority of us, the expression 'feeling someone else's pain' is simply a way of communicating that we sympathise  with them. However, there are some individuals who, either by observingor simply imagining, genuinely feel the physical pain of others. This phenomenon is known as 'synaesthesia for pain' which, until recently, had typically been reported in amputees with phantom pain (Fitzgibbon et al., 2011). So what are the neural mechanisms that underlie our human ability to understand the emotions and, in particular, pain of others?

Being able to interpret emotional facial expressions correctly is crucial to our everyday social functioning (Ekman, 1999). Recent neuroimaging studies are increasing our understanding of which neural systems are activated in individuals observing facial expressions of pain in another. Using functional magnetic resonance imaging (fMRI), Botvinick et al. (2005) explored the neural response while participants watched short video clips depicting facial expressions of either moderate pain or no pain. They found that simply viewing the facial expressions of pain engaged cortical areas, including the anterior cingulate cortex (ACC) and insula, which are involved in the direct experience of pain. 

Recently, Osborn and Derbyshire (2010) demonstrated that a significant minority of normal participants share not only the emotional component of pain in another individual, but the sensory component as well. They presented 108 participants with a sequence of images or short clips of injuries (for example,  a soccer player breaking his leg). After viewing each image participants reported if they felt any sensation of pain while viewing the image. Thirty-one of the participants reported an actual noxious somatic experience (such as a stabbing, shooting or tingling sensation) in response to one or more of the images or movie clips. All 31 responders experienced their pain in the same area of the body as the observed injury. Ten of these pain responders were then selected and matched with 10 non-responders to take part in an fMRI study where they were scanned while observing static images of injuries and emotional pictures that do not contain injuries. The responders activated emotional and sensory brain regions associated with pain, while the non-responders showed no such significant activation of these brain regions. However, there was no relationship between the level of pain intensity experienced and the level of empathy. This lack of connection could also suggest that some people feel pain for personal rather than empathetic reasons. An empathetic experience is described as one in which you share an emotion with another individual. However, this experience may be different from a shared pain experience. Indeed, Osborn and Derbyshire (2010) found that activation in regions associated with the emotional component of pain were activated more strongly and consistently than regions associated with the sensory component.

Using functional imaging, Singer and colleagues (2004) investigated pain-related empathy in 16 couples (assuming that the partners feel empathy for each other!) by assessing brain activity in the female partner while painful stimulation was applied to her or to her partner's right hand through an electrode attached to the back of the hand. Consistent with Osborn and Derbyshire (2010), they found that rostral ACC and anterior insula (AI) appear to reflect the emotional experience that evokes our reactions to pain. Activity in the posterior insula/secondary somatosensory cortex, the sensorimotor cortex and the caudal ACC was related to directly experiencing pain. Thus, a neural response in AI and rostral ACC, activated in common for 'self' and 'other' conditions, suggests that the neural substrate for empathic experience does not involve the whole of the brain region involved in the processing of self-pain (the 'pain matrix').

This discrepancy can perhaps be explained from a functional and evolutionary perspective. The nature of a noxious stimulus (such as its intensity and location) is functionally relevant when it pertains to our bodies' ability to take decisive action to remove ourselves from the noxious stimulus. On the other hand, the ability to understand someone else's emotional reaction to pain does not require such a detailed sensory discriminative representation of the noxious stimulus. Instead, all that is needed is an understanding of its relevance to the unpleasantness that the other person feels.

So it appears that imagining oneself and observing others in painful situations both produce activation of the pain-related neural network. However, as we have seen, empathy does not involve a complete self/other merging – only that part of the pain network associated with its affective qualities, but not its sensory qualities, mediates empathy. This is further supported by the findings of Jackson et al. (2006) using fMRI. Here participants were presented with pictures of people with their hands or feet in painful or non-painful situations and were instructed to imagine and rate the level of pain perceived from different perspectives. Three different perspectives were used: the subject's own perspective (Self), the perspective of a specific but unfamiliar person (Other), and from the perspective of a plastic limb (Artificial). Under each picture scenario a visual analogue rating scale was presented which ranged from 'No Pain' to 'Worst Possible Pain' and participants were instructed to rate the level of pain according to the perspective that they were requested to imagine. All situations were familiar events that can happen in everyday life (e.g. pinching one's finger in a door, or catching one's toe under a heavy object). Findings revealed that both the self's and the other's perspectives were associated with activation in the neural regions involved in pain processing, including the parietal operculum, anterior cingulate cortex and anterior insula. However, the self-perspective resulted in higher pain ratings and recruited more extensively (within the pain matrix) the secondary somatosensory cortex, the ACC and the insula proper. This distinctiveness between the self and other perspectives may be what enables us to distinguish empathic responses to others from our own personal distress.

So far the evidence seems to suggest that empathy may be derived from the ability to simulate the feelings of another individual. Neurobiological models of this simulation hold that observing another person's state activates overlapping cortical areas, 'mirror systems', as if the observer was in that same state themselves (Decety & Jackson, 2004; Gallese, 2003; Rizzolatti et al., 2002). Evidence indicating that empathy for pain may be mediated by mirror systems emerged with the finding that neurons in the ACC fire in response to both pain in the self as well as the observation of pain in others (Hutchison et al., 1999), supporting the studies discussed so far.

Shared sensations of pain are perhaps at their most intriguing and bizarre in synaesthesia for pain. This is distinct from reports where pain is the synaesthetic 'inducer,' such as the artist described by Ward (2008), who experienced colour, taste and smell in association with toothache. In synaesthesia for pain, the 'inducer' is observation of pain in another that subsequently results in the experience of synaesthetic pain.

Anecdotal evidence of synaesthesia for pain has typically been found in individuals who have acquired the sensation after losing a limb. Giummarra and Bradshaw (2009) describe the case of amputee RB. When his father had a quadruple bypass, RB saw the sutured wounds on his father's chest and suddenly experienced strong, painful 'electric' impulses in his phantom foot. The phantom pain was so intense that he had to look away from his father's chest for relief. Although unusual, this experience is by no means unique amongst amputees. Fitzgibbon, Enticott and colleagues (2010) got 74 self-referring amputees to answer questions on synaesthesia for pain within a broader survey of phantom pain, and 16.2 per cent reported that observing or imagining pain in others triggered their phantom pain.

Research suggests that amputees who experience synaesthesia for pain process pain observed in another person differently. Three groups of participants (amputees who experience phantom and synaesthetic pain, amputees who experience phantom pain but not synaesthetic pain and healthy controls) underwent electroencephalography (EEG) as they were presented with still images of hands and feet in potentially painful and non-painful situations (Fitzgibbon et al., 2011).

Interestingly, pain synaesthetes had a reduced ERP amplitude and theta band power, which may reflect a defensive strategy, inhibiting the processing of observed pain. Reduced alpha band power was also found, which may suggest a disinhibition in control processes resulting in synaesthetic pain.

Alternatively, synaesthesia for pain may be the consequence of painful or traumatic experiences resulting in disinhibition in the mirror system, which may underlie our ability to have empathy for others in pain. This dysfunctional mirror system may alter empathic processes by causing the mapping of motor/emotion/perceptual states in such a way that 'exceeds the threshold for conscious experience of those states' (Fitzgibbon, Giummarra et al., 2010). This is supported by Giummarra and Bradshaw (2007), who report a case of mirror pain following a very traumatic childbirth. Their case, CB, reports that when she is told of another individual's traumatic experience, she herself experiences shooting pains from the groin that radiate down her legs.

In sum, synaethesia for pain could be viewed as an abnormal form of empathy. Increasing our understanding of this intriguing disorder may provide us with a useful insight into abnormal empathic functions in clinical populations, and enable the design and implementation of appropriate therapeutic interventions (Fitzgibbon, Giummarra et al., 2010).

Dr Clare Allely is a Research Assistant at the University of Glasgow
[email protected]

References
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