Elsevier

NeuroImage

Volume 40, Issue 3, 15 April 2008, Pages 1419-1428
NeuroImage

Seeing the pain of others while being in pain: A laser-evoked potentials study

https://doi.org/10.1016/j.neuroimage.2007.12.056Get rights and content

Abstract

Seeing actions, emotions and feelings of other individuals may activate resonant mechanisms that allow the empathic understanding of others’ states. Being crucial for implementing pro-social behaviors, empathy is considered as inherently altruistic. Here we explored whether the personal experience of pain make individuals less inclined to share others’ pain. We used laser-evoked potentials (LEPs) to explore whether observation of painful or non-noxious stimuli delivered to a stranger model induced any modulation in the pain system of onlookers who were suffering from pain induced by the laser stimuli. After LEPs recording, participants rated intensity and unpleasantness of the laser pain, and of the pain induced by the movie in themselves and in the model. Mere observation of needles penetrating the model’s hand brought about a specific reduction of the N1/P1 LEP component, related to the activation of somatic nodes of the pain matrix. Such reduction is stronger in onlookers who rated the pain intensity induced by the pain movie as higher in themselves and lower in the model. Conversely, the N2a-P2 component, supposedly associated to affective pain qualities, did not show any specific modulation during observation of others’ pain. Thus, viewing ‘flesh and bone’ pain in others specifically modulates neural activity in the pain matrix sensory node. Moreover, this socially-derived inhibitory effect is correlated with the intensity of the pain attributed to self rather than to others suggesting that being in pain may bias the empathic relation with stranger models towards self-centred instead than other-related stances.

Introduction

Empathy refers to the ability to understand the subjective experience of other individuals by vicariously sharing their desires, beliefs, emotions and feelings. The intrinsically altruistic nature of empathy is suggested by social psychology studies indicating that empathic individuals tend to help people in need even when lending a hand implies specific risks of psychological distress or physical danger (Batson, 1991). However, higher order emotional variables, such us for example the type of social bond between individuals, may modulate empathic behavioral and neural reactions in less altruistic directions. Relevant to this issue is an fMRI study demonstrating that empathic responses to the pain of others’ are dramatically lower for unfair than fair individuals (Singer et al., 2006). Learning about the conditions that allow humans to empathize with others may help understand social and clinical conditions characterized by a lack or an excess of empathy. For example, it has been suggested that pain-induced distress may be prohibitive of empathy (Preston and de Waal, 2002); yet, it is still largely unknown whether and at which neural level suffering from physical pain modulates the way we perceive and understand others’ pain.

Recent fMRI (Morrison et al., 2004, Singer et al., 2004, Botvinick et al., 2005, Jackson et al., 2005, Jackson et al., 2006, Saarela et al., 2007) and neurophysiological studies (Avenanti et al., 2005, Avenanti et al., 2006, Bufalari et al., 2007) explored the mechanisms and the neural underpinnings of empathy for pain in humans. Most of the above fMRI studies reported changes in the neural activity of the anterior cingulate cortex (ACC) and the anterior insula (AI) when subjects observed pictures of painful stimuli delivered to other individuals (Morrison et al., 2004, Morrison et al., 2007, Jackson et al., 2005, Jackson et al., 2006) or imagined their partners feeling pain (Singer et al., 2004). Thus, most of the fMRI studies converge to indicate that mainly the affective nodes of the pain matrix are called into play during empathy for pain. However, single pulse Transcranial Magnetic Stimulation (TMS) (Avenanti et al., 2005, Avenanti et al., 2006) and Somatosensory Evoked Potentials (SEPs) (Bufalari et al., 2007) studies found that the neurophysiological modulations contingent upon observation of “flesh and bone” painful stimuli delivered to a stranger model triggers an automatic mapping of the noxious stimulus onto the observer’s body, a phenomenon we called sensorimotor contagion. Interestingly, this effect was correlated with the observer’s subjective empathetic rating of the sensory qualities of the pain supposedly felt by the model but not with self-centered state-or trait-empathy measures.

Here we sought to add a new dimension to current knowledge by exploring whether an observer suffering from physical pain is still prone to the basic form of empathy for the pain of strangers called sensorimotor contagion. To this aim, we used the emergent, high-temporal resolution, neurophysiological technique of CO2 laser-evoked potentials (LEPs), which offers the unique opportunity to induce acute pain on the body part stimulated by the laser beam and at the same time to explore non-invasively and specifically neural activity in sensory (secondary somatosensory area, SII) and emotional (cingulate cortex) nodes of the pain matrix (Bromm and Lorenz, 1998).

Section snippets

Subjects

Twelve right-handed, healthy subjects (5 women), mean age (±SD) = 25.75 (± 5.53) years, range 22–41, participated in the study. Participants gave their written informed consent and were naive as to the purposes of the experiment. The procedures were approved by the local ethics committee and were in accordance with the standards of the 1964 Declaration of Helsinki.

LEP recording

Cortical potentials were evoked by means of a CO2 laser stimulation device (El.En., Florence, Italy). 32 recording electrodes were

Electrophysiological data

Inspection of Fig. 1 shows that the amplitude of the N1/P1 component evoked by laser stimuli delivered to the observer’s right hand is specifically reduced during viewing of needles penetrating the model’s right hand. Amplitude modulations of the N2a-P2 component are also visible during pain observation. However, these modulations seem comparable in the different observational conditions.

The ANOVA performed on normalized N1/P1 amplitudes showed a significant main effect of Condition (F(4,44) = 

Discussion

Empathy allows us to share and comprehend the feelings and the intentions of other individuals and it is thus fundamental for social interactions and for shaping pro-social behaviour (Eisenberg, 2007). Far from being an all-or-nothing phenomenon, empathy is quite a multifarious construct ranging from low-level mechanisms such as emotional contagion to higher order processes such as perspective taking and mentalizing (Preston and de Waal, 2002, Decety and Lamm, 2006, Lamm et al., 2007). Empathy

Conclusion

In summary, we have demonstrated that viewing “flesh and bone” painful stimuli delivered to a stranger model modulates the pain system of onlookers suffering from acute pain induced by the laser stimuli. The modulation consisted of the inhibition of the N1/P1 LEP component that originates in the SII area and likely reflects the sensory qualities of pain. Previous studies of empathy for pain show that neural modulations are linked to sensory or affective pain qualities attributed to the model (

Acknowledgments

This work was supported by grants from the Ministero Istruzione Università (PRIN) , Università di Roma “La Sapienza” and Fondazione Santa Lucia (Italy) awarded to Salvatore M. Aglioti. Domenico Restuccia is now at IRCCS “E. Medea”, Regional Scientific Research Center, San Vito al Tagliamento and Pasian di Prato, I-37078, Udine, Italy. Alessio Avenanti is now at Department of Psychology, University of Bologna “Alma Mater Studiorum”, Bologna and Centro studi e ricerche in Neuroscienze Cognitive,

References (59)

  • IannettiG.D. et al.

    Operculoinsular cortex encodes pain intensity at the earliest stages of cortical processing as indicated by amplitude of laser-evoked potentials in humans

    Neuroscience

    (2005)
  • HaukO. et al.

    Somatotopic representation of action words in human motor and premotor cortex

    Neuron

    (2004)
  • JacksonP.L. et al.

    How do we perceive the pain of others? A window into the neural processes involved in empathy

    NeuroImage

    (2005)
  • JacksonP.L. et al.

    Empathy examined through the neural mechanisms involved in imaging how I feel versus how you feel pain

    Neuropsychologia

    (2006)
  • KeysersC. et al.

    A touching sight: SII/Pv activation during the observation and the experience of touch

    Neuron

    (2004)
  • KundeV. et al.

    Topography of middle-latency somatosensory evoked potentials following painful laser stimuli and non-painful electrical stimuli

    Electroencephalogr. Clin. Neurophysiol.

    (1993)
  • LegrainV. et al.

    Involuntary orientation of attention to unattended deviant nociceptive stimuli is modulated by concomitant visual task difficulty. Evidence from laser evoked potentials

    Clin. Neurophysiol.

    (2005)
  • LorenzJ. et al.

    Contribution of attentional and cognitive factors to laser evoked brain potentials

    Neurophysiol. Clin.

    (2003)
  • PerrinF. et al.

    Mapping of scalp potentials by surface spline interpolation

    Electroencephalogr. Clin. Neurophysiol.

    (1987)
  • PeyronR. et al.

    Functional imaging of brain responses to pain

    A review and meta-analysis. Neurophysiol. Clin.

    (2000)
  • PeyronR. et al.

    Role of the operculoinsular cortices in human pain processing: converging evidence from PET, fMRI, dipole modeling, and intracerebral recordings of laser evoked potentials

    NeuroImage

    (2002)
  • ValerianiM. et al.

    Scalp topography and dipolar source modelling of potentials evoked by CO2 laser stimulation of the hand

    Electroencephalogr. Clin. Neurophysiol.

    (1996)
  • ValerianiM. et al.

    Reduced habituation to experimental pain in migrain patients: a CO2 laser evoked potential study

    Pain

    (2003)
  • ValerianiM. et al.

    Short-term plastic changes of the human nociceptive system following acute pain induced by capsaicin

    Clin. Neurophysiol.

    (2003)
  • ValerianiM. et al.

    Segmental inhibition of cutaneous heat sensation and of laser-evoked potentials by experimental muscle pain

    Neuroscience

    (2005)
  • AvenantiA. et al.

    Transcranial magnetic stimulation highlights the sensorimotor side of empathy for pain

    Nat. Neurosci.

    (2005)
  • BatsonC.D.

    The altruism question: Toward a social-psychological answer

    (1991)
  • BlakemoreS.J. et al.

    Somatosensory activations during the observation of touch and a case of vision-touch synaesthesia

    Brain

    (2005)
  • BoninoS. et al.

    Empatia I processi di condivisione delle emozioni

    (1998)
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