Elsevier

NeuroImage

Volume 50, Issue 4, 1 May 2010, Pages 1676-1682
NeuroImage

Physicians down-regulate their pain empathy response: An event-related brain potential study

https://doi.org/10.1016/j.neuroimage.2010.01.025Get rights and content

Abstract

Watching or imagining other people experiencing pain activates the central nervous system's pain matrix in the observer. Without emotion regulation skills, repeated exposure to the suffering of others in healthcare professionals may be associated with the adverse consequences of personal distress, burnout and compassion fatigue, which are detrimental to their wellbeing. Here, we recorded event-related potentials (ERP) from physicians and matched controls as they were presented with visual stimuli depicting body parts pricked by a needle (pain) or touched by a Q-tip (no-pain). The results showed early N110 differentiation between pain and no-pain over the frontal area as well as late P3 over the centro-parietal regions were observed in the control participants. In contrast, no such early and late ERP responses were detected in the physicians. Our results indicate that emotion regulation in physicians has very early effects, inhibiting the bottom-up processing of the perception of pain in others. It is suggested that physicians' down-regulation of the pain response dampens their negative arousal in response to the pain of others and thus may have many beneficial consequences including freeing up cognitive resources necessary for being of assistance.

Introduction

Research in cognitive neuroscience using functional neuroimaging techniques reliably demonstrated that perceiving or even imagining other people in pain is associated with activation in a neural circuit involved in pain processing, including the somatosensory cortex, anterior insula, dorsal anterior cingulate cortex (dACC), anterior medial cingulate cortex (aMCC), and periaqueductal gray (PAG), a major site in pain transmission and processing of fear and anxiety (e.g., Akitsuki and Decety, 2009, Jackson et al., 2006 for a review). These results suggest that attending to people in pain triggers a sort of empathic mimicry response in the observer. It is worth mentioning that the activation of this neural network reflects a general aversive response (Yamada and Decety, 2009). Indeed, this network of regions underpin a physiological mechanism that mobilizes the organism to react–with heightened arousal and attention–to threatening situations (Decety, in press-a). Pain itself signals a potential threat in the environment and urges individuals to escape or avoid its source (Williams, 2002).

When witnessing another person experience pain, the scope of observer's reaction can range from concern for personal safety, including feelings of alarm, fear and avoidance, to concern for the other person, including compassion, sympathy, and care-giving (Goubert et al., 2009). The somatic sensorimotor resonance in pain processing areas between other and self may trigger empathic concern and feelings of sympathy (e.g., Decety et al., 2008). But the same signals may also constitute a threat to the individual that can lead to personal distress (i.e., feelings of discomfort and anxiety) or even compassion fatigue. If not regulated, this distress can be costly, both physiologically and cognitively, impact on the individual's wellbeing, and can eventually conflict with their capacity of being of assistance to the other (Decety and Lamm, 2009).

This necessity of regulation is particularly relevant for physicians and other health care professionals who, by the very nature of their work, not only encounter people with various injuries in their everyday practice, but also often need to inflict pain in the course of their treatments. Being overly sensitive to other people's pain could thus be detrimental and cause a host of serious deleterious effects such as compassion fatigue or burnout in this population (Figley, 2002). It is therefore vital that physicians regulate their capacity to empathize with their patients so that their emotional reaction does not interfere with the efficacy of their treatment nor impact their wellbeing. However, active (conscious) regulation of negative emotions also has physiological and socio-psychological costs. For instance, research has shown that it can disrupt communication, reduce rapport and increase blood pressure (Butler et al., 2003). Without some powerful regulatory mechanisms, it is very likely that medical practitioners would experience personal distress and anxiety when facing other people in pain, and this negative arousal would interfere with their ability to heal.

Previous neuroimaging work showed that the perception of pain in others can be modulated by a host of factors including attentional demands (Fan and Han, 2008, Gu and Han, 2007), social relationship between individuals (Singer et al., 2006), cognitive appraisal (Lamm et al., 2007), and a priori attitudes towards others (Decety et al., 2009). Of special interest in the context of medical practitioners, an fMRI study conducted by Cheng et al. (2007) compared the brain hemodynamic response in a group of physicians and a group of matched control participants when they were exposed to short video clips depicting hands and feet being pricked by a needle (painful situations) or being touched by a Q-tip (non-painful situations). The results demonstrated activation of the pain matrix in the control participants when they attended to the painful situations relative to the non-painful ones. A different pattern of signal change and effective connectivity was detected in the physicians when they watched the painful procedures. Cortical regions underpinning executive functions, self-regulation (dorsolateral and medial prefrontal cortex), and executive attention (precentral, superior parietal and temporo-parietal junction) were activated, and unlike in the control group, no activation was detected in the dACC, anterior insula and PAG.

Current models of empathy for pain emphasize that this phenomenon involves both an automatic component (bottom-up) based on the perception–action coupling that results in affective sharing, and a executive control (top-down) component subserved by the prefrontal cortex to regulate this experience (Decety, in press-b, Decety and Jackson, 2004, Decety and Moriguchi, 2007, Goubert et al., 2009). However, it is not known at what stage of information processing this regulation occurs in physicians. Because of the low temporal resolution of the blood oxygen dependent signals, which has a sensitivity of several seconds, functional MRI studies are not optimally suited to address this important question.

To investigate this issue, the current study used event-related potentials (ERP) to compare the time course of pain perception processing (and subsequent emotion regulation) in physicians (Physicians) and non-physicians (Controls), who were exposed to a series of static visual stimuli showing body parts either being pricked by a small needle or being touched by a Q-tip. The body parts pricked by the needle would actually activate the nociceptive system via sensory information conveyed by A-delta nerve fibers, which qualitatively differ from the second nociceptive input system conveyed by c-nociceptors.

According to the results of recent ERP studies in the domain of pain empathy, the temporal dynamics of perception of pain in others consists of two responses: (1) an early emotional sharing component (frontal N110); and (2) a late cognitive evaluation (centro-parietal P3) (Fan and Han, 2008, Han et al., 2008). Here, we hypothesized that the Physicians would demonstrate an early modulation of the emotion-sharing component that would reflect their acquired ability to down-regulate the bottom-up processing of negative stimuli. In this case, we anticipate no difference in ERP response between the stimuli depicting painful situations and the stimuli depicting non-painful situations in physicians. However, it may also be possible that the automatic resonance to pain is still present in the physicians and that the down-modulation of pain processing occurs at a later stage, as part of a cognitive re-evaluation. If this is the case, similar early ERP response between the Physicians and the Controls should be observed, with group differences occurring only at a later cognitive evaluative stage of pain-perception processing. The results of this investigation have a significant impact on the neurophysiological and psychological models of emotion regulation.

Section snippets

Participants

Thirty-three participants (17 females, mean age 35; SD 8 years) were enrolled in the study after providing written informed consent approved by the local Ethics Committee of Yang-Ming University. Three participants (2 males and 1 female) were excluded from data analysis because of excessive artifacts during EEG recording. According to their medical expertise, the participants were divided into two groups. One group (N = 15; eight females) consisted of physicians (Physicians) from internal

Behavioral measures

No difference was found in the dispositional measures between the two groups (F 1, 28 = 0.032, P = 0.859) (Table 1). However, one-way ANOVAs calculated on the subjective pain ratings showed a significant difference between the groups for pain intensity (F 1, 28 = 54.359, P < 0.001) and unpleasantness (F 1, 28 = 63.777, P < 0.001), such that the control participants reported significantly higher pain intensity and unpleasantness ratings than did the physicians. All participants correctly reported the pain

Discussion

In sum, in line with previous ERP studies on pain empathy (Fan and Han, 2008, Han et al., 2008), the present study demonstrates a frontal N110 and a late centro-parietal P3 while the controls participants watched body parts pricked by a needle in comparison with body parts being touched by a Q-tip. In contrast, in the physicians, there was no such ERP differentiation, as well as lower subjective ratings of pain intensity and unpleasantness with respect to the controls' rating. The frontal N110

Acknowledgments

The study was sponsored by National Science Council (NSC 97-2410-H-010-003-MY2; NSC 97-2752-H-010-004-PAE), National Yang-Ming University Hospital (RD2008-015; RD2009-005), and Health Department of Taipei City Government (97001-62-020). Dr. Jean Decety was supported by the NSF (BCS-0718480). None of the authors have any conflict of interest.

References (46)

  • KarayanidisF. et al.

    Frontal processing negativity in a visual selective attention task

    Electroencephal. and Clin. Neurophysiol.

    (1996)
  • OlofssonJ.K. et al.

    Affective picture processing: an integrative review of ERP findings

    Biol. Psychol.

    (2008)
  • TaakeI. et al.

    Early frontal responses elicited by physical threat words in an emotional stroop task: modulation by anxiety sensitivity

    Biol. Psychol.

    (2009)
  • YamadaM. et al.

    Unconscious affective processing and empathy: an investigation of subliminal priming on the detection of painful facial expressions

    Pain

    (2009)
  • BufalariI. et al.

    Empathy for pain and touch in the human somatosensory cortex

    Cereb. Cortex

    (2007)
  • ButlerE.A. et al.

    The social consequences of expressive suppression

    Emotion

    (2003)
  • ClarkW.C. et al.

    Applications of sensory detection theory to problems in laboratory and clinical pain

  • DavisM.H.

    Empathy: a Social Psychological Approach

    (1996)
  • DecetyJ.

    A social cognitive neuroscience model of human empathy

  • Decety, J., in press-a. Dissecting the neural mechanisms mediating empathy and sympathy. Emotion...
  • Decety, J., in press-b. To what extent is the experience of empathy mediated by shared neural circuits? Emotion...
  • DecetyJ. et al.

    The functional architecture of human empathy

    Behav. Cogn. Neurosci. Rev.

    (2004)
  • DecetyJ. et al.

    Human empathy through the lens of social neuroscience

    Sci. World J.

    (2006)
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