What are you feeling? Using functional magnetic resonance imaging to assess the modulation of sensory and affective responses during empathy for pain

Abstract

Background: Recent neuroscientific evidence suggests that empathy for pain activates similar neural representations as the first-hand experience of pain. However, empathy is not an all-or-none phenomenon but it is strongly malleable by interpersonal, intrapersonal and situational factors. This study investigated how two different top-down mechanisms - attention and cognitive appraisal - affect the perception of pain in others and its neural underpinnings.

Methodology/principal findings: We performed one behavioral (N = 23) and two functional magnetic resonance imaging (fMRI) experiments (N = 18). In the first fMRI experiment, participants watched photographs displaying painful needle injections, and were asked to evaluate either the sensory or the affective consequences of these injections. The role of cognitive appraisal was examined in a second fMRI experiment in which participants watched injections that only appeared to be painful as they were performed on an anesthetized hand. Perceiving pain in others activated the affective-motivational and sensory-discriminative aspects of the pain matrix. Activity in the somatosensory areas was specifically enhanced when participants evaluated the sensory consequences of pain. Perceiving non-painful injections into the anesthetized hand also led to signal increase in large parts of the pain matrix, suggesting an automatic affective response to the putatively harmful stimulus. This automatic response was modulated by areas involved in self/other distinction and valence attribution - including the temporo-parietal junction and medial orbitofrontal cortex.

Conclusions/significance: Our findings elucidate how top-down control mechanisms and automatic bottom-up processes interact to generate and modulate other-oriented responses. They stress the role of cognitive processing in empathy, and shed light on how emotional and bodily awareness enable us to evaluate the sensory and affective states of others.

Figure 1. Examples for the stimuli used in the behavioral experiment and in fMRI experiment I.

The upper image shows a needle covered by a black protector cap placed next to the hand (non-painful control stimulus). The lower image shows the (painful) injection of the same needle into the hand.

Figure 2. Samples for the stimuli used in fMRI experiment II.

The upper image shows a (non-painful, but unpleasant) tissue biopsy from the numbed hand. The lower image show the (painful) injection of novocaine into the hand. Note the different types of syringes used in the two conditions, indicating their different functions.

Figure 3. Behavioral data from fMRI experiment II.

Injections led to high intensity and unpleasantness ratings, while rated pain intensity for the numbed hand stimuli is close to zero. Note also that although the unpleasantness ratings for the numbed hand stimuli are significantly smaller than for the injection stimuli, they are substantially high and significantly different from zero.

Figure 4. Significant clusters from the random effects contrast painful>non-painful (intensity and unpleasantness rating trials pooled) of fMRI experiment I, displayed on a high-resolution structural MRI template in MNI space (used in all figures, displayed in neurological convention; red numbers indicate slice number).

The anatomical labels designate the approximate location (in the rfx average) of the functional ROIs (see text for abbreviations). Threshold P = 0.01 (FDR-corrected), k = 10.

Figure 5. Significant clusters in anterior and posterior precuneus (aPRC and pPRC) and in the right temporo-parietal junction (TPJ) revealed by the interaction contrast (Intensity: Numbed>Injection)>(Unpleasant: Numbed>Injection).

Threshold P = 0.001 (uncorrected), k = 5.

Figure 6. Additional clusters in orbitofrontal cortex (OFC) and subcallosal/perigenual ACC when contrasting the biopsy with the injection condition during pain intensity ratings (numbed>injection; intensity rating trials only).

Threshold P = 0.005 (uncorrected), k = 5.

Figure 7. Time-courses in the ROIs (anterior insulae, rostral aMCC and contralateral somatosensory cortex/Area 2) analyzed in fMRI experiment II.

Note that all areas show a significant hemodynamic response during both the injection and the numbed hand stimuli. Significant differences as determined by linear contrasts are indicated by asterisks (** = P<0.05, * P<0.10, see text for details).