Integrating neuroimaging, behavioral and physiological methods in three independent assessments, we show that emotion regulation and pain regulation skills are a shared ability that is reflected in functioning of the amygdala. Specifically, greater success in voluntarily reappraising picture-induced negative emotion as indexed by corrugator EMG predicted greater success in reappraising heat-induced pain as evidenced by changes in subjective ratings of pain unpleasantness and in the modulation of the activity of a bilateral amygdalar cluster during pain regulation associated with pain regulation success. Similarly, the ability to modulate the activity of the left amygdala during emotion regulation was also predictive of self-reported pain regulation success. Although these emotion and pain regulation amygdalar clusters did not spatially overlap, individual differences in the degree of modulation within these clusters were correlated across regulation paradigms. These associations were evident despite significant temporal gaps (1–3+ years) between our assessments, which substantiate previous findings regarding the stability of individual differences in emotion regulation (Davidson, 2003
; Lee et al., 2009
Our results point to a previously unreported commonality between emotion regulatory and pain regulatory success. Prior evidence stemming from various fields has highlighted the frequent co-occurrence of pain and negative affect (Neugebauer et al., 2004
; Price, 2000
; Wiech & Tracey, 2009
). Negative affect deeply permeates both psychopathological and pain states (Price, 2000
; Rainville et al., 2005
) as is illustrated, for example, by the fact that the anxiolytic effects of benzodiazepines provide pain relief despite their lack of analgesic properties (Dellemijn & Fields, 1994
). Thus, skill at volitionally regulating emotions may generalize to pain. We tested this hypothesis using three experimental paradigms that together examined individual ability to reappraise negative emotion and pain. We found that regulatory ability in response to negative pictures predicted success while regulating responses to pain, which suggests that common skills underlie the regulation of both emotion and pain.
Our study further extends previous findings showing that changing the meaning of a negative event impacts functioning of the amygdala. This subcortical region is considered part of the brain’s early appraisal system (LeDoux, 2000
), and recent evidence suggests that it tracks a combination of valence and arousal dimensions of one’s subjective experience in response to an emotional stimulus (Winston, Gottfried, Kilner, & Dolan, 2005
). Following this rapid tracking, the amygdala recruits behavioral, endocrine and autonomic responses via its efferent projections to brainstem nuclei (LeDoux, 2000
; LeDoux, 2000
; Winston et al., 2005
). Relatedly, direct amygdalar stimulation increases activity of the corrugator muscle (Lanteaume et al., 2007
), which is well known to be associated with valence judgments (Lang et al., 1993
). Accordingly, amygdalar activity has been known to be sensitive to regulatory goals of increasing and decreasing negative affect as revealed by cognitive-reappraisal paradigms (Ochsner et al., 2004
; Phan et al., 2005
; Urry et al., 2006
; van Reekum et al., 2007
), where the extent of change in amygdalar activation during regulation correlates with self-reported changes in arousal and negative affect (e.g., Ochsner et al., 2004
). Here, we extended this finding using an objective metric of emotional state, where our participants’ emotion regulatory abilities as measured by corrugator EMG activity were predictive of the degree of change in activity of a left-amygdalar cluster following emotion regulation instruction (Lee et al., 2010
Notably, we found that emotion regulation success measured by corrugator EMG and left amygdalar activation during emotion regulation were both predictors of the modulation of amygdalar activation that was associated with pain regulation success. As noted earlier, the amygdala has been found to reflect emotion-dependent modulation of spinal nociceptive responses (Roy et al., 2009
) and pain unpleasantness (Berna et al., 2010
) following negative mood inductions. Here, we found that the degree of change in amygdalar activity while upregulating versus downregulating pain was associated with corresponding changes in subjective pain unpleasantness and heart rate. Of note, we found separate amygdalar clusters associated with regulatory success in the negative picture-induced emotion and in the thermal pain paradigms. Although our whole-brain image acquisition is not ideally suited to support claims regarding the involvement of specific amygdalar nuclei during our tasks, it is possible that sensory modality-specific demands of our paradigms may have primarily engaged different areas of amygdalar reappraisal circuitry. For example, extracellular recordings of neurons located in the central nucleus of the amygdala of rats have demonstrated that the majority of them respond to thermal and mechanical but not visual or auditory stimuli (Bernard et al., 1992
; Neugebauer et al., 2004
). In contrast, projections from the visual cortex in the monkey have been shown to be primarily to basal and lateral nuclei (Iwai, Yukie, Suyama, & Shirakawa, 1987
). Another related possibility is that reappraising noxious thermal stimulation, an intrinsically threatening stimulus, evoked marked arousal processing in the amygdala, which has been shown to be primarily reflected in dorsal nuclei activity (Davis et al., 2010
), consistent with the location of the peak in amygdalar BOLD signal associated with pain regulation success. In contrast, the reappraisal of negative images containing varying arousal levels, and the reflection of reappraisal outcome in corrugator EMG, which is known to be particularly sensitive to the valence, rather than arousal, dimension of one’s emotional responding (e.g., Lang et al., 1993
), might have contributed to our finding a neural correlate of emotion regulatory success in a more ventral amygdalar region, previously shown to be implicated in valence processing (Davis et al., 2010
). Despite our having found separate clusters reflecting amygdalar engagement across these two modalities of negative affect modulation, our finding that skills in reappraising negative emotion predicted the magnitude of change in the activation of the amygdala during pain regulation suggests that an important way in which affective style may influence the processing of pain is via an individual’s ability to effectively modulate appraisal processes that are at least partially reflected in this brain area. The finding that individual differences in degree of modulation of the amygdala during an emotion regulation paradigm strongly predict individual differences in the degree of modulation of amygdalar activity during a pain regulation paradigm further corroborates this idea.
The unusual nature of this study, with independent assessments of regulatory skill following multi-year temporal intervals, provided us with an excellent opportunity to examine the stability of individual differences in affective responding. The fact that our predictions were confirmed despite significant intervals is a strong indicator of the stability of affective style (Davidson, 2003
). The amygdala is one of a few regions for which the reliability of hemodynamic responses to emotional stimuli (i.e., fearful faces) has been verified (Johnstone et al., 2005
). Our results not only reinforce these findings by providing further evidence of the temporal stability of individual skill in voluntary regulation of negatively valenced emotional experience (Lee et al., 2009
), but also indicate they may be extended to the emotional components involved in pain processing via the engagement of the amygdala.
In our current report of trait-like variability in emotion and pain regulation success, we adopted a contrast between two active regulatory conditions (enhance and suppress), which maximized our ability to identify individual differences in change in activity in a known primary neural target of regulation (i.e., the amygdala). While the focus in our analysis was on the amygdala, future work should address common involvement of cortical circuitry in picture-induced emotion regulation and pain regulation, both across active regulation conditions (controlling for cognitive demand), and across the more commonly analyzed contrasts that include a passive control condition. Of note, the ventrolateral prefrontal cortex (VLPFC) has been shown to play a crucial role in the instantiation of top-down control of both emotion (Wager, Davidson, Hughes, Lindquist, & Ochsner, 2008
) and pain processing (Salomons, Johnstone, Backonja, Shackman, & Davidson, 2007
). Such analyses will shed light on whether circuitry involving the VLPFC is common across similar reappraisal processes of emotion-eliciting information from different modalities.
Two limitations of the current work warrant future research. First, the nociceptive neuronal population in the amygdala is known to be heterogeneous: Although the majority of neurons respond to pain in an excitatory manner, some are inhibitory (Bernard et al., 1992
; Neugebauer et al., 2004
), which may underlie the amygdalar participation in stress-induced analgesia (Fields, 2000
; Fox & Sorenson, 1994
). Thus, delineating which neuronal groups in the amygdala are recruited under differential psychological contexts, leading to analgesic or hyperalgesic outcomes, requires further study. Lastly, although the inclusion of only males is a limitation, we previously found no sex differences in the reliability of emotion regulation skills as indexed by corrugator, suggesting that the predictive value of individual differences in affective style may be similarly valid across males and females(Lee et al., 2009
). Future work should, however, include both females and males.
In conclusion, our findings provide novel evidence that emotion regulation skills predict skill in regulating pain, and that the amygdala reflects processes common to these two domains.