Psychopharmacological modulation of event-related potentials suggests that first-hand pain and empathy for pain rely on similar opioidergic processes

Rütgen, Markus; Seidel, Eva-Maria; Pletti, Carolina; Riečanský, I; Gartus, Andreas; Eisenegger, Christoph; Lamm, Claus

doi:10.1016/j.neuropsychologia.2017.04.023

Cited by 32 publications

(30 citation statements)

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“…While the latter might be achieved by neural processing within the TPJ (Saxe and Kanwisher, 2003), affect sharing may depend on shared representations during the firsthand (pain) experience and empathy for it (Bastiaansen et al, 2009;Singer and Lamm, 2009;Decety, 2010). Previously, this has been linked to neural processing within the dACC/aMCC and anterior insula (Corradi-Dell'Acqua et al, 2011, 2016Lamm et al, 2011;Rütgen et al, 2018;Carrillo et al, 2019), including an initial, univariate analysis of the current study (Rütgen et al, 2015b). Using a novel multivariate analysis approach, we here partly confirmed and extended these previous findings: First, we found increased pattern similarity within the dACC/aMCC and insula during first-hand pain (compared to pain empathy), while pain empathy (compared to first-hand pain) was associated with regions such as hippocampus, inferior temporal cortex, including the fusiform gyrus, MPFC, and PCC (Figure 2AB).…”

Section: Discussionmentioning

confidence: 99%

“…The so-called "shared representations account" suggests that empathy for an affective state engages similar neuronal processes as experiencing the affective state directly (Zaki et al, 2016;Lamm et al, 2019). In line with this assumption, previous studies implicated the dorsal anterior cingulate cortex (also termed anterior mid-cingulate cortex; dACC/aMCC) and the anterior insula in the first-hand experience of pain and in pain empathy (Fan et al, 2011;Lamm et al, 2011;Rütgen et al, 2015bRütgen et al, , 2015aRütgen et al, , 2018Marsh, 2018). Furthermore, a recent animal study revealed neurons within the rat ACC that coded not only for first-hand pain but also fired when rats witnessed a conspecific receiving footshocks (Carrillo et al, 2019).…”

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confidence: 81%

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Pattern similarity and connectivity of hippocampal-neocortical regions support empathy for pain

Wagner

Ruetgen

2019

Preprint

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AbstractEmpathy is thought to engage mental simulation, which in turn is known to rely on hippocampal-neocortical processing. Here, we tested how hippocampal-neocortical pattern similarity and connectivity contributed to pain empathy. Using this approach, we analyzed a data set of 102 human participants who underwent functional MRI while painful and non-painful electrical stimulation was delivered to themselves or to a confederate. As hypothesized, results revealed increased pattern similarity between fist-hand pain and pain empathy (compared to non-painful control conditions) within the hippocampus, retrosplenial cortex, the temporo-parietal junction and anterior insula. While representations in these regions were unaffected by confederate similarity, pattern similarity in the dorsal MPFC was increased the more dissimilar the other individual was perceived. Moreover, hippocampal connectivity with regions engaged in first-hand pain was also increased during pain empathy, during which hippocampal coupling with the fusiform gyrus positively scaled with self-report measures of individual perspective taking skills. These findings highlight that shared representations and interactions within a hippocampal-neocortical network support pain empathy. This potentially reflects memory-based mental simulation processes, which seem partially modulated by personality traits and the perceived similarity of the other individual in pain.

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 81%

Pattern similarity and connectivity of hippocampal-neocortical regions support empathy for pain

Wagner

Ruetgen

2019

Preprint

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“…Research using functional neuroimaging and electrophysiological methods in humans has shown that observing other individuals in an emotional state results in similar brain activations as being in the same emotional state oneself (Coll & Jackson, 2016;Lamm et al, 2017). Such socalled shared neural activations have been identified in brain regions involved in affective, sensory, and motor processing and are considered to be crucial for empathy (Rütgen et al 2015(Rütgen et al , 2018; but see Krishnan et al 2016). This has been demonstrated consistently using the so-called empathy for pain paradigm: being in pain and seeing pain inflicted on others both result in increased activations in several brain regions, including insular, cingulate, and sensorimotor cortex (Betti & Aglioti, 2016;Bufalari & Ionta, 2013;Keysers et al 2010;Lamm et al 2011Lamm et al , 2016Lamm et al , 2017Zaki et al 2016).…”

Section: Introductionmentioning

confidence: 99%

Increasing self-other bodily overlap increases sensorimotor resonance to others’ pain

Riečanský

Lengersdorff

Pfabigan

et al. 2019

Cogn Affect Behav Neurosci

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Empathy for another person's pain and feeling pain oneself seem to be accompanied by similar or shared neural responses. Such shared responses could be achieved by mapping the bodily states of others onto our own bodily representations. We investigated whether sensorimotor neural responses to the pain of others are increased when experimentally reducing perceived bodily distinction between the self and the other. Healthy adult participants watched video clips of the hands of ethnic ingroup or outgroup members being painfully penetrated by a needle syringe or touched by a cotton swab. Manipulating the video presentation to create a visuospatial overlap between the observer's and the target's hand increased the perceived bodily self-attribution of the target's hand. For both ingroup and outgroup targets, this resulted in increased neural responses to the painful injections (compared with nonpainful contacts), as indexed by desynchronizations of central mu and beta scalp rhythms recorded using electroencephalography. Furthermore, these empathy-related neural activations were stronger in participants who reported stronger bodily self-attribution of the other person's hand. Our findings provide further evidence that empathy for pain engages sensorimotor resonance mechanisms. They also indicate that reducing bodily self-other distinction may increase such resonance for ingroup as well as outgroup targets.

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“…Moreover, mechanistic evidence on whether and how the endogenous opioid system functions when perceiving others' pain is still lacking. Using positron emission tomography, Karjalainen et al (2017) revealed the involvement of μ-opioid receptor in vicarious pain, and psychopharmacological and neuroimaging findings of our own lab (Rütgen et al, 2015a;Rütgen et al, 2015b;Rütgen et al, 2018) indicate a causal role of the opioid system in empathy for pain. Recent mediation analyses, though somewhat inconclusively, suggest that this may be explained by effects on emotion identification (Coll et al, 2017), while related research revealed that other neurochemical mechanisms might play a role in empathy for pain as well (Mischkowski et al, 2016).…”

Section: Introductionmentioning

confidence: 70%

“…In this respect, it is important to note that the opioid system has been linked to different facets of prosociality. For instance, release of endogenous opioids has been associated with social bonding, attachment, and empathy (Machin and Dunbar 2011;Rütgen et al, 2015b;Nummenmaa and Karjalainen 2018;Nummenmaa and Tuominen 2018;Rütgen et al, 2018). Therefore, the decreases in discriminating others' facial expressions as showing pain under opioidergic blockade might suggest an attenuation in the sensitivity of pain expression perception, which ultimately may result in a decrease in the social-affective link between persons, and a corresponding reduction in prosociality.…”

Section: Discussionmentioning

confidence: 99%

Pharmacological fMRI provides evidence for opioidergic modulation of discrimination of facial pain expressions

Yan¹,

Rütgen²,

Zhang³

et al. 2020

Preprint

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The endogenous opioid system is strongly involved in the modulation of pain. However, the potential role of this system in perceiving facial pain signals from others has not been sufficiently explored as of yet. To elucidate the contribution of the opioid system to the perception of painful facial expressions, we conducted a double-blind, within-subjects pharmacological functional magnetic resonance imaging (fMRI) study, in which 42 participants engaged in an emotion discrimination task (pain vs. disgust expressions) in two experimental sessions, receiving either the opioid receptor antagonist naltrexone or an inert substance (placebo). On the behavioral level, participants less frequently judged an expression as pain in the naltrexone session compared with the placebo session. On the neural level, parametric modulation of activation in the (putative) right fusiform face area (FFA), which was correlated with increased pain intensity, was higher in the naltrexone than in the placebo session. Regression analyses revealed that brain activity in the right FFA significantly predicts behavioral performance in disambiguating pain from disgust, without difference between sessions. These findings suggest that reducing opioid system activity decreased participants' sensitivity for facial expressions of pain, and that this was linked to possibly compensatory engagement of processes related to visual perception, rather than to higher-level affective processes, and pain regulation.

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Psychopharmacological modulation of event-related potentials suggests that first-hand pain and empathy for pain rely on similar opioidergic processes

Cited by 32 publications

References 51 publications

Pattern similarity and connectivity of hippocampal-neocortical regions support empathy for pain

Pattern similarity and connectivity of hippocampal-neocortical regions support empathy for pain

Increasing self-other bodily overlap increases sensorimotor resonance to others’ pain

Pharmacological fMRI provides evidence for opioidergic modulation of discrimination of facial pain expressions

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