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What (If Anything) Is Shared in Pain Empathy? A Critical Discussion of De Vignemont and Jacob’s Theory of the Neural Substrate of Pain Empathy

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In a recent article in Philosophy of Science, De Vignemont and Jacob defend the view that empathy involves interpersonal similarity between an empathizer and a target person with respect to internal affective states. Focusing on empathy for pain, they propose a theory of the neural substrate of pain empathy. We point out several flaws in their interpretation of the data and argue that currently available data do not differentiate between De Vignemont and Jacob’s model and alternative models. Finally, we offer some suggestions about how this might be achieved in future research.
What ðIf AnythingÞIs Shared in Pain
Empathy? A Critical Discussion of
De Vignemont and Jacobs Theory of
the Neural Substrate of Pain Empathy
John Michael and Francesca Fardo*y
In a recent article in Philosophy of Science, De Vignemont and Jacob defend the view
that empathy involves interpersonal similarity between an empathizer and a target per-
son with respect to internal affective states. Focusing on empathy for pain, they pro-
pose a theory of the neural substrate of pain empathy. We point out several aws in
their interpretation of the data and argue that currently available data do not differenti-
ate between De Vignemont and Jacobs model and alternative models. Finally, we offer
some suggestions about how this might be achieved in future research.
In recent years, controversy has erupted in the philosophy of mind, devel-
opmental psychology, and cognitive neuroscience concerning how best to
conceptualize empathy. Much of this controversy centers on the issue of
how to articulate the common intuition that empathy involves the sharing
of emotional experiences. On one side of the debate, researchers ðe.g., Eisen-
berg and Fabes 1990; Decety and Jackson 2004; De Vignemont and Singer
2006; Batson 2009; Keysers, Kaas, and Gazzola 2010; De Vignemont and
Jacob 2012Þmaintain that empathy involves interpersonal similarity between
an empathizer and a target person with respect to their internal affective
Received May 2013; revised August 2013.
*To contact the authors, please write to: John Michael, Center for Subjectivity Research, Co-
penhagen University; e-mail: johnmichaelaarhus@gmail.com. Francesca Fardo, Center of Func-
tionally Integrative Neuroscience/MindLab, Aarhus University; e-mail: francesca.fardo@gmail
.com.
yWe would like to thank Søren Overgaard, Dan Zahavi, Joe Neisser, and Micah Allen for
helpful suggestions on an earlier version of this article.
Philosophy of Science, 81 (January 2014) pp. 154160. 0031-8248/2014/8101-0002$10.00
Copyright 2014 by the Philosophy of Science Association. All rights reserved.
154
states. On the other side, another group of researchers ðGoldie 1999; Gal-
lagher 2012Þhave pointed out that emotional experiences are usually di-
rected toward intentional objects and proposed that in empathy one person
engages with a target persons experience and thereby comes to have an ex-
perience with the same intentional object.
1
On this latter view, empathy in-
volves the sharing of the intentional component of emotional experience
rather than the sharing of internal affective states. Still other theorists ðe.g.,
Zahavi 2011; Zahavi and Overgaard 2012Þdeny that empathy involves the
sharing of emotional experiences and, thus, do not postulate any kind of in-
terpersonal similarity at all.
One distinct advantage of the approach taken by De Vignemont and
colleagues is that their model endeavors to make sense of recent ndings
in neuroscience and is therefore constrained by the relevant empirical data.
In order to do so, they home in on a specic type of empathy, namely, empa-
thy for pain, which is particularly well researched in the empirical litera-
ture. We embrace this aspect of their approachbearing in mind, of course,
that it will be important to exercise great caution in extrapolating from a
detailed study of pain empathy to other types of empathy or to empathy in
general. But we also point out several aws in their interpretation of the
data they refer to and also criticize their overly selective review of data rel-
evant to the debate. We hope that our criticism can contribute to the fur-
ther renement of their model of empathy as well as the alternatives and to
the development of experimental methods of distinguishing among these
competing theoretical options.
De Vignemont and Jacob ð2012Þrefer to the common view that the ex-
perience of pain derives from the processing and integration of nociceptive
inputs and complex emotional and cognitive processes, implicating the par-
ticipation of several pain-specic brain structures that may be functionally
distinct. The neural network involved in pain processing is often referred
to as the pain matrix, the primary components of which are sometimes
said to be a sensory-discriminative and an affective-motivational network
ðe.g., Singer et al. 2004; Aydede 2006Þ. On this view, primary and secondary
somatosensory and posterior insular cortices are thought to serve the pro-
cessing of sensory-discriminative features of pain stimuli, such as location, du-
ration, and stimulus intensity. In the affective-motivational domain, anterior
cingulate and anterior insular cortices are thought to mediate these aspects
of pain processing, for example, the unpleasantness of pain.
In their review, De Vignemont and Jacob ð2012Þsuggest that these
two components can be dissociated and that this provides a basis for dis-
1. There are important differences among these proposals. But for present purposes,
the only feature of their proposals that is relevant is the claim that empathy involves
interpersonal similarity with respect to intentional structure rather than with respect to
internal affective states. Snow ð2000Þrequires both kinds of interpersonal similarity.
DE VIGNEMONT AND JACOBS THEORY OF PAIN EMPATHY 155
tinguishing pain empathy from the phenomenon of contagious pain. Specif-
ically, they suggest that contagious pain is more likely to recruit the sensory-
discriminative component, whereas empathy is more likely to recruit the
affective component of the pain matrix. In accordance, they argue that em-
pathy is other-centeredinsofar as it involves a concern for the other persons
affective state, whereas contagion is self-centered. In support of this posi-
tion, they refer to research suggesting that in pain empathy the affective
neural components are selectively activated ðSinger et al. 2004; Botvinick
et al. 2005Þ. They further propose a mechanism explaining how exactly pain
empathy is presumed to occur. When one person perceives another person
receiving a painful stimulus ðor a cue anticipating a painful stimulusÞ, De
Vignemont and colleagues thus argue that the affective component of the
observerspainmatrixislikelytoactivate.Theobserversbrainthengener-
ates the expectation that there is a painful stimulus impinging upon her
body and that the sensory-discriminative component of her pain matrix
will therefore be active ðbecause this would normally be the case when the
affective part of her pain matrix is activeÞ. But, of course, this is not the
case, and so the observer makes the judgment that it is not her but the other
person who is experiencing pain.
In the following, we express four separate concerns with this proposal.
The rst is conceptual. Specically, it is not clear to us what the nal in-
ference in the procedure proposed by De Vignemont and Jacob is supposed
to add: after all, the procedure begins with the observer perceiving or oth-
erwise resolving the information that someone else is in pain. So why
does the observer need to register that there is no activation in the sensory-
discriminative component of her own pain matrix in order to infer that it
is the other person who is in pain? Indeed, given that background infor-
mation about the person receiving the painful stimulation modulates the
activation of the affective component of the observers pain matrix ðas re-
viewed in Singer and Lamm ½2009, it seems that the other-centerednessis
there from the start. Hence, it is just as likely that the understanding that it
is the other who is in pain precedes the activation of the pain matrix rather
than being generated by it.
2
Second, why should specically the affective component but not the
sensory component be involved in empathy? De Vignemont and Jacobs
ð2012Þidea seems to be that since empathy is other-centered it should
not involve representations of ones own bodywhich is presumably what
2. Given that participants in the experiments discussed by De Vignemont and Jacob are
always aware that it is othersbodies, and not their own, that are being subjected to
painful stimulation, it is in fact also unclear how the results bear upon contagious pain at
all. Indeed, De Vignemont and Jacob agree ð307 and elsewhereÞthat contagion does not
involve ascription of the painful experience to the other person.
156 JOHN MICHAEL AND FRANCESCA FARDO
activation of the sensory-discriminative component of the pain matrix would
reect. But it would then seem to follow from this that the affective compo-
nent should not be activated either, since ones affective representations are,
after all, also general representations of ones own affective state. In fact, if
empathy involves imagining the experience ðincluding thoughts, feelings,
and sensationsÞof the target person, it is not clear that the sensory aspect
should be any less relevant than the affective component. In other words, if
there can be vicarious affective representations, why not also vicarious
sensory representations? And indeed, there is research suggesting that the
sensory component is also active under some circumstances when one ob-
serves others in pain ðKeysers et al. 2010Þ. The difference between these
results and the results of Singer et al. ð2004Þand Botvinick et al. ð2005Þmay
be explained by the fact that the former involved participants actually ob-
serving other people receiving painful stimuli to specic parts of their bodies,
whereas the latter involved observers receiving cues that another person was
receiving a painful stimulus. In other words, in the latter cases, the observers
did not actually see the relevant body parts, so it is no surprise that somato-
topically organized bodily representations play less of a role in these cases.
Moreover, taking a sidelong glance to the developmental literature, Roth-
Hanania, Davidov, and Zahn-Waxler ð2011Þconducted a longitudinal study
in which they found that 8-month-olds who touched the part of their own
body corresponding to the body part of another person whom they ob-
served to be in pain were subsequently, at 16 months, more likely to engage
in prosocial behavior toward someone in pain than 16-month-olds who had
not shown this response at 8 months. This suggests that a somatotopical
sensory representation of an observed painful experience plays some role
in generating an other-centered representation of the experience.
Third, De Vignemont and Jacob fail to provide adequate justication for
the claim that the sensory component of pain is predominant in contagious
pain. We are aware of no evidence that contagion involves the preferential
activation of the sensory-discriminative component of pain. Moreover, it
seems clear that other contagious affective states, such as contagious fear
and contagious sadness, involve an affective experience of the emotion one
takes on ðand presumably not any particular sensory-discriminative com-
ponentÞ. So why should the situation be reversed in contagious pain?
Fourth, it is currently unclear to what extent activation of the pain matrix
is specically related to pain phenomena. The notion of pain as emerg-
ing from the integrated activity of specic and dissociable modules ðe.g.,
sensory vs. affective components of the pain matrixÞhas been questioned in
light of recent neuroscienticndings. Indeed, the concept of the pain
matrixhas been criticized on the grounds that the different brain struc-
tures gathered together under this label in fact make up a functional catch-
DE VIGNEMONT AND JACOBS THEORY OF PAIN EMPATHY 157
all that is not specic to pain at all but, rather, to stimulus salience regardless
of sensory modality ðe.g., Iannetti and Mouraux 2010Þ. Loud sounds, strong
nonpainful vibrations, and sudden visual inputs have been shown to induce
overlapping activations in the anterior cingulate cortex and anterior insula,
among other brain areas ðMouraux et al. 2011Þ, suggesting that this neural
network may be involved in bottom-up attentional mechanisms induced by
any stimulus that may represent a threat for the individual ðLegrain et al.
2011Þ.
Thus, the very idea of the pain matrix, upon which De Vignemont and
Jacobs account is based, can be called into question. Indeed, the alternative
interpretation of the data in terms of the registration of salience would
actually t well with the idea that empathy involves taking the perspective
of another person and engaging with the intentional objectðsÞof their ex-
perience. For if Jim is in pain, the painful stimulus will be salient to him, and
if Sue takes Jimsperspectiveandengageswithhisexperience,thenthe
painful stimulus will also become salient to Sue. And just as Jim is likely to be
attending to it, Sue will be likely to direct her attention to it, too. Hence, these
data t just as well with the alternative model proposed by Goldie
and Gallagher, according to which empathy involves one person engaging
with another persons emotional experience and thereby coming to have
an experience with the same intentional object. On this latter view, what is
shared in empathy is the intentional component of affective experience
rather than any internal affective states.
Clearly, in order to resolve these issues, it will rst of all be neces-
sary to isolate pain-specic neural activity. And in fact some recent results
may point in a fruitful direction. An investigation using multivariate decod-
ing techniques identied a neurological signature of physical pain ðWager
et al. 2013Þ, providing empirical evidence that physical pain experience
can be predicted by the overall pattern of activity within a specic and dis-
tributed neural network, at least in part overlapping with the classic pain
matrix. The pattern recognition model in that experiment successfully pre-
dicted subjective pain ratings in a different group of participants under sim-
ilar conditions and under the administration of an analgesic opioid drug,
but very interestingly not under a social pain condition related to a recent
romantic breakup. Indeed, although both physical and social pain induced
activation of similar brain areas, the same algorithm failed in predicting the
experienced social pain. These results underscore the importance of caution
in the interpretation of neural activity in the so-called pain matrix. Impor-
tantly, they suggest that pain phenomena are not reected by activity in
any one area, and the level of activation of the same brain region cannot be
considered a sufcient proof of similar functions or brain mechanisms. On
the contrary, similarity in the activation prole of a brain region in different
circumstances may hide subtly different activity within that regions sub-
158 JOHN MICHAEL AND FRANCESCA FARDO
populations. Thus, understanding the brain mechanisms underpinning pain,
as well as any other sensory or cognitive process, including empathy, re-
quires going beyond the localization of function to any one area or network
of areas and actually describing their functional interactions and computa-
tional mechanisms.
And indeed, a detailed neural model of pain could help in adjudicat-
ing among the competing models of empathy. For in order to determine
whether empathy in general, or pain empathy in particular, involves inter-
personal similarity of internal affective states, of intentional objects, or of
nothing at all, it would be very useful to be able to distinguish the processes
underpinning the affective components of experiences such as pain from the
processes underpinning the intentional structure of those experiences ðsuch
as the modulation of attentionÞ. Once this is achieved, a subsequent step
could be to investigate which, if any, of these components are shared. This is
not to say that neuroscientic techniques and computational modeling are
the only tools that will be useful in making progress toward understanding
empathy. Indeed, we suspect that behavioral techniques may be especially
useful in investigating the extent to which the contents of thought, or in-
tentional objects, are shared by a person experiencing pain and a person who
learns of this and empathizes, since it is plausible that the neural differences
between distinct thoughts may be highly subtle and the intersubject variability
quite large.
Although we have identied several aws in the model put forth by
De Vignemont and Jacob ð2012Þ, we must emphasize that we support their
efforts to link up the philosophical discussion with ongoing neuroscientic
research and hope that this brief commentary contributes a further step in this
direction. Clearly, determining an optimal framework for understanding em-
pathy remains an interpretative challenge, requiring further attention from
both neuroscientic and philosophical perspectives.
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160 JOHN MICHAEL AND FRANCESCA FARDO
... It is widely agreed that the primary target of an individual's empathetic response is another's affective state. We have offered a tentative account of empathy for pain based on three further ideas (Vignemont and Singer 2006;Vignemont and Jacob 2012), each of which has recently been subjected to interesting criticisms (Deonna 2007;Michael 2014;Michael and Fardo 2014). First, we assume that empathy and emotional contagion are vicarious experiences. ...
... We have argued that the involvement of affective sharing in empathy is supported by recent findings in social neuroscience showing overlap of brain activity between one individual experiencing some specific affective state (e.g., pain, disgust, fear) and the same individual being provided with cues that another individual is in the very same affective state (Wicker et al. 2003;Keysers et al. 2004;Singer et al. 2004;Vignemont and Jacob 2012). However, as we will now see, our interpretation of the neuroscientific findings has been challenged by Michael (2014) and Michael and Fardo (2014). ...
... However, Michael (2014) and Michael and Fardo (2014) question the claim that contagious responses to another's emotional or affective experience primarily involve the activation of the sensory-discriminative component of one's own emotional or affective system, at the expense of the affective component. As we argue below, there is evidence that the sensorydiscriminative component of one's pain system constitutes vicarious contagious pain (Avenanti et al. 2006;Garbarini et al. 2015). ...
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