Toward an integrative view of human pain and suffering
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Physics of Life Reviews 11 (2014) 569572
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Toward an integrative view of human pain and sufferingReply to comments on Facing the experience of pain:
A neuropsychological perspective
Franco Fabbro a,b,, Cristiano Crescentini a
a Department of Human Sciences, University of Udine, Udine, Italyb Perceptual Robotics (PERCRO) Laboratory, Scuola Superiore SantAnna, Pisa, Italy
Received 3 July 2014; accepted 10 July 2014Available online 23 July 2014
Communicated by L. Perlovsky
Keywords: Pain; Suffering; Salience; Predictive coding; Personality; Mindfulness
We would like to begin this response by recognizing the important contribution made by Grant , Pagnoni and Porro , Avenanti, Vicario and Borgomaneri , Masataka , Gard , and De Anna  to our review . Through their thought-provoking and insightful commentaries, and with their diverse expertise, all commentators have con-tributed to enrich the discussion on human pain and suffering.
In his commentary, Grant  has focused on the different conditions of human suffering, from physical pain to the thought of ones own death. Based on recent neuroscience evidence , he proposes to distinguish the suffering caused by physical pain, which also associates with specific affective components, from the suffering caused, for instance, by social exclusion. In particular, the activation of overlapping brain areas (such as the anterior insula and the anterior cingulate cortex) for physical and psychological pain would not be suggestive of a common experience of pain but would reflect the activation of the nodes of a salience network [8,9], the activation of which is driven by noxious as well as non-painful stimuli and particularly by conditions involving psychological pain. With no difficulty we are willing to accept Grants proposal. Nonetheless, what we really wanted to emphasize in our review concerned more the possible attitudes one can show when facing the experience of pain than the neural representation of physical or psychological pain and suffering. Thus, we were particularly interested in what are the consequences of showing very common attitudes when facing suffering, such as anger, avoidance, denial, compared to perhaps more useful attitudes,
DOI of original article: http://dx.doi.org/10.1016/j.plrev.2013.12.010.DOIs of comments: http://dx.doi.org/10.1016/j.plrev.2013.12.006, http://dx.doi.org/10.1016/j.plrev.2014.05.006,
http://dx.doi.org/10.1016/j.plrev.2014.05.008, http://dx.doi.org/10.1016/j.plrev.2014.06.001, http://dx.doi.org/10.1016/j.plrev.2014.06.015, http://dx.doi.org/10.1016/j.plrev.2014.07.003.
* Corresponding author at: Department of Human Sciences, University of Udine, Via Margreth 3, 33100, Udine, Italy. Tel.: +39 0432 556550; fax: +39 0432 558342.
E-mail address: email@example.com (F. Fabbro).http://dx.doi.org/10.1016/j.plrev.2014.07.0061571-0645/ 2014 Elsevier B.V. All rights reserved.
570 F. Fabbro, C. Crescentini / Physics of Life Reviews 11 (2014) 569572such as being with dignity in front of pain, or even to meet suffering with a gentle and compassionate approach such as that centered on the here and now of mindfulness meditation . We agree with Grant  that all forms of suffering could be salient, and that the salience systems could probably have developed to safeguard the physical integrity of the individual. However, human beings, like all other objects of the universe, have a transient existence, and their integrity is bound, sooner or later, to finish. In front of the transience of life, our subjective experience can either react to suffering with so-called neurotic attitudes (anger, denial, avoidance, etc.), or, if properly educated, with strategies best suited to a species that has defined itself sapiens.
In their comment, Pagnoni and Porro  have reviewed evidence suggesting the possibility to frame the processes involved in placebo hypoalgesia and in contemplative practices such as meditation, but more generally in the cognitive modulation of pain, in terms of the predictive coding perspective [11,12]. According to this framework, the nervous system generates a model of the world that is continually refined based on past experiences. Our perceptions thus depend on the constant integration of top-down and bottom-up processing ; in other words the sensory data are influenced by prior knowledge. Prior experiences and expectations thus play a fundamental role in both the experience of physical pain and more generally in front of suffering. In our opinion, this important perspective may also help to understand better the role that the personality structure plays when facing the experience of pain. Commonly, the notion of personality includes a wide range of knowledge, specific to each individual, which is mainly organized at an implicit level [14,15]. According to clinical psychology, this knowledge has developed from fetal life to help us facing difficult and dangerous situations [16,17]. Thus, our knowledge of the world tends to be experienced with prior feelings generally characterized by emotional states of fear and anxiety. According to the predictive coding perspective, this may determine in many situations an amplification of suffering. For this reason, Pagnoni and Porro rightly argue that mindfulness meditation, to which one must add other paths such as music, art and psychotherapy, can interrupt this sort of short circuit, possibly contributing to cause a progressive personality change .
In their commentary, Avenanti et al.  underscore the importance of the human social dimension in the modulation of pain and suffering. They noticed that the forms of pain originated by the separation from significant others and empathy for pain share many cognitive and neural systems and have probably evolved in combination with parental care in social animals. For this reason, Avenanti et al. argue that social support, positive social relationships and empathy in significant others are associated with feeling less pain. This consideration is supported by a series of studies that have investigated the effects of social modulation on pain and suffering . In line with the proposal of Pagnoni and Porro , within a predictive coding perspective, a few crucial parameters that appear to modulate pain and suffering through influencing the salience of noxious stimuli were seen to be the degree of perceived closeness of the social partners (through appropriate verbal and non-verbal interaction) and the degree to which the intentions of the social partners can be perceived during interpersonal interactions . On the other hand, another important factor capable of modulating pain is the attachment style of the suffering person . This latter parameter, in particular, is one of the factors that influence the personality  and hence, as we mentioned, the attitude with which one faces the experience of suffering. From a complementary perspective, recent proposals suggest that loving-kindnessor compassion meditation, which are found to be effective in increasing positive social emotions, prosocial behavior and feelings of social connectedness [21,22], may also directly promote analgesia in the practitioners through the release of endogenous opioids .
As already mentioned in the present response and in the target article , it is known that humans react to the experience of suffering in very different ways. One of the most typical responses, as suggested by Masataka in his commentary , consists in the construction of stories; a phenomenon defined by clinical psychology as rational-ization and considered as one of many defense mechanisms of the personality . According to Gazzaniga, these stories are generated by a system in the human mind, called the interpreter module, which seeks to unify the conscious-ness and to reduce cognitive dissonance by continuously explaining the world using inputs from the surroundings and from the current cognitive state [24,25]. Often, these stories are built in the complete ignorance of the real reasons that lead an individual to feel specific emotions and/or perform certain actions. As shown in our target article , mindfulness meditation, and in particular vipassana meditation, trains the individual to face pain with an attitude as much neutral (non-judgmental) as possible and also helps to reduce, or at least observe at the right distance (non-attachment or letting go), the continuous evaluative processes of the mind that seeks verbal explanations and solutions to the experience of pain [10,2628].
In regard to this latter aspect, in his commentary Gard  has elegantly reviewed the brain signatures of supe-rior pain modulation through mindfulness meditation and, more importantly, has highlighted as such signatures differ
F. Fabbro, C. Crescentini / Physics of Life Reviews 11 (2014) 569572 571depending on the strategy and skill applied by meditators when facing painful stimuli. Thus, it seems that only ad-vanced meditators are able to simply process the sensory quality of the painful experience while refraining from excessive cognitive/emotional elaboration (non-judging/non-reactive attitude). Accordingly, pain modulation with this strategy in expert meditators occurs through an increased activation in pain related brain regions, such as the insula and the anterior cingulate cortex, and decreased activation in cognitive control/evaluative brain areas such as the lat-eral prefrontal cortex [10,27,28]. Of great interest and worth to be taken into consideration in future studies on pain modulation and mindfulness, Gard  has noticed that activation in pain related regions during pain processing also depends on skill learning, namely on how one is proficient in applying a strategy. Thus, increased effort and brain ac-tivation are required at the beginning of skill learning relative to what happens at higher levels of proficiency. Overall, recent researches investigating the neurofunctional mechanisms of pain modulation through mindfulness, as summa-rized by Gard , contribute to a point that we raised in our original target review , namely that stand mindfully in the face of pain is a difficult task that requires a long and constant meditation practice. However, despite the challenges that this task requires, the studies also suggest that the effort can be fully justified.
Coming back to the comment by Masataka , he has also claimed that music is an important skill that can reduce cognitive dissonance and thus relieve the pain experience. Both hypotheses are substantiated by data in the literature. It is well-known in fact that musical experience tends to deactivate language processing cortical areas (thus reducing cognitive dissonance), while simultaneously activating several cortical and subcortical structures (nucleus accumbens, ventral tegmental area, periacqueductal gray) responsible for the regulation of emotional pain and suffering . Moreover, it was found that some forms of music trigger positive emotions, determining the release of dopamine, oxytocin, and endogenous opioids. These psychobiological effects appear to be associated with the influence that music has on reducing pain, anxiety and depression .
Finally, in his commentary, De Anna  has summarized the position of the leading philosophers of classical antiq-uity in relation with the problem of reality. According to these philosophers, and in agreement with some recent ideas developed in theoretical physics, reality (of objects, time, etc.) is not as it appears [33,34]. Since the existence of the objects has ambivalent aspects, the teaching of classical philosophy suggests focusing the attention on the world of our experiences, that is, on the sphere in which we experience pain and suffering. Even the classical Western philosophy, along with many non-European philosophical traditions, has stressed the importance of the practice of virtue, and in particular non-attachment as a strategy to alleviate pain and suffering . In this regard, De Anna  rightly suggests that there is a renewed interest among contemporary historians to study the issues of pain and suffering developed in Western culture. The integration of this knowledge and practices with the strategies to cope with suffering, as has happened to many forms of meditation inspired by the East [10,36], will improve our practices and skills to face pain experiences.
The issue of pain and suffering is a great example of how the major human problems cannot be addressed in a strictly sectoral manner. Who works in the context of pain and human suffering must, therefore, be able to develop an integrated approach taking into consideration knowledge from a range of different disciplines such as physics, neuroscience, pharmacology, clinical psychology, art, philosophy, and even spiritual traditions. To pay attention only to ones own discipline while denying other forms of knowledge is counterproductive both for those involved in the research field and for those who are interested in clinical or technological programs aimed at alleviating human suffering.
This research was supported by a grant from the Mind and Life Institute (Mind and Life Contemplative Fellowship 2012-04-001 to FF). CC was supported by a Post-Doctoral research fellowship funded by the University of Udine, Department of Human Sciences.
 Grant JA. What constitutes pain? Comment on Facing the experience of pain: a neuropsychological perspective by Franco Fabbro and Cristiano Crescentini. Phys Life Rev 2014;11:5534 [in this issue].
 Pagnoni G, Porro CA. Cognitive modulation of pain and predictive coding. Comment on Facing the experience of pain: a neuropsychological perspective by Fabbro and Crescentini. Phys Life Rev 2014;11:5557 [in this issue].
572 F. Fabbro, C. Crescentini / Physics of Life Reviews 11 (2014) 569572 Avenanti A, Vicario CM, Borgomaneri S. Social dimensions of pain. Comment on Facing the experience of pain: a neuropsych...