The pain of social disconnection: examining the shared neural underpinnings of physical and social pain
Identifieur interne : 002003 ( Istex/Corpus ); précédent : 002002; suivant : 002004The pain of social disconnection: examining the shared neural underpinnings of physical and social pain
Auteurs : Naomi I. EisenbergerSource :
- Nature Reviews Neuroscience [ 1471-003X ] ; 2012-06.
Abstract
Experiences of social rejection, exclusion or loss are generally considered to be some of the most 'painful' experiences that we endure. Indeed, many of us go to great lengths to avoid situations that may engender these experiences (such as public speaking). Why is it that these negative social experiences have such a profound effect on our emotional well-being? Emerging evidence suggests that experiences of social pain — the painful feelings associated with social disconnection — rely on some of the same neurobiological substrates that underlie experiences of physical pain. Understanding the ways in which physical and social pain overlap may provide new insights into the surprising relationship between these two types of experiences.
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DOI: 10.1038/nrn3231
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<front><div type="abstract" xml:lang="eng">Experiences of social rejection, exclusion or loss are generally considered to be some of the most 'painful' experiences that we endure. Indeed, many of us go to great lengths to avoid situations that may engender these experiences (such as public speaking). Why is it that these negative social experiences have such a profound effect on our emotional well-being? Emerging evidence suggests that experiences of social pain — the painful feelings associated with social disconnection — rely on some of the same neurobiological substrates that underlie experiences of physical pain. Understanding the ways in which physical and social pain overlap may provide new insights into the surprising relationship between these two types of experiences.</div>
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<profileDesc><abstract><p>Experiences of social rejection, exclusion or loss are generally considered to be some of the most 'painful' experiences that we endure. Indeed, many of us go to great lengths to avoid situations that may engender these experiences (such as public speaking). Why is it that these negative social experiences have such a profound effect on our emotional well-being? Emerging evidence suggests that experiences of social pain — the painful feelings associated with social disconnection — rely on some of the same neurobiological substrates that underlie experiences of physical pain. Understanding the ways in which physical and social pain overlap may provide new insights into the surprising relationship between these two types of experiences.</p>
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<p><list xml:id="l1"><item>Observational evidence has highlighted similarities between physical pain and 'social pain' — the painful feelings associated with actual or potential damage to social bonds. Thus, experiences of social rejection or loss are often described with physical pain words ('hurt feelings' and 'broken heart'), and both physical and social pain are highly noxious experiences.</item>
<item>Research on the neurochemical substrates of physical and social pain has demonstrated that both rely on opioid processes. Thus, opiates, which are potent analgesics, have also been shown to reduce separation distress behaviours in animals.</item>
<item>Neuroimaging research has demonstrated that experiences of social exclusion predominantly activate the dorsal anterior cingulate cortex (dACC) and anterior insula (AI) — regions known to have a role in the distressing experience of physical pain.</item>
<item>In addition, several lines of research have shown that experiences of negative social evaluation, rejection from a romantic partner and bereavement also lead to activity in the dACC and AI. A few studies have also shown neural activity in regions associated with the sensory component of pain (posterior insula); additional research will be needed to determine the types of social pain that elicit sensory-related processing.</item>
<item>On the basis of the shared neural circuitry associated with physical and social pain, research has shown that individuals who are more sensitive to one kind of pain are also more sensitive to the other. Thus, greater physical pain experience or sensitivity is associated with greater social pain sensitivity (rejection sensitivity or anxious attachment).</item>
<item>Another consequence of a physical–social pain overlap is that factors that alter one type of pain have a similar effect on the other. For example, social support, which is known to reduce social pain, can also reduce physical pain, and Tylenol (paracetamol; Johnson and Johnson), which is known to reduce physical pain, can also reduce social pain.</item>
<item>On the basis of the role of the dACC and AI in responding to socially painful experience, these regions may be crucial for translating experiences of social disconnection into downstream physiological responses, which have implications for health. Indeed, the dACC and AI may have a mediating role in the links between social rejection and both inflammatory activity and depression.</item>
<item>Observational evidence has highlighted similarities between physical pain and 'social pain' — the painful feelings associated with actual or potential damage to social bonds. Thus, experiences of social rejection or loss are often described with physical pain words ('hurt feelings' and 'broken heart'), and both physical and social pain are highly noxious experiences.</item>
<item>Research on the neurochemical substrates of physical and social pain has demonstrated that both rely on opioid processes. Thus, opiates, which are potent analgesics, have also been shown to reduce separation distress behaviours in animals.</item>
<item>Neuroimaging research has demonstrated that experiences of social exclusion predominantly activate the dorsal anterior cingulate cortex (dACC) and anterior insula (AI) — regions known to have a role in the distressing experience of physical pain.</item>
<item>In addition, several lines of research have shown that experiences of negative social evaluation, rejection from a romantic partner and bereavement also lead to activity in the dACC and AI. A few studies have also shown neural activity in regions associated with the sensory component of pain (posterior insula); additional research will be needed to determine the types of social pain that elicit sensory-related processing.</item>
<item>On the basis of the shared neural circuitry associated with physical and social pain, research has shown that individuals who are more sensitive to one kind of pain are also more sensitive to the other. Thus, greater physical pain experience or sensitivity is associated with greater social pain sensitivity (rejection sensitivity or anxious attachment).</item>
<item>Another consequence of a physical–social pain overlap is that factors that alter one type of pain have a similar effect on the other. For example, social support, which is known to reduce social pain, can also reduce physical pain, and Tylenol (paracetamol; Johnson and Johnson), which is known to reduce physical pain, can also reduce social pain.</item>
<item>On the basis of the role of the dACC and AI in responding to socially painful experience, these regions may be crucial for translating experiences of social disconnection into downstream physiological responses, which have implications for health. Indeed, the dACC and AI may have a mediating role in the links between social rejection and both inflammatory activity and depression.</item>
</list>
</p>
</abstract>
<abstract><p><title>Web-summary</title>
</p>
<p>The experience of social rejection, exclusion or loss is often described as 'painful'. Naomi Eisenberger here outlines the evidence that the processing of these forms of 'social pain' share many underlying neural substrates with physical pain mechanisms and considers the implications of this convergent neural circuitry.</p>
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<jtl>Nature Reviews Neuroscience</jtl>
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<fm>
<atl display="show">The pain of social disconnection: examining the shared neural underpinnings of physical and social pain</atl>
<aug>
<cau>
<fnm>Naomi I.</fnm>
<snm>Eisenberger</snm>
<inits>N I</inits>
<orf rid="a1"></orf>
<corf rid="c1"></corf>
<bio>
<p>Naomi Eisenberger is an assistant professor of psychology at the University of California, Los Angeles (UCLA), USA. She received her Ph.D. in social psychology and then completed a postdoctoral fellowship in psychoneuroimmunology at UCLA. Her research seeks to identify the basic neural systems that may have been co-opted to support more complex socio-emotional experiences, such as social rejection and social connection. She is also interested in elucidating the neural mechanisms that may translate experiences of social rejection or connection into physiological responses that have implications for health outcomes. She is the recipient of early career awards from the Association for Psychological Science, the American Psychosomatic Society and the International Union for Psychological Science.</p>
</bio>
</cau>
<aff><oid id="a1"></oid>
<org>University of California, Department of Psychology</org>
, <street>4444 Franz Hall</street>
, <cty>Los Angeles</cty>
, <st>California</st>
<zip>90095</zip>
, <cny>USA</cny>
.</aff>
<caff>
<coid id="c1"></coid>
<email>neisenbe@ucla.edu</email>
</caff>
</aug>
<hst>
<pubdate day="03" month="05" type="aop" year="2012"></pubdate>
</hst>
<execsumm>
<p>
<list id="l1" type="bullet">
<li>Observational evidence has highlighted similarities between physical pain and 'social pain' — the painful feelings associated with actual or potential damage to social bonds. Thus, experiences of social rejection or loss are often described with physical pain words ('hurt feelings' and 'broken heart'), and both physical and social pain are highly noxious experiences.</li>
<li>Research on the neurochemical substrates of physical and social pain has demonstrated that both rely on opioid processes. Thus, opiates, which are potent analgesics, have also been shown to reduce separation distress behaviours in animals.</li>
<li>Neuroimaging research has demonstrated that experiences of social exclusion predominantly activate the dorsal anterior cingulate cortex (dACC) and anterior insula (AI) — regions known to have a role in the distressing experience of physical pain.</li>
<li>In addition, several lines of research have shown that experiences of negative social evaluation, rejection from a romantic partner and bereavement also lead to activity in the dACC and AI. A few studies have also shown neural activity in regions associated with the sensory component of pain (posterior insula); additional research will be needed to determine the types of social pain that elicit sensory-related processing.</li>
<li>On the basis of the shared neural circuitry associated with physical and social pain, research has shown that individuals who are more sensitive to one kind of pain are also more sensitive to the other. Thus, greater physical pain experience or sensitivity is associated with greater social pain sensitivity (rejection sensitivity or anxious attachment).</li>
<li>Another consequence of a physical–social pain overlap is that factors that alter one type of pain have a similar effect on the other. For example, social support, which is known to reduce social pain, can also reduce physical pain, and Tylenol (paracetamol; Johnson and Johnson), which is known to reduce physical pain, can also reduce social pain.</li>
<li>On the basis of the role of the dACC and AI in responding to socially painful experience, these regions may be crucial for translating experiences of social disconnection into downstream physiological responses, which have implications for health. Indeed, the dACC and AI may have a mediating role in the links between social rejection and both inflammatory activity and depression.</li>
</list>
</p>
</execsumm>
<websumm type="regular">The experience of social rejection, exclusion or loss is often described as 'painful'. Naomi Eisenberger here outlines the evidence that the processing of these forms of 'social pain' share many underlying neural substrates with physical pain mechanisms and considers the implications of this convergent neural circuitry.</websumm>
<abs>
<p>Experiences of social rejection, exclusion or loss are generally considered to be some of the most 'painful' experiences that we endure. Indeed, many of us go to great lengths to avoid situations that may engender these experiences (such as public speaking). Why is it that these negative social experiences have such a profound effect on our emotional well-being? Emerging evidence suggests that experiences of social pain — the painful feelings associated with social disconnection — rely on some of the same neurobiological substrates that underlie experiences of physical pain. Understanding the ways in which physical and social pain overlap may provide new insights into the surprising relationship between these two types of experiences.</p>
</abs>
</fm>
<bdy>
<p>
<i>“... a sense of separation is a condition that makes being a mammal so painful.” Paul MacLean<bibr rid="b1"></bibr>
</i>
</p>
<p>Some of the most distressing experiences that we face involve the dissolution of our closest social bonds. Indeed, it is difficult to imagine a situation more upsetting than a relationship break-up or one more devastating than the loss of a loved one. In fact, according to one study, nearly three out of four people listed the loss of a close relationship (for example, through death or a relationship break-up) as the “single most negative emotional event” of their lives<bibr rid="b2"></bibr>
. Interestingly, some individuals have gone so far as to describe these experiences of social loss or social separation as being 'painful'<bibr rid="b1"></bibr>
. Given the intense emotional consequences of broken social bonds, one may ask why we react so strongly to the loss of our social ties.</p>
<p>Research over the past century, from social psychology to behavioural neuroscience, has demonstrated the importance of social bonds for mammalian well-being and survival<bibr rid="b3 b4 b5"></bibr>
. Early in life, many mammalian infants are completely dependent on caregivers, relying on them exclusively for nourishment, care and protection<bibr rid="b6"></bibr>
. Later on, connections to a social group aid survival through the shared responsibility for food acquisition, predator protection and care for offspring<bibr rid="b3"></bibr>
. Owing to this profound reliance on others, threats to social connection may be just as detrimental to survival as threats to basic physical safety and thus may be processed by some of the same underlying neural circuitry. Specifically, it has been proposed<bibr rid="b6 b7 b8 b9 b10"></bibr>
that experiences of 'social pain' — which is defined as the unpleasant experience that is associated with actual or potential damage to one's sense of social connection or social value (owing to social rejection, exclusion, negative social evaluation or loss) — may be processed by some of the same neural circuitry that processes physical pain (which is defined as the unpleasant experience that is associated with actual or potential tissue damage<bibr rid="b11"></bibr>
). Given the importance of social connection for survival, the definition of social pain used here is intentionally broad and includes multiple experiences that signal the loss, or potential loss, of social connection or social value, therefore signifying an increased survival risk. Thus, social pain includes experiences in which a relationship is threatened or lost because the self is devalued (rejection or negative evaluation), as well as experiences in which a relationship is lost but the self is not implicated (death of a loved one), as both of these experiences signify a loss of a protective social bond.</p>
<p>This Review highlights the growing body of literature suggesting a possible overlap in the neural circuitry underlying physical and social pain. This article first summarizes the observational evidence that provides the starting point for the hypothesis that negative social experiences are painful and considers why the physical pain signal may have been co-opted to prevent social disconnection. The neurochemical and neural substrates that process physical pain are then reviewed, and research showing that some of these substrates also process social pain is summarized. Next, some of the potentially surprising consequences of this shared neural circuitry are reviewed. Finally, the possible involvement of this neural circuitry in the link between social connection and both mental and physical health is discussed, as well as several remaining questions regarding the nature of social pain.</p>
<crosshd>Observational evidence of social pain</crosshd>
<p>
<i>“The intense, ever-increasing cathexis of the absent (lost) object generated by the child's unassuageable longing creates exactly the same economic conditions as does the pain-generated cathexis of an injured part of the body ...” Sigmund Freud<bibr rid="b12"></bibr>
</i>
</p>
<p>Several early psychological thinkers, dating at least back to Freud, have drawn analogies between physical and social pain. However, one need look (or listen) no further than to our everyday language to see how physical and social pain are similarly conceptualized. Individuals use the same words to describe instances of physical and social injury, complaining of 'broken bones' and 'broken hearts' or 'hurt muscles' and 'hurt feelings'. In fact, experiences of social rejection or exclusion have been shown to elicit a discrete category of affective responses termed 'hurt feelings', which are described in a manner reminiscent of physical pain (for example, a “cutting stab” or a “sinking inner pain”<bibr rid="b13"></bibr>
). Importantly, using physical pain words to describe experiences of social pain is a phenomenon common to many languages<bibr rid="b10"></bibr>
, suggesting a potentially universal overlap in the experience of physical and social pain.</p>
<p>Perhaps more convincing than a linguistic overlap, however, is the fact that experiences of social pain appear to be just as noxious and dreaded as experiences of physical pain. Suicide, one means to escape negative experience, is not only more prevalent in patients with chronic pain (in comparison to healthy controls)<bibr rid="b14"></bibr>
but is also more common in those suffering from social isolation or social loss<bibr rid="b15 b16"></bibr>
. Anxiety disorders, characterized by a heightened focus on possible harm and its avoidance, have been shown to be rooted in two fundamental types of concerns: concerns about the possibility of physical harm (and thus physical pain) and concerns about the possibility of social harm, including rejection or evaluation (and thus social pain)<bibr rid="b17"></bibr>
.</p>
<p>In addition, behavioural evidence suggests that, in a similar way to experiences of physical injury, experiences of social injury result in self-reported pain. People recalling prior episodes of social pain report that they were just as painful (using a pain rating scale) as prior episodes of physical pain<bibr rid="b18 b19"></bibr>
. Moreover, following the death of a loved one — arguably one of the most devastating forms of social pain — bereaved people report feeling intense psychological pain and often complain of somatic symptoms<bibr rid="b20 b21"></bibr>
.</p>
<p>Thus, there is considerable indirect evidence that social pain may be processed in a manner similar to physical pain. Considering the severe survival threat imposed by social disconnection, it makes sense that threats to social connection may utilize the same pain signal that signifies threats to the physical body. The pain signal interrupts ongoing behaviour; promotes quick responses aimed at terminating, reducing or escaping the source of threat; and serves as a punishment-based reinforcer to teach organisms to avoid threatening stimuli in the future<bibr rid="b22"></bibr>
. Not surprisingly, individuals born without the ability to feel pain die significantly earlier<bibr rid="b23"></bibr>
. Such a salient signal could be invaluable in signalling, terminating and later motivating the avoidance of threats to social connection as well. Consequently, the pain mechanisms involved in preventing physical harm may have been co-opted to prevent social separation<bibr rid="b6"></bibr>
, thereby increasing survival likelihood.</p>
<crosshd>Neurochemical substrates of social pain</crosshd>
<p>Perhaps the earliest evidence for an overlap in the systems underlying physical and social pain was the demonstration that opiates, best known for their pain-relieving effects, also reduce separation distress behaviours in non-human mammals6. Opiates, such as morphine, have well-documented analgesic (as well as euphoric) effects<bibr rid="b24"></bibr>
and are part of the first line of defence for ameliorating severe physical pain. The pain-relieving effects of opiates appear to be mediated by the mu-opioid receptor, as mice lacking the mu-opioid receptor gene (<i>OPRM1</i>
) are unresponsive to the pain-relieving effects of morphine and show increased sensitivity to painful stimuli<bibr rid="b25"></bibr>
.</p>
<p>In addition to their pain-relieving effects, opiates reduce behaviours associated with the distress of social separation, such as <deflistr rid="df1">isolation calls</deflistr>
, a type of distress vocalization emitted by infants upon maternal separation. Across multiple species, low, non-sedative doses of morphine, an opioid receptor agonist, reduce isolation calls in response to maternal separation, whereas naloxone, an opioid receptor antagonist, increases isolation calls<bibr rid="b26 b27 b28 b29"></bibr>
. Consistent with this evidence, mice lacking <i>OPRM1</i>
show significant deficits in attachment behaviours, including reductions in isolation calls following mother–infant separation<bibr rid="b30"></bibr>
. In these mice pups, the lack of mu-opioid signalling may reduce the rewarding experience associated with maternal interaction, resulting in little distress following maternal separation and thus fewer isolation calls. Opioid-related processes have also been shown to have a role in social affiliative processes. Opioid receptor agonists reduce time spent in close proximity with con-specifics<bibr rid="b26 b27 b31"></bibr>
, presumably because the opioids act as a substitute for the rewarding experience of social connection. Conversely, opioid receptor antagonists increase attempts at social connection through grooming<bibr rid="b32"></bibr>
, presumably in order to increase the experience of reward (through social means) that is being reduced by opioid receptor antagonists.</p>
<p>On the basis of these findings, it has been suggested that the social attachment system may have piggybacked onto the opioid substrates of the physical pain system to maintain proximity with others, eliciting distress upon separation (through low opioid receptor activity) and comfort upon reunion (through high opioid receptor activity)6. Indeed, given the robust effects of opiates on social attachment processes, some have drawn parallels between the nature of opiate addiction and social bonding, noting that both involve the development of strong attachments to a particular object (opiates or a loved one) and intense distress (including crying, irritability, depression and insomnia) to its withdrawal<bibr rid="b6 b26"></bibr>
. In sum, endogenous brain opioid systems, which are known to regulate the distress of physical pain, may be one of the neurochemical regulators of the distress associated with social separation, as well as the pleasure associated with social connection. Other neurochemical systems are likely to be involved as well<bibr rid="b6"></bibr>
.</p>
<crosshd>Neural substrates of social pain</crosshd>
<p>In addition to shared opioid substrates, experiences of social and physical pain rely on shared neural circuitry. To better understand the ways in which social pain might utilize physical pain-related neural circuitry, it is important to first elaborate on two components of the physical pain experience and their underlying neural substrates. Although physical pain 'feels like' a single, unified experience, pain researchers have subdivided pain into two dissociable (although highly interrelated) components: a sensory component involved in coding for stimulus localization (for example, arm versus leg), quality discrimination (such as stinging or burning) and intensity discrimination (the objective strength of the nociceptive signal); and an affective component associated with the unpleasant or distressing experience of pain (such as the subjective bothersomeness of the nociceptive signal) and the drive to terminate the stimulus causing this experience<bibr rid="b33 b34"></bibr>
.</p>
<p>Given the significance of the affective component of pain for signalling an aversive state and motivating behaviour to terminate, reduce or escape the source of painful stimulation<bibr rid="b22 b34"></bibr>
, it has been hypothesized that experiences of social pain rely on brain regions associated with the affective component of pain in order to warn against and prevent the dangers of social harm<bibr rid="b8 b9 b10"></bibr>
. Sensory-related regions may also be involved, as 'somatic' symptoms are often reported following social pain<bibr rid="b13 b20"></bibr>
. However, the affective component of pain may be more directly implicated in social pain experience. In agreement with this assertion, a patient with congenital insensitivity to physical pain — which involves an impairment of the sensory (but not affective) component of pain — reported feeling pain for the first time shortly after the unexpected death of a younger sibling<bibr rid="b35"></bibr>
, suggesting that painful experience can arise from social loss even in the absence of sensory-related processing ability. Hence, the affective component of pain may be more crucial for experiencing the pain associated with negative social experiences.</p>
<p><bi>Neural substrates of physical pain</bi>
. The affective component of physical pain is processed cortically by the dorsal anterior cingulate cortex (dACC; defined here as Brodmann areas 24 and 32, superior and posterior to the genu of the corpus callosum) and the anterior insula (AI)<bibr rid="b33 b34"></bibr>
(<figr rid="f1">Fig. 1</figr>
). Following cingulotomy for the treatment of chronic pain, in which a portion of the dACC is surgically lesioned<bibr rid="b36"></bibr>
, patients are still able to localize pain sensations but report that the 'pain no longer bothers them'<bibr rid="b37"></bibr>
, highlighting a unique role for this region in the distressing experience of physical pain. Consistent with this, lesions to this region in animals result in reductions in affective pain responses (pain-induced conditioned place avoidance)<bibr rid="b38"></bibr>
and impairments in learning to avoid noxious stimuli<bibr rid="b39"></bibr>
. Insular lesions produce similar outcomes, leading to pain asymbolia, a condition in which pain is perceived but does not cause distress or suffering<bibr rid="b40"></bibr>
, or other disruptions of pain affect<bibr rid="b41"></bibr>
. Neuroimaging studies largely echo these neuropsychological findings. Hypnotic suggestions to increase the felt unpleasantness of pain lead to specific increases in dACC activity without altering activity in the somatosensory cortex, a sensory-related neural region<bibr rid="b42"></bibr>
. Moreover, there is a direct correspondence between the magnitude of felt pain unpleasantness and activity in the dACC and AI<bibr rid="b43 b44 b45 b46 b47"></bibr>
. Finally, given the profound capacity of opiates to reduce the affective component of pain<bibr rid="b24"></bibr>
, it is not surprising that both the dACC and AI have some of the highest densities of mu-opioid receptors in the central nervous system<bibr rid="b48 b49"></bibr>
.</p>
<p>The sensory component of pain, however, is largely processed by the primary and secondary somatosensory cortices (S1 and S2, respectively)<bibr rid="b50 b51 b52"></bibr>
, as well as the posterior insula (PI)<bibr rid="b44"></bibr>
(<figr rid="f1">Fig. 1</figr>
). Thus, patients with lesions to one or a combination of S1, S2 and PI show deficits in processing pain sensations as well as other sensory information (such as temperature discrimination)<bibr rid="b41 b53 b54"></bibr>
, but in some cases still describe the sensations as unpleasant, suggesting that the affective component of pain is intact<bibr rid="b54"></bibr>
. Similarly, neuroimaging studies have shown that manipulations that augment the felt intensity of painful stimulation activate S1 as well as S2 and/or PI<bibr rid="b44 b45 b51 b55"></bibr>
. Using these pain-related neural substrates as a framework, animal and human research has demonstrated that some of the same regions — in particular, the affective neural regions — contribute to social pain.</p>
<p><bi>Neural substrates of social pain in animals</bi>
. Although animal studies cannot provide direct information regarding the experiential correlates of threats to social bonds, they provide important information about the neural regions associated with social separation-related behaviours. Two behaviours intimately linked with social separation in non-human mammals are isolation calls and maternal behaviour (including retrieving, crouching over and licking pups), both aimed at reducing mother–infant separation and thereby ensuring infant survival. Both of these behaviours seem to rely, in part, on neural activity in the dACC or more broadly in the ACC.</p>
<p>The ACC is well-positioned to contribute to the distress of social separation and behaviours aimed at reducing social separation. This region has no counterpart in the reptilian brain and thus, along with attachment-related and maternal behaviour, may distinguish the evolutionary transition from reptiles to mammals (and birds)<bibr rid="b1 b56"></bibr>
. Indeed, the thalamocingulate division of the brain — which includes the cingulate cortex and connected medial thalamic nuclei — is not only involved in mammalian attachment-related processes but is also directly involved in the affective component of physical pain<bibr rid="b33 b34"></bibr>
, again highlighting the part that pain processes may play in maintaining social attachments.</p>
<p>As evidence for the role of the ACC in isolation calls, lesioning the ACC (dorsal and/or ventral to the genu) reduces these distress vocalizations<bibr rid="b57 b58"></bibr>
, whereas electrically stimulating this region or its afferent inputs (from the mediodorsal thalamus) leads to the spontaneous production of these distress vocalizations<bibr rid="b26 b59 b60"></bibr>
. Interestingly, lesions to the ACC (both dorsal and ventral to the genu) have also been shown to lead to reductions in social interactions and time spent in proximity with other animals<bibr rid="b58"></bibr>
, suggesting that this region may be crucial for registering the distress associated with social separation and motivating attempts at social reconnection.</p>
<p>In addition to isolation calls, the cingulate cortex has been shown to contribute to maternal behaviour aimed at pup retrieval (returning pups to the nest). For example, hamsters with lesions to the cingulate cortex retain most species-typical forms of behaviour but show severe deficits in maternal behaviour, failing completely in pup retrieval<bibr rid="b61"></bibr>
. Mice and rats with cingulate lesions are similarly impaired<bibr rid="b62 b63"></bibr>
. Together, these studies demonstrate the critical role of the cingulate cortex generally, and the ACC more specifically, in behaviours that promote social bonds in non-human mammals.</p>
<p><bi>Neural substrates of social pain in humans</bi>
. Although there have been few studies examining the effect of neural lesions on social behaviour in humans, some studies support the idea that the dACC contributes to social motivation. Following cingulotomy, patients show decrements in self-consciousness<bibr rid="b64 b65"></bibr>
as well as a reduced concern about the opinions or social judgements of others<bibr rid="b65"></bibr>
. To date, however, no studies have investigated the effect of dACC lesions on sensitivity to discrete types of socially painful experiences (such as social rejection). Instead, the majority of evidence for the role of the dACC and AI in social pain in humans comes from neuroimaging studies.</p>
<p>The first study to examine the neural substrates of social pain focused on neural responses to social exclusion7. In this study, participants believed they were playing a virtual game of catch, called '<deflistr rid="df2">Cyberball</deflistr>
,' with two other individuals over the Internet (<figr rid="f2">Fig. 2a</figr>
). In reality, the other players were computer-controlled and the game was preset so that participants were first included in the game and then excluded when the two players stopped throwing them the ball. Notably, in response to social exclusion versus inclusion, participants showed increased activation in the dACC and AI (<figr rid="f2">Fig. 2b</figr>
). Moreover, greater activity in the dACC was associated with greater feelings of social distress (for example, “I felt rejected”) in response to social exclusion (<figr rid="f2">Fig. 2c</figr>
).</p>
<p>Several additional studies have used the Cyberball task to examine the neural correlates of social exclusion from strangers. Many of these studies have shown increased activity in the dACC and/or AI in response to social exclusion<bibr rid="b7 b66 b67 b68 b69 b70 b71 b72 b73 b74 b75"></bibr>
(<bxr rid="bx1">Box 1</bxr>
) and/or a positive correlation between neural activity in these regions and self-reported feelings of social distress in response to exclusion<bibr rid="b7 b67 b69 b70 b73 b76 b77 b78"></bibr>
(<bxr rid="bx2">Box 2</bxr>
). Moreover, factors typically associated with a greater sensitivity to social exclusion, such as low self-esteem<bibr rid="b79"></bibr>
, <deflistr rid="df3">anxious attachment</deflistr>
<bibr rid="b77"></bibr>
, interpersonal sensitivity<bibr rid="b80"></bibr>
or a tendency to feel socially disconnected on a daily basis<bibr rid="b81"></bibr>
, have been shown to be associated with increased neural activity in the dACC and/or AI in response to social exclusion. Likewise, factors typically associated with a reduced sensitivity to social exclusion, such as social support<bibr rid="b67 b78"></bibr>
or <deflistr rid="df4">avoidant attachment</deflistr>
<bibr rid="b77"></bibr>
, have been shown to be associated with reduced activity in the dACC and/or AI.</p>
<p>In addition, some Cyberball studies have found increased activity in the subgenual ACC (subACC) in response to social exclusion<bibr rid="b68 b71 b72 b73 b74 b75 b82"></bibr>
. The subACC is a region implicated in affective processes<bibr rid="b83"></bibr>
but not, typically, in physical pain. Although some studies have shown that greater activity in this region correlates with greater social distress<bibr rid="b73 b76"></bibr>
, others have shown increased activity in this region in response to social acceptance rather than social rejection<bibr rid="b84"></bibr>
. Moreover, many studies that find subACC activity have not examined correlations between self-reported distress and neural activity, and so it is not yet clear how this region contributes to the experience of social exclusion. Interestingly, as shown in <bxr rid="bx1">Box 1</bxr>
, subACC activity is more likely to appear in Cyberball studies that include adolescent participants. Indeed, some work has shown that subACC responses to exclusion are higher in adolescents and decrease with increasing age<bibr rid="b72"></bibr>
. Thus, it is possible that subACC, rather than dACC, activity in response to social exclusion is indicative of an earlier developmental processing of exclusion. This is consistent with models that have suggested differential development in dorsal versus ventral emotion-processing systems and fits with prior work showing that dACC responses to threatening stimuli do not become evident until later in development<bibr rid="b85"></bibr>
. Future studies, however, are needed to further examine the role of the subACC in social pain processes.</p>
<p>Studies of another form of social pain — feelings associated with being socially evaluated (which signals the possibility of being rejected by others) — have yielded findings that are similar to those from studies of exclusion. Thus, during a social-evaluative task, in which participants prepared a speech that would later be evaluated by a panel, participants showed increased activity in the dACC<bibr rid="b86"></bibr>
. Similarly, in response to being evaluated on a personal interview, feeling worse in response to negative social evaluative feedback (“you are boring”) was associated with greater activity in the dACC and AI<bibr rid="b87"></bibr>
. Moreover, when participants were made to evaluate themselves negatively, through an unfavourable comparison with a superior peer, they showed increased activity in the dACC<bibr rid="b88"></bibr>
.</p>
<p>Even subtle rejection cues that do not necessarily elicit feelings of social pain can activate some of these pain-related neural regions, perhaps attesting to the salience of social disconnection among humans. Thus, viewing rejection-themed paintings (by Edward Hopper) led to increased activity in the dACC and AI compared to viewing acceptance-themed paintings (by August Renoir)<bibr rid="b89"></bibr>
. Also, viewing (non-personal) videos of individuals displaying disapproving facial expressions led to increased activity in the dACC for those more sensitive to rejection<bibr rid="b90"></bibr>
.</p>
<p>Although most studies examining social pain have focused on interactions with strangers, a few studies have examined the neural correlates of social rejection from a close other, which is likely to be a more socially painful experience. In these studies, participants who recently experienced an unwanted romantic relationship break-up were asked to view pictures of their ex-partner and think about the rejection experience<bibr rid="b91 b92"></bibr>
. In response to thinking about the ex-relationship partner versus a friend, participants showed increased activity in the dACC and AI, which are affective pain-related regions, as well as in the PI<bibr rid="b91 b92"></bibr>
and, in one study<bibr rid="b92"></bibr>
, the S2, which are regions associated with the sensory component of pain. In addition, one study<bibr rid="b92"></bibr>
included a physical pain task alongside the social pain task and found overlapping neural activity to physical and social pain in each of these regions, again lending support to the idea that physical and social pain rely on shared neural circuitry.</p>
<p>Finally, although less work to date has focused on the neural correlates of social loss (such as the death of a close other), several studies have demonstrated that thinking about a lost loved one can activate affective pain-related neural regions. Thus, viewing pictures of a deceased loved one (versus a stranger) led to increased activity in the dACC and AI<bibr rid="b93 b94"></bibr>
. Moreover, females who lost an unborn child (versus those who delivered a healthy baby) showed greater activity in the posterior dACC when viewing images of smiling baby faces<bibr rid="b95"></bibr>
.</p>
<p>In sum, studies examining various situations that are likely to produce social pain — ranging from social exclusion to the loss of a loved one — have shown activity in several pain-related neural regions. Although the most commonly activated regions, particularly for adults, are the dACC and AI (<bxr rid="bx1">Box 1</bxr>
) — which are regions involved in the affective component of physical pain — some studies, such as those examining romantic rejection, have also shown activity in sensory-related neural regions (PI). It has been suggested that this sensory-related neural activity is due to the more intense experience of social pain that results from rejection from a close other<bibr rid="b92"></bibr>
. Although this account seems plausible, it is at odds with the fact that studies of social loss or bereavement — some of the most intense experiences of social pain — have not typically yielded these types of activations. Still, it is possible that sensory-related neural regions are crucial for experiences of social pain that involve the devaluation of the self by others (being rejected) rather than experiences of social pain that involve the termination of a relationship but do not imply that the self is devalued (bereavement). Future work will be needed to fully examine whether, and under what circumstances, sensory regions are implicated in social pain processing. In addition, it will be important for future research to continue to examine how self-reported experience in response to socially painful events correlates with observed neural activity. Although not a perfect solution, self-reported experiences of distress may provide additional leverage in trying to determine whether the neural regions observed in response to socially painful events are involved in processing distress or in some other co-occurring process, such as the attempted regulation of this distress. Finally, additional research will be needed to determine the precise types of inputs to which the dACC and AI respond, as these regions have also been implicated in other types of psychological processes (<bxr rid="bx3">Box 3</bxr>
).</p>
<crosshd>Consequences of shared pain circuitry</crosshd>
<p>One of the implications of this shared neural circuitry is that there should be predictable consequences of a physical–social pain overlap. Two hypothesized consequences are that individuals who are dispositionally more sensitive to one kind of pain should also be more sensitive to the other and that factors that increase or decrease one kind of pain should influence the other kind of pain in a similar manner (<figr rid="f3">Fig. 3</figr>
).</p>
<p><bi>Individual differences</bi>
. Although shared sensitivity to physical and social pain is not an obvious hypothesis, several lines of clinical research support this idea. Patients with chronic pain, who experience more physical pain, are also more sensitive to social pain than control subjects, as evidenced by greater fear and avoidance of social interactions and a greater incidence of social phobia<bibr rid="b96"></bibr>
. Moreover, higher levels of daily pain affect are associated with higher levels of anxious attachment or a greater concern about being rejected by others<bibr rid="b97"></bibr>
. Similarly, a large amount of work has demonstrated that those with a heightened sensitivity to social pain — such as those with an anxious attachment style or high levels of <deflistr rid="df5">rejection sensitivity</deflistr>
— report more somatic symptoms overall, including pain, than those with secure attachment styles<bibr rid="b98 b99 b100"></bibr>
.</p>
<p>Experimental work in healthy controls also supports this overlap. Individuals who are more sensitive to physical pain (assessed through experimental pain stimulation) also report higher levels of social pain in response to social exclusion<bibr rid="b101"></bibr>
. In addition, participants with the rare form of the <i>OPRM1</i>
polymorphism, which has previously been linked with increased physical pain sensitivity<bibr rid="b102"></bibr>
, demonstrate higher levels of rejection sensitivity and show greater activity in the dACC and AI in response to an experimental episode of social exclusion<bibr rid="b103"></bibr>
.</p>
<p><bi>Factors that enhance or reduce pain</bi>
. A second consequence of a physical–social pain overlap is that factors that increase or decrease one kind of pain should have a similar effect on the other. For example, factors that typically increase social pain — such as social trauma, failure or exclusion — should also increase sensitivity to physical pain. Indeed, although there are some inconsistencies, several studies support this premise. Patients with somatoform pain disorder and fibromyalgia, who experience pain with no medical explanation, also report greater levels of early social trauma (including emotional abuse or family conflict)<bibr rid="b104"></bibr>
, suggesting a potential link between these early socially painful experiences and later reports of physical pain.</p>
<p>In addition, experiences of both failure and social exclusion are related to increased physical pain sensitivity. Experimental manipulations of failure (which may convey that one would not be liked or accepted by others) have been shown to increase pain ratings to a cold-pressor task, a painful task that involves immersing one's hand in ice water for extended periods of time<bibr rid="b105 b106"></bibr>
. Similarly, experiences of social exclusion have been shown to increase physical pain sensitivity<bibr rid="b107"></bibr>
, and those who report feeling more rejected in response to exclusion report higher physical pain ratings in response to a pain stimulus delivered at the end of the exclusion episode<bibr rid="b101"></bibr>
.</p>
<p>However, some studies have shown opposite effects. Paralleling the finding that endogenous analgesic systems can be triggered by the presence of physical threats<bibr rid="b108 b109"></bibr>
, some work has shown that analgesic responses can also result from the presence of social threats. For example, being told that one will be alone in the future has been shown to reduce physical pain sensitivity<bibr rid="b107 b110"></bibr>
. Although it is not clear why social rejection and/or exclusion sometimes leads to increased physical pain and sometimes to reduced physical pain, these differences are not incompatible with the physical pain literature, which has shown both hyperalgesia and analgesia following nociceptive stimulation<bibr rid="b109 b111 b112"></bibr>
. One possibility is that these differential pain outcomes may be due to the severity of the threatening stimulus<bibr rid="b107"></bibr>
. In line with this possibility, it has been shown that exposure to a severe social injury (such as being told that one will be alone in the future) reduces physical pain sensitivity, whereas exposure to a less severe social injury (Cyberball exclusion) increases physical pain sensitivity<bibr rid="b107"></bibr>
. Additional work will be needed to determine the precise conditions under which specific types of social pain increase or decrease physical pain, as well as how they are manifested neurobiologically.</p>
<p>More consistent findings have emerged from studies examining whether factors that typically increase physical pain also increase social pain. For example, it has long been noted that, in children, factors that increase the experience of physical pain (such as injury or sickness) also increase the child's sensitivity to the whereabouts of their caregiver, leading to more frequent experiences of distress upon separation5. Similarly, in adults, inflammatory activity, which is known to increase physical pain<bibr rid="b113"></bibr>
, can also increase social pain, leading to greater feelings of social disconnection<bibr rid="b114"></bibr>
. Moreover, greater inflammatory activity in response to an inflammatory challenge has been shown to be associated with greater activity in the dACC and AI in response to an experimental episode of social exclusion<bibr rid="b115"></bibr>
. Finally, although somewhat surprising, recent work has shown that experiences of physical pain can directly increase feelings of social exclusion even in the absence of being socially excluded; participants exposed to painfully cold water (versus warm water) reported feeling more ignored and excluded<bibr rid="b19"></bibr>
.</p>
<p>In addition to pain-enhancing effects, factors that reduce one type of painful experience should reduce the other as well. Along these lines, considerable research has shown that social support, typically associated with reduced perceptions of social harm, is related to reduced physical pain. Correlational research has demonstrated that individuals with more social support experience less pain across a number of different domains<bibr rid="b116 b117"></bibr>
. In addition, experimental work has demonstrated a causal effect of social support on pain<bibr rid="b118 b119 b120"></bibr>
. For example, viewing a picture or holding the hand of a loved one (relative to a stranger or object) leads to reductions in self-reported pain<bibr rid="b118 b119 b120"></bibr>
, as well as reductions in pain-related neural activity (in the dACC and AI)<bibr rid="b119 b120"></bibr>
. Thus, the perception or presence of social support, presumably indicative of a lesser likelihood of social harm, appears to reduce physical pain as well.</p>
<p>Finally, factors that are known to reduce physical pain should also reduce social pain. In addition to research showing that opiates can reduce social as well as physical pain6, other analgesic drugs typically used to manage physical pain have also been shown to reduce social pain. Thus, in a double-blind, placebo-controlled study, taking Tylenol (paracetamol; Johnson and Johnson), an over-the-counter pain reliever, for a 2-week period was shown to reduce daily self-reported hurt feelings and to reduce dACC and AI activity in response to an experimental episode of social exclusion<bibr rid="b66"></bibr>
.</p>
<p>Together, these findings lend additional support to the hypothesis that physical and social pain processes overlap by highlighting some of the, sometimes surprising, consequences of such an overlap. Although it might seem objectively odd that social support would lessen physical pain or that a physical pain-reliever would ameliorate social pain, couching these findings within the larger framework of an overlap in the systems underlying physical and social pain helps to make sense of these relationships. Of course, experiences of physical and social pain are not identical and undoubtedly rely on distinct neural and neurobiological underpinnings as well. It will be crucial for future research to examine the boundary conditions for the extent of the physical–social pain overlap (<bxr rid="bx4">Box 4</bxr>
).</p>
<crosshd>dACC and AI in health</crosshd>
<p>In addition to being involved in social pain-related responding, the dACC and AI may have a key role in the relationship between experiences of social disconnection and health. Considerable research has shown links between social disconnection and health: for example, those higher in objective or subjective social disconnection (that is, those who have fewer social ties or greater perceived social isolation) have a greater risk of mortality and a greater incidence of physical health problems (such as coronary heart disease) and negative mental health-related outcomes (such as depression)<bibr rid="b121 b122"></bibr>
. Given that the dACC and AI are involved in responding to social disconnection, these regions may have a role in translating experiences of social disconnection into downstream physiological responses — such as heightened inflammatory activity, the immune system's first line of defence against foreign agents and infection — which have health implications. Indeed, several lines of research support this hypothesis.</p>
<p>Experiences of social disconnection have been shown to be associated with increases in various indices of inflammatory activity. Lonely individuals, who perceive greater levels of social disconnection on a daily basis, show an upregulation of pro-inflammatory response genes, which may contribute to their increased risk of inflammatory disease<bibr rid="b123"></bibr>
. Social-evaluative stressors that involve the possibility of social rejection have been shown to increase pro-inflammatory activity, and this effect is heightened for those who feel more evaluated<bibr rid="b124"></bibr>
. Finally, in guinea pigs, social (maternal) separation has been shown to lead to increases in the levels of pro-inflammatory cytokines<bibr rid="b125"></bibr>
.</p>
<p>In addition to being involved in responding to perceived social disconnection, the dACC and AI may contribute to inflammatory activity through their role in sympathetic responses, which have been shown to increase inflammatory activity<bibr rid="b126 b127"></bibr>
. Thus, activity in both the dACC and AI in response to effortful or socially stressful tasks has been shown to correlate with increases in measures of sympathetic activity<bibr rid="b86 b128 b129"></bibr>
. Moreover, the dACC has been posited to play a part in the generation of these peripheral sympathetic responses, as patients with dACC lesions do not show the expected increase in sympathetic responses to mental stress<bibr rid="b129"></bibr>
. Building on this evidence, a recent study demonstrated that greater activity in both the dACC and AI in response to social exclusion was associated with greater increases in pro-inflammatory cytokines in response to a separate social stressor<bibr rid="b130"></bibr>
. Thus, these regions may have an important role in translating experiences of social disconnection into inflammatory-related responses.</p>
<p>Finally, inflammatory-related processes are known to relate to negative physical and mental health outcomes. Increased inflammatory activity has been linked with several chronic diseases of ageing (including cardiovascular disease and some types of cancer)<bibr rid="b131"></bibr>
. In addition, considerable research has implicated enhanced inflammatory responding in depression. Depressed individuals show increased levels of pro-inflammatory cytokines<bibr rid="b132"></bibr>
, and healthy individuals exposed to an experimental inflammatory challenge show an increase in depressive symptoms<bibr rid="b115 b133"></bibr>
.</p>
<p>Triangulating across these various lines of evidence suggests that the dACC and AI may be important mediators of the links between experiences of social disconnection and both physical and mental health<bibr rid="b134"></bibr>
. People who are more sensitive to experiences of social disconnection may be more likely to activate the dACC and AI, which may be associated with greater increases in sympathetic and inflammatory activity, and such individuals may therefore be at greater risk of developing inflammatory-related diseases and depression.</p>
<crosshd>Conclusions</crosshd>
<p>In summary, evidence from animals and humans supports the hypothesis that there is an overlap in the neurobiological underpinnings of physical and social pain. This finding fits with other work showing that certain, basic neural systems (those involved in pain and reward) may have been co-opted to support more complex social experiences<bibr rid="b135 b136 b137 b138"></bibr>
. Focusing on the overlap between physical and social pain helps to make sense of several surprising findings, such as the reduction in physical pain that occurs in the presence of social support and the increase in feelings of social disconnection that accompanies physical pain. A better understanding of this overlap may provide a new way of thinking about the factors that contribute to physical pain and the methods that could be used to treat experiences of social pain or certain conditions, such as depression, that have strong links with both types of painful experience<bibr rid="b16"></bibr>
.</p>
<p>Nevertheless, several questions remain about the nature of the physical–social pain overlap. First, although the dACC and AI have been shown to activate in response to both physical and social pain, these two regions are also activated in response to many tasks that generate negative affect. Although it is certainly the case that some of these affective tasks induce negative affect through negative social experiences, not all of them do. Thus, it is possible that these regions have a broader role as a neural alarm system (<bxr rid="bx3">Box 3</bxr>
), which triggers affective, behavioural and autonomic responses8 to various types of survival relevant threats — with indicators of social or physical harm being some salient examples. Further research is needed to determine the precise types of survival-relevant threats to which these regions are responsive.</p>
<p>Another remaining issue is whether experiences of social pain activate sensory, as well as affective, pain-related neural regions. Although most of the neuroimaging literature has shown that experiences of rejection or loss activate affective pain-related regions, some studies have also shown sensory-related neural activity in response to rejection. Given that socially painful experiences are sometimes described as being localized to a certain part of the body ('heartache'), it will be important to better understand how, and in what situations, social pain activates sensory-related neural regions. Furthermore, it will be important to identify the pathways whereby socially painful experiences become represented in or localized to the body.</p>
<p>More generally, the findings reviewed here highlight the counterintuitive nature of pain. We typically reify physical pain as 'real' pain and often dismiss social pain as 'psychological', but the connection between the two kinds of pain suggests that each of these lay theories is only half right. Physical pain is a deeply psychological phenomenon that can be altered by expectations, mood and attention. Likewise, social pain is a deeply biological phenomenon that has been built into our brains and bodies over millions of years of mammalian evolution because of the crucial part it plays in our survival. A better understanding of the commonalities between these two types of painful experience may provide greater insight into the underlying nature of each.</p>
</bdy>
<bm>
<objects>
<deflist colwd="1 5" id="df1" sepch=" " type="unenum">
<term>Isolation calls</term>
<defn>
<p>A type of distress vocalization produced by infant mammals in response to separation from a caregiver. These vocalizations function to facilitate reunion with the caregiver.</p>
</defn>
</deflist>
<deflist colwd="1 5" id="df2" sepch=" " type="unenum">
<term>Cyberball</term>
<defn>
<p>A virtual ball-tossing game that can be used to induce social inclusion or exclusion, depending on the behaviour of the other virtual players (whether they toss the ball to the participant).</p>
</defn>
</deflist>
<deflist colwd="1 5" id="df3" sepch=" " type="unenum">
<term>Anxious attachment</term>
<defn>
<p>A style of relating to close others characterized by a heightened concern about being abandoned by close others and therefore an exaggerated sensitivity to signs of acceptance or rejection by others.</p>
</defn>
</deflist>
<deflist colwd="1 5" id="df4" sepch=" " type="unenum">
<term>Avoidant attachment</term>
<defn>
<p>A style of relating to close others characterized by an avoidance of seeking out support or closeness from others.</p>
</defn>
</deflist>
<deflist colwd="1 5" id="df5" sepch=" " type="unenum">
<term>Rejection sensitivity</term>
<defn>
<p>The tendency to anxiously expect, readily perceive and intensely react to experiences of social rejection.</p>
</defn>
</deflist>
<linkgrp>
<linkset name="FURTHER INFORMATION">
<weblink url="http://sanlab.psych.ucla.edu/">Naomi Eisenberger's homepage</weblink>
</linkset>
</linkgrp>
<fig entref="figf1" id="f1" type="bmp">
<!--nrn3231-f1-->
<figtl>Cortical substrates of the affective and sensory components of physical pain.</figtl>
<caption>
<p>The medial view on the left shows the dorsal anterior cingulate cortex (dACC). The lateral view on the right shows the primary somatosenory cortex (S1) on the outer surface of the brain, the secondary somatosensory cortex (S2) on the edge of the cut-out of the brain and the anterior insula (AI) and posterior insula (PI) in the middle of the cut-out of the brain. Sensory components are shown in green and affective components in red.</p>
</caption>
</fig>
<fig entref="figf2" id="f2" type="bmp">
<!--nrn3231-f2-->
<figtl>Neural responses to social exclusion.</figtl>
<caption>
<p><b>a</b>
| Pictorial depiction of what participants see during the inclusion and exclusion rounds of the Cyberball game. On the left, the participant, depicted by the hand at the bottom of each screenshot, is included in the ball-tossing game with the two other players, depicted in the upper left and right hand corners of the screenshots. On the right, the participant is excluded when the two other players stop throwing the ball to the participant. <b>b</b>
| Activity in the dorsal anterior cingulate cortex (dACC; coordinates: −8,20,40) and anterior insula (AI; coordinates: 42,16,1) that was greater during social exclusion than during social inclusion<bibr rid="b7"></bibr>
. <b>c</b>
| Activity in the dACC that correlated positively with self-reported distress in response to social exclusion<bibr rid="b7"></bibr>
. Figure modified, with permission, from Ref. <bibrinl rid="b8">8</bibrinl>
© (2004) Elsevier.</p>
</caption>
</fig>
<fig entref="figf3" id="f3" type="bmp">
<!--nrn3231-f3-->
<figtl>Model depicting the functional consequences of a physical–social pain overlap.</figtl>
<caption>
<p><b>a</b>
| To the extent that physical and social pain rely on shared neural substrates (dorsal anterior cingulate cortex, (dACC) and anterior insula, (AI)), there should be trait and state consequences. <b>b</b>
| The trait consequences of a physical–social pain overlap are that individual differences in sensitivity to one kind of pain should relate to individual differences in sensitivity to the other. The graph here shows the forms of social pain sensitivity that have been associated with physical pain sensitivity. <b>c</b>
| The state consequences of a physical–social pain overlap are that factors that increase or decrease one kind of pain should affect the other in a similar manner. The box here lists the factors that are typically associated with altering one kind of pain (for example, Tylenol typically reduces physical pain) and have been shown to have the same effect on the other kind of pain (for example, Tylenol can also reduce social pain). Figure modified, with permission, from Ref. <bibrinl rid="b148">148</bibrinl>
© (2012) Wolters Kluwer Health.</p>
</caption>
</fig>
<bx id="bx1" placement="external" type="reg">
<bxtitle>Box 1 | Summary of neural activations in social pain studies</bxtitle>
<p>To identify the neural regions most frequently activated in response to social pain, studies examining neural responses to social exclusion (using the Cyberball method), social evaluation, rejection-themed images, romantic rejection and bereavement were reviewed. It is important to note that this was not a complete meta-analysis and, as such, no efforts were made to contact authors to identify unpublished null findings. The table illustrates the pattern of neural activity observed in response to various social pain tasks in several pain-related regions, including the dorsal anterior cingulate cortex (dACC), anterior insula (AI), thalamus (Thal), primary somatosensory cortex (S1), secondary somatosensory cortex (S2), posterior insula (PI) and periaqueductal grey (PAG), as well as the subgenual ACC (subACC; as this region is activated in some studies). Notably, dACC and AI activations were each observed in 67% of the 24 studies reviewed. Compared to these affective pain-related neural regions, sensory-related neural regions were not as consistently activated (Thal (13%); S1 (0%); S2 (4%); PI (25%)). The subACC was observed in 29% of these studies, all of which used the Cyberball methodology. Interestingly, 71% of the studies that showed subACC activation included adolescent participants; thus, it is possible that subACC activity to exclusion is more prevalent in developing samples. Indeed, when assessing only studies of adult participants, the dACC and AI were activated in 74% and 63% of the studies, respectively, whereas the subACC was activated in 100% of the studies that included adolescent participants.<illusr align="right" rid="i1"></illusr>
</p>
</bx>
<bx id="bx2" placement="external" type="reg">
<bxtitle>Box 2 | Correlations between neural activity and self-reported distress in response to social pain</bxtitle>
<p>In addition to identifying the neural regions that show activity in response to socially painful events, it is important to explore how neural activity in these regions correlates with self-reported negative experience in response to these events. This is important, in part, because neural activity in response to a socially painful event could be indicative of several different responses, including negative affect or attempts at regulating negative affect (“I don't care what those people think about me anyway”). Examining correlations between neural responses to social pain and self-reported negative affect may provide some clues about whether the activated neural regions are involved in the negative experience associated with social pain. The table highlights the neural regions that correlate with self-reported social distress in response to certain tasks. Most of the studies that examine self-reported social distress used the Cyberball methodology and asked subjects to rate how they felt in response to being socially excluded (using items such as: “I felt rejected”, “I felt meaningless” or “I felt invisible”). The most consistent pattern observed here is that greater feelings of social distress in response to socially painful tasks are associated with greater activity in the dorsal anterior cingulate cortex (dACC) and the anterior insula (AI). This is particularly true for the non-adolescent samples, in which dACC and AI activity are observed in 73% and 45% of the studies, respectively.<illusr align="right" rid="i2"></illusr>
</p>
</bx>
<bx id="bx3" placement="external" type="reg">
<bxtitle>Box 3 | Affective versus cognitive processing in the dACC</bxtitle>
<p>Although substantial evidence supports the role of the dorsal anterior cingulate cortex (dACC) in negative affective experience (pain, fear and distress)<bibr rid="b34 b51"></bibr>
, this concept is at least superficially at odds with an otherwise predominantly cognitive account of dACC activity. For example, research has highlighted the role of this region in conflict monitoring — detecting conflicting response tendencies (in the Stroop task, for example) or mismatches between produced and intended responses (that is, error detection) in order to signal the need for cognitive control<bibr rid="b140"></bibr>
. On the basis of this, some have suggested that this region is involved in cognition, not affect<bibr rid="b141"></bibr>
. However, another possibility is that these two accounts of dACC function are not incompatible, but rather work together as two components of a neural alarm system involved in the detection of discrepancies from a desired set point and the sounding of an alarm (which may include affective responses and autonomic activity) to recruit attention and resources aimed at fixing the discrepancy<bibr rid="b8"></bibr>
. From this perspective, studies of conflict monitoring and error detection have examined the discrepancy detection function of the dACC, whereas studies on pain distress, fear or autonomic responding have focused on the alarm sounding function of the dACC. Indeed, recent meta-analyses have shown that negative affect, pain and tasks requiring cognitive control activate overlapping regions of the dACC<bibr rid="b142 b143"></bibr>
. Moreover, we have recently shown that fluctuations in the magnitude of dACC activity in response to errors during a cognitive stop-signal task were positively correlated with fluctuations in self-reported negative affect (frustration) across the task, even after controlling for various cognitive variables (number of errors, self-reported attention and effort)<bibr rid="b149"></bibr>
. Thus, the dACC may perform both cognitive and affective functions that complement one another in supporting efficient goal-corrected behaviour.</p>
</bx>
<bx id="bx4" placement="external" type="reg">
<bxtitle>Box 4 | Differences between physical and social pain</bxtitle>
<p>Although the majority of the research reviewed in this article highlights an overlap in the systems underlying physical and social pain, there are important ways in which these experiences differ. One difference has to do with the way in which individuals experience pain in the absence of any direct threat to themselves — either through reliving prior experiences of pain or through observing the pain of others. With regard to reliving pain, studies have shown that reliving socially painful experiences elicits more pain. Thus, subjects reported feeling more pain after reliving a prior episode of social pain than after reliving a prior episode of physical pain, even though there were no differences in the amount of pain experienced at the time the event originally occurred ('initial pain', see the figure, part <b>a</b>
)<bibr rid="b18 b19"></bibr>
. Interestingly, when it comes to observing the pain of others (empathy), the reverse pattern is observed. When observing others in physical pain, participants show increased activity in affective pain-related neural regions, such as the dorsal anterior cingulate cortex (dACC) and the anterior insula (AI)<bibr rid="b135"></bibr>
(dACC activation shown in part <b>b</b>
of the figure<bibr rid="b144"></bibr>
), whereas these same neural responses are not present when observing others in social pain (mentalizing regions, such as the dorsomedial prefrontal cortex, are present instead; see part <b>c</b>
of the figure)<bibr rid="b145"></bibr>
, unless the target of the social pain is a close friend (see part <b>d</b>
of the figure)<bibr rid="b146 b147"></bibr>
.</p>
<p>One way to understand these findings is to hypothesize that experiences of social pain may rely on more abstract types of social-cognitive processing that can be intentionally activated, whereas experiences of physical pain may rely on more low-level, automatic processes that are less accessible to intentional activation. If this were the case, it would make sense that social pain would be more easily relived than physical pain because the processes that elicit social pain can be more easily accessed than those that elicit physical pain. Moreover, to the extent that intentional social cognitive processing is required to experience others' social, but not physical, pain, it would make sense that observing anyone in physical pain would activate pain-related neural regions, but that these same neural regions might only be engaged in response to viewing close others (but not strangers) in social pain. Additional research is needed to further explore these possibilities. Part <b>a</b>
is reproduced, with permission, from Ref. <bibrinl rid="b18">18</bibrinl>
© (2008) SAGE Publications. Part <b>b</b>
is reproduced, with permission from Ref. <bibrinl rid="b144">144</bibrinl>
© (2005) Elsevier Science. Part <b>c</b>
is reproduced, with permission, from Ref. <bibrinl rid="b145">145</bibrinl>
© (2011) Elsevier. The left panel of part <b>d</b>
is reproduced, with permission, from Ref. <bibrinl rid="b146">146</bibrinl>
© Oxford University Press. The right panel of part <b>d</b>
is reproduced, with permission, from Ref. <bibrinl rid="b147">147</bibrinl>
© (2011) Taylor and Francis.<illusr align="right" rid="i3"></illusr>
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<ack>
<p>I am grateful to M. Lieberman, S. Taylor, M. Irwin and the members of the Social and Affective Neuroscience Laboratory for their helpful comments on earlier versions of this review.</p>
</ack>
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<mods version="3.6"><titleInfo lang="eng"><title>The pain of social disconnection: examining the shared neural underpinnings of physical and social pain</title>
</titleInfo>
<titleInfo type="alternative" lang="eng" contentType="CDATA"><title>The pain of social disconnection: examining the shared neural underpinnings of physical and social pain</title>
</titleInfo>
<name type="personal"><namePart type="given">Naomi I.</namePart>
<namePart type="family">Eisenberger</namePart>
<affiliation>University of California, Department of Psychology, 4444 Franz Hall, Los Angeles, California 90095, USA.</affiliation>
<affiliation>E-mail: neisenbe@ucla.edu</affiliation>
<role><roleTerm type="text">author</roleTerm>
</role>
<description>Naomi Eisenberger is an assistant professor of psychology at the University of California, Los Angeles (UCLA), USA. She received her Ph.D. in social psychology and then completed a postdoctoral fellowship in psychoneuroimmunology at UCLA. Her research seeks to identify the basic neural systems that may have been co-opted to support more complex socio-emotional experiences, such as social rejection and social connection. She is also interested in elucidating the neural mechanisms that may translate experiences of social rejection or connection into physiological responses that have implications for health outcomes. She is the recipient of early career awards from the Association for Psychological Science, the American Psychosomatic Society and the International Union for Psychological Science.</description>
</name>
<typeOfResource>text</typeOfResource>
<genre type="review-article" displayLabel="Review (rv)" authority="ISTEX" authorityURI="https://content-type.data.istex.fr" valueURI="https://content-type.data.istex.fr/ark:/67375/XTP-L5L7X3NF-P">review-article</genre>
<originInfo><publisher>Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.</publisher>
<dateIssued encoding="w3cdtf">2012-06</dateIssued>
<copyrightDate encoding="w3cdtf">2012</copyrightDate>
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<language><languageTerm type="code" authority="iso639-2b">eng</languageTerm>
<languageTerm type="code" authority="rfc3066">en</languageTerm>
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<abstract lang="eng">Experiences of social rejection, exclusion or loss are generally considered to be some of the most 'painful' experiences that we endure. Indeed, many of us go to great lengths to avoid situations that may engender these experiences (such as public speaking). Why is it that these negative social experiences have such a profound effect on our emotional well-being? Emerging evidence suggests that experiences of social pain — the painful feelings associated with social disconnection — rely on some of the same neurobiological substrates that underlie experiences of physical pain. Understanding the ways in which physical and social pain overlap may provide new insights into the surprising relationship between these two types of experiences.</abstract>
<relatedItem type="host"><titleInfo><title>Nature Reviews Neuroscience</title>
</titleInfo>
<genre type="journal" authority="ISTEX" authorityURI="https://publication-type.data.istex.fr" valueURI="https://publication-type.data.istex.fr/ark:/67375/JMC-0GLKJH51-B">journal</genre>
<subject displayLabel="410"><genre>category</genre>
<topic>410</topic>
</subject>
<subject displayLabel="370"><genre>category</genre>
<topic>370</topic>
</subject>
<identifier type="ISSN">1471-003X</identifier>
<identifier type="eISSN">1471-0048</identifier>
<part><date>2012</date>
<detail type="volume"><caption>vol.</caption>
<number>13</number>
</detail>
<detail type="issue"><caption>no.</caption>
<number>6</number>
</detail>
<extent unit="pages"><start>421</start>
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