66477073 why rejection hurts a common neural alarm system for physical and social pain

8/2/2019 66477073 Why Rejection Hurts a Common Neural Alarm System for Physical and Social Pain

1/7

Why rejection hurts: a commonneural alarm system for physicaland social painNaomi I. Eisenberger and Matthew D. LiebermanDepartment of Psychology, Franz Hall, University of California, Los Angeles, Los Angeles, CA 90095-1563, USA

Numerous languages characterize social pain, the feel-ings resulting from social estrangement, with wordstypically reserved for describing physical pain (brokenheart, broken bones) and perhaps for good reason. Ithas been suggested that, in mammalian species, thesocial-attachment system borrowed the computationsof the pain system to prevent the potentially harmfulconsequences of social separation. Mounting evidencefrom the animal lesion and human neuroimaging litera-tures suggests that physical and social pain overlapin their underlying neural circuitry and computationalprocesses. We review evidence suggesting that theanterior cingulate cortex plays a key role in the physicalsocial pain overlap. We also suggest that the physicalsocial pain circuitry might share components of a broader

neural alarm system.

When people speak of hurt feelings or broken hearts, itis clear that these descriptions are meant to reect painfulexperiences. Writers have long noted that some of the mostpainful experiences known to humankind are those thatinvolve the loss of important social bonds. Indeed, theuse of physical pain words to describe episodes of socialestrangement is common across many different languages[1] . However, is feeling socially estranged truly compar-able to feeling physical pain or is this merely poeticlicense? This review presents evidence suggesting thatthe similarity between physical and social pain does notend with this linguistic overlap but extends into how thehuman brain processes both kinds of pain. We proposethat, based on similarities in purpose, process, and func-tion, physical and social pain share parts of the sameunderlying system for their operation.

An overlap between physical and social painWe have recently proposed that physical pain the painexperienced upon bodily injury and social pain thepain experienced upon social injury when social relation-ships are threatened, damaged or lost share neural andcomputational mechanisms [1] . This shared system isresponsible for detecting cues that might be harmful tosurvival, such as physical danger or social separation, andthen for recruiting attention and coping resources tominimize threat.

Such an overlap would be evolutionarily adaptive.Because of the prolonged period of immaturity and thecritical need for maternal care in mammalian infants, ithas been suggested that the pain mechanisms involved indetecting andpreventing physical danger were co-opted bythe more recently evolved social attachment system todetect and prevent social separation [2] . This hypothesiswas rst proposed to explain why opioids are effective inalleviating both physical pain and separation distress inseveral different animal species [2] . Because of its aver-siveness, pain captures attention, disrupts ongoing behav-ior, and motivates action aimed at regaining safety andmitigating painful experience [3] . If the need to maintainclose contact with the mother for nurturance and protec-tion is crucial to mammalian survival, experiencing painupon social separation would be an adaptive way toprevent the harmful consequences of maternal separation.

Before continuing, we briey dene physical and socialpain. Physical pain is dened as the unpleasant sensoryand emotional experience associated with actual or poten-tial tissue damage [4] . Social pain is dened as thedistressing experience arising from the perception of actual or potential psychological distance from close othersor a social group (see Box 1 ). This parallels Bowlbysconception of the infant attachment system that monitorsfor physical distance from the caregiver and elicits distressonce a certain distance has been exceeded [5] , but allowsfor theabstract and implied sense of psychological distanceto which adults are sensitive.

A common neural basisSeveral lines of evidence suggest that the anterior cingu-late cortex (ACC), specically the dorsal subdivision(dACC; areas 24 0 and 32 0), is involved in the affectivelydistressing components of both physical and social pain.For decades, neurosurgeons have performed cingulo-tomies, a circumscribed lesioning of the ACC, to treatintractable chronic pain [6] . Patients who have undergonecingulotomies for chronic pain report that they are stillable to feel the pain but that it no longer bothers them [6] ,highlighting the ACCs role in the distressing, rather than

the sensory, component of physical pain.More recently, pain researchers have subdivided

pain experience into two psychological components:sensory processing and felt unpleasantness [7] . NumerousCorresponding author: Naomi I. Eisenberger ([email protected]).

Opinion TRENDS in Cognitive Sciences Vol.8 No.7 July 2004

www.sciencedirect.com 1364-6613/$ - see front matter q 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.tics.2004.05.010
http://www.sciencedirect.com/http://www.sciencedirect.com/


2/7

neuroimaging studies have pointed to the role of thedACC in the felt unpleasantness of physical pain [811] ;whereas the somatosensory cortex and posterior insulahave been associated with the sensory-discriminativeaspects of pain [11] . Specically, increasing levels of

dACC activity correspond with increasing levels of self-reported pain unpleasantness [811] . Thus, individualswho are dispositionally pain-sensitive show more dACCactivity and report greater levels of perceived unpleasant-ness to painful stimulation [12] .

The dACC has also been shown to relate to social paindistress in humans and other mammals. The experience of social pain might be exclusive to mammals because of theirextended need for maternal care, and thus might speci-cally relate to behaviors and neural structures unique tomammalian species. Two behavioral characteristics thatseparate mammals fromtheir reptilian ancestors are vocalcommunication for maintaining mother-infant contact and

the nursing of young along with maternal care [13] .Paralleling these newly acquired behaviors, the cingulategyrus also appears for the rst time, phylogenetically, inmammals and thus might contribute to these behaviors [13] .

Distress vocalizations, emitted by young animals whenseparated from caregivers, rely on an intact cingulategyrus for their production [1315] . Consistent with acausal role for the ACC in the production of social pain anddistress vocalizations, ablating the dACC in squirrelmonkeys eliminates the spontaneous production of dis-tress vocalizations [16,17] , whereas electrically stimulat-ing the dACC in macaques leads to the spontaneousproduction of distress vocalizations [18,19] . In addition,ablating the ACC in macaques leads to decreases inafliativebehavior [20,21] , potentially reecting a reducedneed for social closeness as social separation is no longerdistressing.

The cingulate gyrus also plays a role in maternalresponses to distress vocalizations. Ablating the cingulategyrus in rodent mothers disrupts maternal responses todistress vocalizations, including retrieving pups and keep-

ing them near [22,23] . In one study, the survival rate of ratpups whose mothers had cingulate lesions was only 12%[23] , highlighting the importance of the cingulate in pro-moting mother-infant contact and facilitating offspringsurvival. Two human neuroimaging studies are generallyconsistent with these ndings [14,15] .

To date, only one study has examined the neural corre-lates of social pain in humans. This neuroimaging studyinvestigated the neural correlates of social exclusion [24] .Participants were scanned while playing a computerizedball-tossing game, supposedly with two others, and wereultimately excluded from the game (see Figure 1 a). Whenexamining neural activity during exclusion, compared

with inclusion, participants showed increased activity indACC (see Figure 1 b). The magnitude of dACC activitycorrelated strongly with self-reports of social distress feltduring the exclusion episode (see Figure 1 c and Box 2 ).

A common computational basisProcesses that share the same neural circuitry often sharesome of the same computational mechanisms [25] . Acrossseveral neuroimaging and computational modeling studies,it has been shown that the dACC acts as a conict ordiscrepancy detector, activated by behavioral responseconicts, such as those produced in the Stroop task [26] . Inaddition, the dACC might be sensitive to goal conicts,expectation violations, and errors more generally [27,28](see Box 3 ). Discrepancy detection in dACC leads to pre-frontal activations that promote contextually-appropriate,top-down responses to resolve the discrepancy [29] .

Although the phenomenological experience of paindistress and the computational process of discrepancydetection have been shown to activate neighboring andsometimes overlapping regions of dACC [30] , the phenom-enological and computational correlates of dACC activityhave seldom been investigated together. Typically, studiesof physical or social pain have examined the role of dACCin distress rather than in discrepancy detection, whereasstudies of the computational mechanisms underlyingdACC function have examined its role in discrepancy

detection rather than in distress. In one study that inves-tigated dACC activity to both a discrepancy-detection taskand a pain task, it was found that these tasks activatedmostly adjacent, but sometimes overlapping sections of

Box 1. The link between social rejection and self-esteem

Many psychologists haveassumed that high self-esteem is essentialto positive psychological health [47]. Consistent with this view, highself-esteem has been associated with psychological well-being,whereas low self-esteem has been associated with greater depres-sion, anxiety, and other psychological problems [48]. However,research suggests that it might not be self-esteem per se thatcontributesto psychological well-being, but ratherthe stateof socialconnectedness that underlies this construct.

Leary and colleagues have proposed sociometer theory toexplain why self-esteem appears to be crucial for psychologicalhealth [48,49], maintaining that self-esteem is a measure of thedegree to which an individual is included or excluded by others.Because of the importance of social ties for human survival, it isimportantto be ableto monitor onesacceptanceor rejectionwithinasocial group. In the same manner that a fuel gauge provides a read-out of the amount of gas ina car to prevent empty tanks,self-esteemmight provide a read-out of a persons inclusionarystatus to preventexclusion [48].

Several studies have provided direct evidence for this theoryshowing that increasing degrees of rejection are associated withmore negative self-feelings and reductions in self-esteem [48,49].Additionally, being socially ostracized or excluded during a compu-terized, interactive ball-tossing game (Cyberball) played over theinternet, ostensibly with others, causes reductions in self-esteem[50].Perhapsmost surprising, though, is that evenwhen participantsare told they are playing with a computer program and that thecomputerized players are going to stop throwing the ball to them,participants still report lower self-esteem following the game [51].

Similarly, in an fMRI study of social exclusion [24], participantswere prevented from playing a ball-tossing game, ostensiblybecause of technical difculties, in an implicit exclusion condition.Participantswatched theothers play thegame without them, in whatlooked like exclusion, although participants consciously knew theother players were not excluding them. Nevertheless, implicit exclu-

sion produced dACC activity indistinguishable from explicit exclu-sion. These studies suggest that the capacity for social exclusionto cause social pain and decrease self-esteem might be so powerfulthat simply viewing a scene that bears a resemblance to rejectionproduces these effects. Just as conscious knowledge of a visualillusion does not prevent it from occurring, conscious knowledgethat one is not actually being actively excluded does not preventdACC activity or diminished self-esteem.

Opinion TRENDS in Cognitive Sciences Vol.8 No.7 July 2004 295

www.sciencedirect.com
http://www.sciencedirect.com/http://www.sciencedirect.com/


3/7

dACC in six subjects [30] . In another study that examineddACC activity to both a cognitive task (although not adiscrepancy-detection task) and a pain task, it was foundthat the cognitive task activated a more anterior andsuperior part of dACC; whereas the pain task activated amore posterior part of dACC [31] . However, no studieshave investigated whether true discrepancy-detection

tasks and pain tasks activate the same region of dACCwithin a large sample.

One way to triangulate the relationships between dis-tress, discrepancy detection, and general dACC activity is

by conceptualizing the dACC as a neural alarm system.For an alarm system to function properly, two componentsare needed: a discrepancy monitoring system, which detectsdeviations from desired standards (e.g. detecting an exces-sive amount of smoke), and a sounding mechanism whichsignals that there is a problem that needs to be addressed(e.g. an alarm bell ringing). The discrepancy-detection

function of the dACC can be likened to the detection of excessive smoke whereas pain distress can be likened tothe sound of an alarm bell ringing. Thus, rather thandiscrepancy detection and distress being two competing

Figure 1 . Methodology and results from an fMRI study of social exclusion [24] . (a) Example of what participants viewed while in the scanner. Participants were includedin the ball-tossing game during one round and excluded during another. (b) Participants showed increased dorsal anterior cingulate cortex (dACC) activity during theexclusion compared with the inclusion episode. (c) Participants levels of self-reported distress correlated highly with dACC activity during the exclusion episode comparedwith the inclusion episode.

TRENDS in Cognitive Sciences

1.0

1.5

2.0

2.5

3.0

3.5

4.0

0.06 0.03 0 0.03 0.06 0.09 0.12 0.15

Anterior cingulate activity (6, 8, 45)

S o c

i a l d i s t r e s s

including the third player excluding the third player(a)

(b) (c)

Anterior cingulate(8, 20, 40)

r = 0.88


http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/


4/7

explanations of dACC activity, they might actually becomplementary processes underlying the functioning of this neural alarm system.

One way to test whether discrepancy detection anddistress are complementary processes in the broader

functioning of an alarm system, is to examine whetherindividuals who chronically experience more distressalso show greater dACC reactivity during discrepancydetection. This would suggest that individual differences

operate at the level of the alarm system rather than at thelevel of thecomponent processes. In a recent neuroimagingstudy [32] , individuals with obsessivecompulsive disorder(OCD), an anxiety disorder characterized by heightenedlevels of distress, doubt and worry, were scanned whileperforming a conict monitoring task. Individuals withOCD, compared with healthy controls, showed signi-cantly more dACC activity to high-conict trials. In addi-tion, there was a trend such that within the OCD group,patients with more severe symptoms showed more ACCactivity to conict than those with less severe symptoms.In a study we conducted (reported in [1]), neuroticism, thedispositional tendency to experience distress and negativeaffect, correlated strongly (r 0.76) with ACC activationto a non-distressing discrepancy-detection task. Together,these studies suggest that discrepancy detection and dis-tress might be two complementary processes supporting

the brains alarm system in the ACC.

Consequences of the overlapOne of the hypotheses derived from the physicalsocialpain overlap is that endogenous and exogenous factorsthat enhance sensitivity to one type of pain should enhancethe sensitivity of this alarm system and thus potentiatesensitivity to the other type of pain as well. Alternatively,factors that downregulate the sensitivity to one type of pain should downregulate the sensitivity of the alarm andthus diminish sensitivity to the other type of pain. Existingevidence supports both of these claims.

First, when young children experience physical pain,

they experience social pain more easily and more fre-quently in response to separation from their caregiver [5] .Similarly, individuals with chronic pain disorders aremore likely than healthy controls to have an anxiousattachment style, characterized by a preoccupation withthe commitment status of relationship partners [33] and tohave heightened fears of social evaluation and rejection[34] . Lastly, rejection-sensitive, compared with non-rejec-tion-sensitive, individuals report more distress whenwatching video clips of people experiencing physical pain[35] . These ndings provide evidence that an enhancedsensitivity to one type of pain accompanies an enhancedsensitivity to the other.

Second, increased social support, which reduces socialpain [36] , is also associated with a reduction in pain fromchronic ailments, during cancer, following heart surgery,and during childbirth [3740] . Experimental evidencedemonstrates similar effects in animals and humans. Inanimals, shock punishment is less effective in traininggroups of rats than in training rats individually [41] , leadsto less immobility in rats in the presence of a companion[42] , and elicits fewer emotional reactions in infant goatsin the presence of their mother [43] . Similarly, in humans,the presence of social support increases tolerance of elec-tric shock stimulation [44] and decreases levels of self-reported pain during a cold-pressor task [45] .

Finally, certain drugs have similar regulatory effects on

both physical and social pain. Opiate-based drugs, knownfor their effectiveness in alleviating physical pain, lessensocial pain in animals and humans [2] . Additionally, anti-depressants, often prescribed for anxiety or depression

Box 2. The neural regulation of pain

In addition to dorsal anterior cingulate cortex (dACC), right ventralprefrontal cortex (RVPFC) was also found to be active in response tosocial exclusion(see FigureIa) [24]. This same prefrontalregion wasalso activated in a neuroimaging study of placebo effects whenparticipantsreceivedpainful stimulation to thegut [8](Figure Ib)andhasbeen reported inmore thana dozenneuroimaging studiesof pain[52]. Although RVPFC was activated along with dACC in the socialpain and placebo studies, there was a strong negative relationshipbetween these activations such that greater RVPFC activation wasassociated with less dACC activation and less self-reported distressacross participants (c.f. [53]). These results suggest that RVPFCmight serve a self-regulatoryfunction by disruptingthe paindistressassociated with dACC activity.

RVPFC activity might be set in motion by thinking about , ratherthan merely experiencing, pain. Several studies have reportedincreased RVPFC activity when thinking about, labeling, or evaluat-ing affective stimuli, particularly when thinking about negativestimuli [8,54]. Additionally, RVPFC has been implicated in theinhibition of motor,cognitiveand affectiveprocesses and possessesefferent connections projecting to dACC [55,56].

Similar reciprocal effects have been observed for RVPFC and theamygdala. Hariri et al. found that labeling emotionally expressivefaces produced more RVPFC, and less amygdala, activity thanmatching emotionally expressive faces to other faces [57]. Parallel-ing the pain ndings, in this study, the participants who generatedmore RVPFC activity during the labeling task tended to generateweaker amygdala activations.

Evolutionarily, such a feedback mechanism from RVPFC to alarmsystems such as the ACC and amygdala makes good sense. Thesealarms often trigger a changein ourattentionto deal with thesourceof the threat or to cope in the aftermath. If the alarms continue tosound at full volume, however, they could detract from the limitedprocessing capacity of executive processes in prefrontal cortex.A feedback mechanism in RVPFC might assure that the partialdampening down of an alarm only occurs after attention has beenturnedto thesource of thealarm, thepointat which continuedalarmsounds become maladaptive.

Figure I . Right ventral prefrontal cortex (RVPFC) activation associated with(a) social pain regulation, and (b) physical pain regulation. (Part a reproducedwith permission from [24]).


Social pain regulationRVPFC (y = 27)

Physical pain regulationRVPFC (y = 30)

(a) (b)


http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/


5/7

resulting from social stressors, have recently been found toalleviate physical pain as well [46] and are now prescribedregularly to treat chronic pain.

Conclusion

The ndings reviewed here suggest that social andphysical pain might rely on overlapping neural processes

in the form of a common neural alarm system. Such anoverlap is adaptive for mammalian survival given theextended period of immaturity in mammalian young.Nevertheless, evolutions solution to ensured nurturancemight have unintentionally produced a lifelong need for

social connection and a corresponding sense of distresswhen social connections are broken. A more completeunderstanding of the elicitors and regulators of social painwill benet from further investigations into its links withphysical pain (see Box 4 ).

AcknowledgementsThe preparation of this article was supported by an NSF predoctoralfellowship to N. Eisenberger and by a grant from the National Institute of Mental Health (R21MH6670901) to M. Lieberman. The authors wish tothank the UCLA Brain Mapping Center and the UCLA Social CognitiveNeuroscience Laboratory for their support in conducting several of thestudies that were reviewed here.

References1 Eisenberger, N.I. and Lieberman, M.D. Why it hurts to be left out:the neurocognitive overlap between physical and social pain. In The Social Outcast: Ostracism, Social Exclusion, Rejection, and Bullying(Williams, K.D. et al. , eds), Cambridge University Press, (in press)

Box 3. The function of rostral versus dorsal ACC

In recent years, the activity of the ACC has received a great deal of attention, showing engagement during cognitive tasks involvingattention, error monitoring and target detection [26], during painfulstimulation [11], and during emotional tasks involving the recollectionof emotional experiences [58]. An inuential review of this literaturesuggested that dorsal ACC (dACC) is involved in cognitive processes,whereas the rostral-ventral ACC (rACC) is involved in emotional pro-cesses [58]. However, this analysis did not include studies of physicalpain. Intuitively, pain studies should cluster within the rostral, affectivedivisionof the ACC,but instead typicallyactivate dACC[11]. Thus,dACCactivations to pain remain either unexplained or surprisingly relegatedto the cognitive subdivision of the ACC. This poses a challenge to thecognitive/affective explanation of ACC activity.

One prominent computational explanation that might more ade-quately characterize ACC activity is an account of the ACC as a conictmonitor. Based on theories of cognitive control, it has been suggestedthat the ACC is specically involvedin detecting conicts in informationprocessing to signal situations requiring cognitive control [26]. Thistheory has been primarily applied to cognitive conict and has thustypically been associated with dACC activity. However, some theoriesof emotion suggest that conicts or interruptions to goals and plansresult in strong emotional responses [59,60]. Thus, conict detectionmight be an important computational process underlying emotionalprocesses as well.

Both dACC and rACC might be involved in conict detection butbe sensitive to different forms of conict. Thus, an alternative accountto the cognitive/affective description of ACC activity is that rACC isinvolved in detecting conict when there is an explicit symbolicrepresentation of the stimulus or event that constitutes conict,whereas dACC is involved in more bottom-up conict that is eithersensorimotor or lacks an explicit symbolic representation of the objectof conict (see Figure I).

For instance, conict detection processes that activate dACC arewell characterized by subsymbolic parallel constraint satisfaction

models in which competing behavioral responses produce tensionin the network as the conict increases. However, errordetection, whichactivates rACC [61], involves a symbolic representation of the conictthat just occurred, namely the error. Similarly, discrete emotions areoften dened as having a focal object or event, in contrast to moods,such as anxiety, which do not [62]. At least some studies of affect andemotion demonstratea dorsal/rostralsplit suchthat emotion inductions

activate rACCwhereasanxietyinductions activatedACC [63,64]. Finally,Ploghaus et al. [65] recently reviewed data suggesting that expectedpain activates rACC, whereas unexpected pain activates dACC. This

distinction suggests that, as with physical pain, expected socialrejection should activate rACC, whereas unexpected rejection shouldactivate dACC. A thorough review of the literature is needed todetermine how much of the existing ndings t with this alternativeaccount. Nevertheless, pain studies present a challenge to the currentcognitive/affective conception of ACC function and warrant furtherinvestigation.

Figure I . A subsample of studies that activated rostral ACC (rACC) vs. dorsalACC (dACC). Tasks involving conict that contained a symbolic representationof conict (denoted by squares) activated rostral-ventral ACC, whereas tasksinvolving conict that did not contain a symbolic representation of conict(circles) activated dACC.


Conflict monitoring Error detection

Unexpected/experienced pain Expected/anticipated pain

Induced anxiety Induced emotion (happy, sad, anger, disgust)

Ambiguous emotion pictures Expected negative emotional pictures

Box 4. Questions for future research

How do individual differences in the reactivity of the ACC predictindividual differences in the experience of physical or social pain?Would an individual who is highly sensitive to the possibility of onetype of pain also be more sensitive to the possibility of the other? When does discrepancy detection elicit distress and when does itnot? To what extent do these two processes activate overlapping ordistinct parts of the ACC? Aside from the ACC and the opioid system, what are the otherneural regions and relevant neurotransmitters involved in the

physicalsocial pain overlap? If physical and social pain overlap in parts of their underlyingneural circuitry, might these two types of pain show similarbehavioral or health consequences?


http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/


6/7

2 Panksepp, J. (1998) Affective Neuroscience , Oxford University Press3 Wall, P.D. (1999) Pain: The Science of Suffering , Weidenfeld &

Nicolson4 International Association for the Study of Pain Task Force On

Taxonomy (1994) Classication of Chronic Pain: Description of Chronic Pain Syndromes and Denition of Pain Terms (2nd edn)(Merskey, H. and Bogduk, N., eds), IASP Press

5 Bowlby, J. (1969) Attachment and Loss (Vol. I): Attachment , BasicBooks

6 Foltz, E.L. and White, L.E. (1968) The role of rostral cingulotomy inpain relief. Int. J. Neurol. 6, 353373

7 Price, D.D. (2000) Psychological and neural mechanisms of theaffective dimension of pain. Science 288, 17691772

8 Lieberman, N. et al. (2004) The neural correlates of placebo effects:a disruption account. Neuroimage 22, 447455

9 Rainville, P. et al. (1997) Pain affect encoded in human anteriorcingulate but not somatosensory cortex. Science 277, 968971

10 Tolle,T.R. et al. (1999) Region-specic encoding of sensory and affectivecomponents of pain in the human brain: a positron emission tomo-graphy correlation analysis. Ann. Neurol. 45, 4047

11 Peyron, R. et al. (2000) Functional imaging of brain responses to pain. A review and meta-analysis. Neurophysiol. Clin. 30, 263288

12 Coghill, R.C. et al. (2003) Neural correlates of interindividual differ-ences in the subjectiveexperience of pain. Proc. Natl. Acad. Sci. U. S. A.100, 85388542

13 MacLean, P.D. (1993) Perspectives on cingulate cortex in the limbicsystem. In Neurobiology of Cingulate Cortex and Limbic Thalamus: A Comprehensive Handbook (Vogt, B.A. and Gabriel, M., eds),pp. 1 15, Birkhauser

14 Lorberbaum, J.P. et al. (1999) Feasibility of using fMRI to studymothers responding to infant cries. Depress. Anxiety 10, 99104

15 Lorberbaum, J.P. et al. (2002) A potential role for thalamocingulatecircuitry in human maternal behavior. Biol. Psychol. 51, 431445

16 MacLean, P.D. and Newman, J.D. (1988) Role of midline frontolimbiccortex in production of the isolation call of squirrel monkeys. Brain Res. 45, 111123

17 Kirzinger, A. and Jurgens, U. (1982) Cortical lesion effects and vocalization in the squirrel monkey. Brain Res. 233, 299315

18 Robinson, B.W. (1967) Vocalization evoked from forebrain in Macacamulatta. Physiol. Behav. 2, 345354

19 Smith, W. (1945) The functional signicance of the rostral cingu-lar cortex as revealed by its responses to electrical excitation. J. Neurophysiol. 8, 241255

20 Hadland, K.A. et al. (2003) The effect of cingulate lesions on socialbehaviour and emotion. Neuropsychologia 41, 919931

21 Ward, A.A. (1948) The cingular gyrus: area 24. J. Neurophysiol. 11,1323

22 Murphy, M.R. et al. (1981) Species-typical behavior of hamstersdeprived from birth of the neocortex. Science 213, 459461

23 Stamm, J.S. (1955) The function of the medial cerebral cortex inmaternal behavior of rats. J. Comp. Physiol. Psychol. 47, 2127

24 Eisenberger, N.I. et al. (2003) Does rejection hurt: an f MRI study of social exclusion. Science 302, 290292

25 Kosslyn, S.M. and Koenig, O. (1992) Wet mind: The New Cognitive Neuroscience , Free Press

26 Botvinick,M.M. et al. (2001) Conict monitoring and cognitive control. Psychol. Rev. 108, 624652

27 Braver, T.S. et al. (2001) Anterior cingulate cortex and responseconict: effects of frequency, inhibition and errors. Cereb. Cortex 11,825836

28 Weissman, D.H. et al. (2003) Conict monitoring in the humananterior cingulate cortex during selective attention to global and localobject features. Neuroimage 19, 13611368

29 Carter, C.S. et al. (2000) Parsing executive processes: strategic vs.evaluative functions of the anterior cingulate cortex. Proc. Natl. Acad. Sci. U. S. A. 97, 19441948

30 Derbyshire, S.W.G. et al. (1998) Pain and stroop interference tasks

activate separate processing modules in anterior cingulate cortex. Exp. Brain Res. 118, 526031 Davis, K.D. et al. (1997) Functional MRI of pain- and attention-related

activations in the human cingulate cortex. J. Neurophysiol. 77,33703380

32 Ursu, S. et al. (2003) Overactive action monitoring in obsessive-compulsive disorder: evidence from functional magnetic resonanceimaging. Psychol. Sci. 14, 347353

33 Ciechanowski, P. et al. (2003) The relationship of attachment style todepression, catastrophizing and health care utilization in patientswith chronic pain. Pain 104, 627637

34 Gordon, J.G. et al. (1998) Social, blood/injury, and agoraphobic fears inpatients with physically unexplained chronic pain: are they clinicallysignicant? Anxiety 2, 2833

35 MacDonald, G. andShaw, S. Adding insult to injury: socialpain theoryand response to social exclusion. In The Social Outcast: Ostracism, Social Exclusion, Rejection, and Bullying (Williams, K.D. et al. , eds),Cambridge University Press (in press)

36 Taylor, S.E. Social support. In Oxford Handbook of Health Psychology(Friedman, H.S. and Silver, R.C., eds), Oxford University Press(in press)

37 Hoogendoorn, W.E. et al. (2000) Systematic review of psychosocialfactors at work and private life as risk factors for back pain. Spine 25,21142125

38 Zaza, C. and Baine, N. (2002) Cancer pain and psychosocial factors:

a critical review of the literature. J. Pain Symptom Manag. 24,52654239 King, K.B. et al. (1993) Social support and long-term recovery from

coronary artery surgery: effects on patients and spouses. Health Psychol. 12, 5663

40 Kennell, J. et al. (1991) Continuous emotional support during laborin US hospital: a randomized control trial. J. Am. Med. Assoc. 265,21972201

41 Rasmussen, E.W. (1939) Social facilitation. Acta Psychol. 4, 27529142 Davitz, J.R. and Mason, D.J. (1955) Socially facilitated reduction of a

fear response in rats. J. Comp. Physiol. Psychol. 48, 14915143 Liddell, H.S. (1954) Conditioning and emotions. Sci. Am. 190, 485744 Buck, R.W. and Parke, R.D. (1972) Behavioral and physiological

response to the presence of a friendly or neutral person in two types of stressful situations. J. Pers. Soc. Psychol. 24, 143153

45 Brown, J.L. et al. (2003) Social support and experimental pain.

Psychosom. Med. 65, 27628346 Nemoto, H. et al. (2003) Fluvoxamine modulates pain sensation andaffective processing of pain in human brain. Neuroreport 14, 791797

47 Taylor, S.E. and Brown, J.D. (1988) Illusion and well-being: A socialpsychological perspective on mental health. Psychol. Bull. 103,193210

48 Leary, M.R. et al. (1995) The role of low self-esteem in emotional andbehavioral problems: why is low self-esteem dysfunctional? J. Soc.Clin. Psychol. 14, 297314

49 Leary, M.R. et al. (1998) Calibrating the sociometer: the relationshipbetween interpersonal appraisals and state self-esteem. J. Pers. Soc. Psychol. 74, 12901299

50 Williams, K.D. et al. (2000) Cyberostracism: effects of being ignoredover the Internet. J. Pers. Soc. Psychol. 79, 748762

51 Zadro, L. and Williams, K.D. (2003) Impact of ostracism on social judgments and decisions: explicit and implicit responses. In Social

Judgments: Implicit and Explicit Processes (Forgas, J.P. et al. , eds),pp. 325342, Cambridge University Press52 Petrovic, P. et al. (2000) Pain-related cerebral activation is altered by

a distracting cognitive task. Pain 85, 193053 Lorenz, J. et al. (2003) Keeping pain out of mind: the role of

the dorsolateral prefrontal cortex in pain modulation. Brain 126,10791091

54 Cunningham, W.A. et al. (2003) Neural components of socialevaluation. J. Pers. Soc. Psychol. 85, 639649

55 Preibisch, C. et al. (2003) Event-related f MRI for the suppression of speech-associated artifacts in stuttering. Neuroimage 19, 10761084

56 Vogt, B.A. and Pandya, D.N. (1987) Cingulate cortex of the rhesusmonkey: II. Cortical afferents. J. Comp. Neurol. 262, 271289

57 Hariri, A.R. et al. (2000) Modulating emotional responses: effects of aneocortical network on the limbic system. Neuroreport 11, 4348

58 Bush, G. et al. (2000) Cognitive and emotional inuences in anterior

cingulate cortex. Trends Cogn. Sci. 4, 21522259 Mandler, G. (1975) Mind and Emotion , Wiley60 Miller, G.A.E.H. et al. (1960) Plans and the Structure of Behavior , Holt61 Garavan, H. et al. (2003) A midline dissociation between error-

processing and response-conict monitoring. Neuroimage 20,1132 1139


http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/


7/7

62 Fridja, N.H. (1994) Varieties of affect: emotions and episodes, moods,and sentiments. In The Nature of Emotion: Fundamental Questions(Ekman, P. and Davidson, R.J., eds), pp. 5967, Oxford UniversityPress

63 Liotti, M. et al. (2000) Differential limbic-cortical correlates of sadnessand anxiety in healthy subjects: implications for affective disorders. Biol. Psychol. 48, 3042

64 Kimbrell, T.A. et al. (1999) Regional brain activity during transientself-induced anxiety and anger in healthy adults. Biol. Psychol. 46,454465

65 Ploghaus, A. et al. (2003) Neural circuitry underlying pain modulation:

expectation, hypnosis, placebo. Trends Cogn. Sci. 7, 197200

Endeavour

the quarterly magazine for the historyand philosophy of science

You can access Endeavour online viaScienceDirect , where youll nd acollection of beautifully illustrated

articles on the history of science, bookreviews and editorial comment.

Featuring

Sverre Petterssen and the Contentious (and Momentous) Weather Forecasts for D-Day, 6 June 1944 by J.R. FlemingFood of Paradise: Tahitian breadfruit and the Autocritique of European Consumption by P. White and E.C. Spary

Two Approaches to Etiology: The Debate Over Smoking and Lung Cancer in the 1950s by M. Parascandola

Sicily, or sea of tranquility? Mapping and naming the moon by J. VertesiThe Prehistory of the Periodic Table by D. RouvrayTwo portraits of Edmond Halley by P. Fara

and coming soonFighting the microbe of sporting mania: Australian science and Antarctic exploration in the early twentieth century

by P. RobertsLearning from Education to Communicate Science as a Good Story by A. Negrete and C. Lartigue

The Trafc and Display of Body Parts in the Early-19th Century by S. Alberti and S. ChaplinThe Rise, Fall and Resurrection of Group Selection by M. Borrello

Pomets great Compleat History of Drugs by S. ShermanSherlock Holmes: scientic detective by L. SnyderThe Future of Electricity in 1892 by G.J.N. Gooday

The First Personal Computer by J. NovemberBaloonmania: news in the air by M.G. Kim

and much, much more . . .Locate Endeavour on ScienceDirect (http://www.sciencedirect.com)


http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/http://www.sciencedirect.com/

66477073 why rejection hurts a common neural alarm system for physical and social pain

Documents