1-s2.0-s0168010212000041-main

8/12/2019 1-s2.0-S0168010212000041-main

1/6

8/12/2019 1-s2.0-S0168010212000041-main

2/6

284 K. Izuma / NeuroscienceResearch 72 (2012) 283288

Fig. 1. Subtle cues of being watched that were found to increase pro-social behavior in previous studies. Pictures of eyes (A), paintings of eyes (B andC), an image of a robot

with human-like eyes (D), andeven three dots configured in the watching-eyes configuration (E, left) compared to three dots in the neutral configuration (E, right) were

found to be sufficient to increase the pro-social tendency of subjects. The figures are adapted, with permission, from the following: (A) Bateson et al. (2006), (B) Haley and

Fessler (2005), (C) Mifuneet al.(2010), (D) Burnhamand Hare (2007), and (E) Rigdon et al. (2009).

of reputation-based processing (but see also Fehr and Schneider,

2010). The importanceof reputation-baseddecision-makingis ever

increasing in themodernworld,where web-basedsocialnetworks

are increasingly popular and people interact with strangers on a

daily basis (Tennie et al., 2010). Apart from itseffects on pro-social

behaviors, reputation-based social cognition pervades actions of

everyday life, from deciding what to say during a casual conversa-

tion with friends to what to wear for a date or a job interview.

In this article, I argue that reputation-based decision-making

is a critical component of numerous human social behaviors,

and I briefly discuss the possible neural mechanisms underly-

ing it from the studies thus far. What makes reputation-based

decision-makingparticularlyinteresting (andsimultaneouslychal-lenging) is that certain components of the process are likely to

be uniquely human. It should be stressed that reputation-based

decision-making here refers specifically to decision-making based

on a representation of ones own reputation in the eyes of others

(i.e.,whatother people think ofme), asopposed toones ownopin-

ion about other people (i.e., social attitudes or what I think about

others). Although some nonhuman animals with complex social

behavior also behave differentially depending on who is present

and where they are looking (e.g., a young monkey avoids picking

up food in front of a gazing alpha male, and social facilitation on

behavior seem to be ubiquitous according to some accounts), there

is no need to processones own reputation in such situations. Ani-

mals are certainly influenced by the presence of conspecifics, and

some can select their actions based on the reputations they haveformed about others (e.g., approaching an individual with a good

reputation and avoiding another with a bad reputation); however,

thesecasesarelargelyexplainedby basiclearningmechanismsand

do not necessitate the constructionof a self-representation of how

others think about oneself.

Processing ones own reputation in the eyes of others and mak-

ing a decision based on its expected reward value entail highly

complex cognitive processes that may be evident only in humans.

Understanding our reputationinvolves thinking about whatothers

think of us and thus requires some level of meta-representation

(e.g., thinking about thinking) (Amodio and Frith, 2006). In partic-

ular, it requires the ability to represent the possible future beliefs

ofothers about oneself (if I makea donation, theywill think I ama

generous person [positive expected value]; if I do not donate, they

will think I am greedy [negative expected value]). Although there

is evidence that chimpanzees can understand that others see and

know things that are in fact the case, Call and Tomasello (2008)

argue that the past 30 years of research indicate that chimpanzees

simplycannotunderstandanothersfalsebelief, whichsuggeststhat

chimpanzees lack the capacity for thekind of meta-representation

required for reputation-based processing.Consistentwiththis idea

is the finding that human pro-social tendencies are affected by

the presence of a third party individual who does not directly

benefit from the pro-social act. Although pro-social behavior is

well-documented in non-human primates (Silk and House, 2011;

Warneken and Tomasello, 2009), studies have shown that chim-

panzees fail to show any increased pro-social behavior in thepresence of another group member even when given the oppor-

tunity to directly give food to the individual at no extra cost to

themselves (Jensen et al., 2006; Silk et al., 2005; Vonk et al., 2008).

These findings suggest that non-human primates lack the cogni-

tive ability to construct a self-representation (i.e., reputation) that

is shaped by others.

2. Evolutionaryperspectives on reputation

The uniquely human link between pro-social behavior and

reputation is emphasized by the theoretical and empirical con-

siderations of how certain aspects of altruism may have evolved.

Humans exhibit pro-social or altruistic acts (providing a benefitto others at a cost to oneself) even toward non-kin who they will

never meet again (e.g., making a donation to a charity, volunteer-

ing, and giving blood). These observations are not easily explained

in an evolutionary framework, and have been used as evidence

for the unique social structure of humans (Fehr and Fischbacher,

2003). Reputation is considered to be a key concept explaining

such uniquely human altruism through the mechanism of indirect

reciprocity (Alexander, 1987; Nowak and Sigmund, 1998, 2005)

(see Fig. 2). The logic of indirect reciprocity is as follows: help-

ing someone is based partly on the reputation of the person in

need, so helping others improves ones own reputation and thus

indirectly increases thechance that onewill receive help if needed

in the future. Consequently, self-interested individuals help others

in order to maximize their own benefits, however indirect those

8/12/2019 1-s2.0-S0168010212000041-main

3/6

K. Izuma / NeuroscienceResearch 72 (2012) 283288 285

Fig. 2. Indirect reciprocity based on reputation. Individual A first helps B. This altruistic act by A is observed by others (observers are depicted as dotted circles), and they

modify thereputation of A accordingly (left). Because A has developed a good reputation by helping B, A receives help from C in thenext round (right). Because individuals

with a good reputation are more likely to be helped in the future, self-interested individuals come to help others in order to maximize their own benefits. Modified, with

permission, from Nowak and Sigmund (2005).

benefits may be. Consistent with this view, studies in experimen-

tal economics have found that cooperation can be driven by an

individuals motivation to acquire a good reputation or image

score (Engelmann and Fischbacher, 2009; Seinen and Schram,

2006; Wedekind and Milinski, 2000). It has been argued that the

selective pressure caused by indirect reciprocity may have led to

the development of uniquely human aspects of social cognition,

such as theory of mind (Nowak and Sigmund, 2005).

3. Neural mechanisms underlying reputation-based

decision-making

Reputation-based decision-making entails at least two pro-

cesses: the formation of meta-representations and a cost-benefit

analysis integrating the expected value of ones reputation withthat of other rewards. At the front end, social perception of people

(where they are directing their gaze and attention, for instance) is

also essential, as we noted in our invisibility thought-experiment.

In this section, I summarize studies implicating the striatum and

the medial prefrontal cortex (mPFC) in reputation-based decision-

making along with other potentially relevant mechanisms (see

Fig. 3).

3.1. Striatum

Because valence (either positive or negative) is an intrinsic

aspect of reputation, reputation-based decision-making may be

considereda subset of value-based decision-making.Thus, individ-

uals are required to evaluate whether the expected reward value

of obtaininga good reputation is worthpursuing. Theories of social

exchange (Homans, 1958; Thibaut andKelley, 1959) posit that just

as individuals in economic situations try to maximize monetarygain and minimize monetary loss, individuals in social situations

engage in a cost-benefit analysis of social rewards and social costs.

Fig. 3. Component processes of reputation-baseddecision-makingand candidate brain areas for each process. At first, reputation processing draws on neural mechanisms

for perceiving othersand gaze detection, such as theamygdalaand FFA(shown in red), indicating that ones reputation is taken into account when determining howto act

in a given social situation. Processing ones reputation formedby other peoplerequiresthe formationof a meta-representation, and themPFC (alongwith theTPJ, shown in

cyan) plays a pivotal role in this process.Subsequently,the expected rewardvalue (orutility)of ones reputation must be comparedwith other rewards by usinga common

currencyin thebrainsrewardsystem(striatum,vmPFC,or OFC,shownin yellow) to identifythe action withthe highestvalue. If theexpected rewardvalue ofonesreputation

is worth pursing,pro-socialor altruistic behaviors areexhibited. FFA,fusiform facearea; mPFC, medial prefrontal cortex; TPJ,temporoparietaljunction; vmPFC, ventromedial

prefrontal cortex; OFC, orbitofrontal cortex.

8/12/2019 1-s2.0-S0168010212000041-main

4/6


For example, when making a donation in front of other people, an

individual evaluates the cost and benefit of donating or not donat-

ing and selects an action with the highest expected value. Doing

so requires the conversion of all types of rewards, including the

abstract social reward of ones reputation, to some common cur-

rency to allow for comparisons to be made (Montague and Berns,

2002). Consistent with this idea, a neuroimaging study revealed

that obtaining a monetary reward or perceiving ones good repu-

tation among others both resulted in activation within the same

area in the striatum (Izuma et al., 2008), a brain region associated

with rewardprocessing (Delgado,2007; Schultz, 2000). Daveyetal.

(2010) also found that the striatum is activated by the perception

of being liked by others and Izuma et al. (2010a) extended these

studies by investigating the role of the striatum in social reward

processing during actual social decision-making. Subjects in this

experiment were asked to choose whether to donate to charities

or take the money for themselves in the presence or absence of

real observers. The same striatal region was found to encode the

rewardvalueofboth moneyandsocial reward(reputationor social

approval from others) during pro-social decision-making (Izuma

et al., 2010a). These recent findings suggest that reputation-based

decision-making recruits neural mechanisms partly overlapping

withthoseunderlying decision-makinginvolvingmaterialrewards

such as food (Lau and Glimcher, 2008; Samejima et al., 2005) or

money (Kable and Glimcher, 2007; Tom et al., 2007).

3.2. Medial prefrontal cortex (mPFC)

Theprefrontalcortexis knowntoplay a pivotal role inmaintain-

ing goals (Miller and Cohen, 2001), and manipulating how other

individuals think of us (e.g., I want them to think I am kind) may

be one of the most complex representations only human brains

can accomplish. As mentioned previously, processing ones own

reputation requires one to form a meta-representation, and the

mPFCseems toplaya criticalrolein thisprocess (Amodio andFrith,

2006;Gallagher andFrith, 2003). Functional neuroimaging studies

in humans consistently show that themPFC is activatedwhen par-

ticipants are required to represent others false beliefs (GallagherandFrith, 2003). Similar to representing onesownreputation, rep-

resenting others false beliefs is based on the ability to represent

counterfactuals (Leslie, 1987).

In support of a role for the mPFC in reputation processing are

studies showing increased activation in this region when subjects

perceived others forming an opinion about them (Davey et al.,

2010; Izuma et al., 2008); moreover, thiseffectoccurred regardless

of itsrewardvalues (bothhighlygood reputation andneutral repu-

tation) (Izumaet al., 2008). Ochsner et al. (2005) and DArgembeau

et al. (2007) observed activation of the mPFC when subjects were

asked to judgewhether certain adjectives couldbeused todescribe

themselves as seen from the perspective of another person. In

another study, instead of askingsubjects to judge howothersthink

of them, Izuma et al. (2010b) manipulated a situational factorand found that the mPFC is activated whenever there is increased

demand for reputation processing. In that study, subjects were

asked to perform various tasks upon seeing sentences depicting

pro- or anti-social behaviors (e.g., I never hesitate to go out of

my way to help someone in trouble), and in half of the imaging

sessions, their performances were watched by two real observers

whose faces were visible to the subject being scanned. Increased

mPFC activation was observed when the disclosure of subjects

about their attitudesor knowledgeof socialnormsexpressed in the

sentences was combined with the presence of watching observers

(Izuma et al., 2010b). Furthermore, mPFC activation was observed

when subjects performed an interactive task requiring them to

represent what others think of their thoughts. Coricelli and Nagel

(2009) showed that mPFC activity is positively correlated with the

depth of thinking about other players thoughts and Yoshida et al.

(2010) similarly showed that mPFC activity is correlated with the

uncertainty of inference about another players depth of reason-

ing. It has also been shown that mPFC activity is better correlated

with a computational model that incorporates the belief concern-

ing how ones actions influence the other player (Hampton et al.,

2008). Taken together, these studies suggest that the mPFC is a key

region involved in the formation of meta-representations, which

are essential for reputation processing.

3.3. Other regions

As reputation-based behaviors encompassprocesses that range

from social perception to decision-making and self-regulation

(Adolphs, 2001), it necessarily recruits many structures in addition

to the mPFC and striatum (Fig. 3). Although the role other brain

regions play in reputation processing largely remains unknown,

thisquestionrepresentsa ripeopportunity for investigationwithin

the field of social neuroscience.

In terms of social perception, social information regarding

whetheranaction inagivensituationaffects onesreputationornot

first hasto bedetected (i.e., cues indicating thepresence of others),

processing that likely recruits temporal cortices and the amyg-

dala. The amygdala receives inputs from all sensory modalities,

processes the emotional or social significance of stimuli (Adolphs,

2010; Zald, 2003), and heavily connected with the prefrontal and

temporal cortices as well as the striatum (Amaral et al., 1992;

Barbas andDe Olmos,1990; Carmichael andPrice, 1995). Especially

relevant to reputation processing is the detection of eyes and gaze

direction. The aforementioned behavioral studies (Bateson et al.,

2006; Burnham and Hare, 2007; Ernest-Jones et al., 2011; Haley

and Fessler, 2005; Mifune et al., 2010; Oda et al., 2011; Rigdon

et al., 2009) suggest that eyes, or mere representationsof them, are

potent stimuli for inducing pro-social behaviors (Fig. 1), and the

amygdala is known to play a crucial role in the detection of eyes

and gaze processing (Itier and Batty, 2009). Multiple studies in a

rare patient with bilateralamygdalalesions suggestthat theamyg-

dala is essential forprocessing thesignificance of eyes within faces(Adolphs et al., 2005; Kennedy and Adolphs, 2010; Spezio et al.,

2007). Another structure likely to play a role in reputation-based

decision-making is the temporal visual cortex; because thereward

value of an expected reputation depends on who the audience is,

regions encoding face identity, such as the fusiform face area, are

also likely to be important (Kanwisher et al., 1997). In agreement

with these ideas,people whocan provide resources(e.g.,a boss and

potential spouse) or a person with whom future interactions are

anticipated (e.g., roommates, colleagues, and neighbors) should be

evaluated as more important than strangers with respect to ones

own reputation (Leary and Kowalski, 1990).

Other possible regions that may be involved in reputation

processing, especially for the representation of reward value,

are more ventral sectors of the prefrontal cortex (vmPFC andOFC), which are known to be involved in value-based decision-

making using a common currency (Chib et al., 2009; Hare

et al., 2010) (for a review, see Rangel and Hare, 2010). There

is now evidence demonstrating the activation of this area

when subjects perceive their own positive reputation (Ito et al.,

2011). Along with the mPFC, the temporoparietal junction (TPJ)

is implicated in the meta-representations required for theory

of mind (Saxe and Kanwisher, 2003). Whether the TPJ also

plays a role in reputation-based decision-making has yet to be

determined.

Reputation processing sometimes requires self-control, and

there is evidence that the dorsolateral prefrontal cortex (DLPFC),

an area implicated in self-control, plays an important role in devel-

oping good reputations (Knoch et al., 2009). While people strive

8/12/2019 1-s2.0-S0168010212000041-main

5/6

8/12/2019 1-s2.0-S0168010212000041-main

6/6


Ito, A., Fujii, T., Ueno, A., Koseki, Y., Tashiro, M., Mori, E., 2011. Neural basis ofpleasant and unpleasant emotions induced by social reputation. Neuroreport22, 679683.

Izuma, K., Matsumoto, K., Camerer, C.F., Adolphs, R., 2011. Insensitivity to socialreputation in autism. Proc.Natl. Acad. Sci. U.S.A. 108,1730217307.

Izuma, K., Saito, D.N., Sadato, N., 2008. Processing of social and monetary rewardsin the human striatum.Neuron 58, 284294.

Izuma, K., Saito, D.N., Sadato, N., 2010a. Processing of the incentive for socialapproval in the ventral striatum during charitable donation. J. Cogn. Neurosci.22, 621631.

Izuma, K., Saito, D.N., Sadato, N., 2010b. The roles of the medial prefrontal cortex

and striatum in reputation processing. Soc. Neurosci. 5, 133147.Jensen,K., Hare, B., Call, J., Tomasello,M., 2006. Whats in it forme?Self-regardpre-

cludesaltruism and spitein chimpanzees. Proc. R. Soc. Lond.B 273, 10131021.Kable, J.W., Glimcher, P.W., 2007. The neural correlates of subjective value during

intertemporal choice. Nat.Neurosci. 10, 16251633.Kanwisher, N., McDermott, J., Chun, M.M., 1997. The fusiform face area: a module

in human extrastriate cortex specialized for face perception. J. Neurosci. 17,43024311.

Kennedy, D.P., Adolphs, R., 2010. Impaired fixation to eyes following amygdaladamage arises from abnormal bottom-up attention. Neuropsychologia 48,33923398.

Knoch, D., Schneider, F., Schunk, D., Hohmann, M., Fehr, E., 2009. Disrupting theprefrontal cortex diminishesthe human ability to build a goodreputation.Proc.Natl. Acad. Sci. U.S.A. 106, 2089520899.

Kurzban,R.,DeScioli, P.,OBrien,E., 2007.Audienceeffectsonmoralisticpunishment.Evol. Hum. Behav. 28, 7584.

Lamba, S., Mace, R., 2010. People recognise when they are really anonymous in aneconomic game. Evol. Hum.Behav. 31, 271278.

Lau, B., Glimcher, P.W., 2008.Value representations in the primate striatum during

matching behavior.Neuron 58, 451463.Leary, M.R., Kowalski,R.M., 1990. Impression management: a literature review and

two-component model. Psychol. Bull. 107,3447.Leslie, A.M., 1987. Pretence and representation: the origins of theory of mind. Psy-

chol. Rev. 94, 412426.Mifune, N., Hashimoto, H., Yamagishi, T., 2010. Altruismtoward in-groupmembers

as a reputation mechanism. Evol. Hum. Behav. 31, 109117.Milinski,M., Semmann,D., Krambeck, H.J., 2002. Reputation helps solve thetragedy

ofthe commons. Nature 415, 424426.Miller, E.K., Cohen, J.D., 2001. An integrative theory of prefrontal cortex function.

Annu. Rev.Neurosci. 24, 167202.Montague, P.R., Berns, G.S., 2002. Neural economicsand the biologicalsubstrates of

valuation. Neuron 36, 265284.Nowak, M.A., Sigmund, K.,1998. Evolution of indirect reciprocity by image scoring.

Nature 393, 573577.Nowak, M.A., Sigmund, K., 2005. Evolution of indirect reciprocity. Nature 437,

12911298.Ochsner, K.N., Beer, J.S., Robertson, E.R., Cooper, J.C., Gabrieli, J.D., Kihsltrom,

J.F., DEsposito, M., 2005. The neural correlates of direct and reflected self-knowledge. Neuroimage 28, 797814.

Oda, R., Niwa, Y., Honma, A., Hiraishi, K., 2011. An eye-like painting enhances theexpectation of a good reputation. Evol. Hum. Behav.32, 166171.

Rangel,A., Hare, T.,2010.Neuralcomputationsassociatedwith goal-directedchoice.Curr. Opin. Neurobiol. 20, 262270.

Rege, M., Telle, K., 2004. The impact of social approval and framing on cooperationin public goodsituations. J. Public Econ. 88, 16251644.

Rigdon, M., Ishii, K., Watabe, M., Kitayama, S., 2009. Minimal social cues in thedictator game. J. Econ. Psychol. 30,358367.

Samejima,K., Ueda, Y.,Doya, K.,Kimura,M., 2005. Representation of action-specificreward values in the striatum. Science 310, 13371340.

Satow, K.L., 1975. Socialapproval andhelping.J. Exp. Soc. Psychol. 11, 501509.

Saxe, R.,Kanwisher,N., 2003. People thinking aboutthinking people. The role of thetemporo-parietal junction in theory of mind. Neuroimage 19, 18351842.

Schlenker, B.R., 1980. Impression Management: The Self-Concept, Social Identity,and Interpersonal Relations. Brooks/Cole, Monterey.

Schultz, W., 2000. Multiple reward signals in the brain. Nat. Rev. Neurosci. 1,199207.

Seinen, I., Schram, A.,2006. Social statusand group norms: indirect reciprocity in arepeatedhelping experiment. Eur. Econ. Rev.50, 581602.

Silk, J.B., Brosnan, S.F., Vonk, J., Henrich, J., Povinelli,D.J., Richardson, A.S., Lambeth,S.P., Mascaro, J., Schapiro, S.J., 2005.Chimpanzeesare indifferent to the welfareofunrelatedgroup members. Nature 437, 13571359.

Silk,J.B.,House,B.R.,2011.Evolutionaryfoundationsof human prosocialsentiments.Proc. Natl. Acad. Sci. U.S.A. 108,1091010917.

Soetevent, A.R., 2005. Anonymity in givingin a natural context a field experimentin 30 churches. J. Public Econ. 89, 23012323.

Spezio, M.L. , Huang, P.Y. , Castelli, F. , Adolphs, R. , 2007. Amygdala damageimpairs eye contact during conversations with real people. J. Neurosci. 27,39943997.

Tennie,C., Frith, U.,Frith,C.D.,2010.Reputationmanagement in theageofthe world-

wide web. TrendsCogn.Sci. 14, 482488.Thibaut,J.W.,Kelley, H.H., 1959.TheSocialPsychology ofGroups.John Wiley& Sons,

New York.Tom, S.M., Fox, C.R., Trepel, C.,Poldrack, R.A., 2007. The neuralbasis of loss aversion

in decision-makingunder risk. Science 315, 515518.Van Vugt, M., Hardy, C.L., 2010. Cooperation for reputation: wasteful con-

tributions as costly signals in public goods. Group Process Interg. 13,101111.

Vonk, J., Brosnan, S.F., Silk, J.B., Henrich, J.,Richardson,A.S., Lambeth,S.P., Schapiro,S.J., Povinelli, D.J., 2008. Chimpanzees do not take advantage of very low costopportunities to deliver food to unrelated group members. Anim. Behav. 75,17571770.

Warneken, F., Tomasello, M., 2009. Varieties of altruism in children and chim-panzees. Trends Cogn. Sci. 13, 397402.

Wedekind, C., Milinski, M., 2000. Cooperation through image scoring in humans.Science 288,850852.

Yoshida,W., Seymour,B., Friston,K.J.,Dolan,R.J., 2010. Neural mechanisms of beliefinference during cooperative games. J. Neurosci. 30, 1074410751.

Zald, D.H., 2003. The human amygdala and the emotional evaluation of sensorystimuli. Brain Res. Brain Res. Rev. 41, 88123.

1-s2.0-s0168010212000041-main

Documents