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Sweet revenge?

September 2004

Authors:

Stanford University

You've been waiting in line in traffic for what seems like hours, when a red sports car whips past on the shoulder. Eventually, the sports car creeps back into view--the driver has run out of shoulder and signals to be let in. Instead of giving way, you stare ahead and accelerate, inching dangerously close to the bumper in front of you. After squeezing back the intruder, you can't help but notice a smile creep onto your face. Judges worry, whereas filmmakers delight, in the fact that revenge feels good. Evolutionary theorists argue that such an "eye-for-an-eye" strategy makes sense, preventing future damage to one's self or kin (1, 2). Yet, in cases ranging from inconsiderate drivers to Nazi war criminals, even unrelated onlookers seem highly motivated to seek revenge, often in spite of personal cost. From the standpoint of self-interest, punishing those who violate the interests of strangers--a form of revenge called altruistic punishment--seems irrational. Enter de Quervain and colleagues (3) on page 1254 of this issue, who offer an alternative explanation--instead of cold calculated reason, it is passion that may plant the seeds of revenge. "Go ahead, make my day." Dirty Harry succinctly informs a norm violator that he anticipates deriving satisfaction from inflicting altruistic punishment.

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Science, Vol 305, Issue 5688, 1246-1247, 27 August 2004

BEHAVIOR:

Sweet Revenge?

Brian Knutson*

You've been waiting in line in traffic for what seems like hours, when

a red sports car whips past on the shoulder. Eventually, the sports car

creeps back into view--the driver has run out of shoulder and signals to

be let in. Instead of giving way, you stare ahead and accelerate,

inching dangerously close to the bumper in front of you. After

squeezing back the intruder, you can't help but notice a smile creep

onto your face.

Judges worry, whereas filmmakers delight, in the fact that revenge feels good.

Evolutionary theorists argue that such an "eye-for-an-eye" strategy makes sense,

preventing future damage to one's self or kin (1, 2). Yet, in cases ranging from

inconsiderate drivers to Nazi war criminals, even unrelated onlookers seem highly

motivated to seek revenge, often in spite of personal cost. From the standpoint of self-

interest, punishing those who violate the interests of strangers--a form of revenge called

altruistic punishment--seems irrational. Enter de Quervain and colleagues (3) on page

1254 of this issue, who offer an alternative explanation--instead of cold calculated reason,

it is passion that may plant the seeds of revenge.

"Go ahead, make my day." Dirty Harry succinctly informs a norm violator that he

anticipates deriving satisfaction from inflicting altruistic punishment.

Using an elegant laboratory task designed to elicit acts of revenge among human

volunteers, de Quervain and colleagues appear to have captured this complex emotional

dynamic of schadenfreude with a positron emission tomography (PET) camera. During

the task, subjects played games involving real money with a series of different partners.

In each interaction, subjects chose to give their partners money, which was then

quadrupled. Next, partners who received the money had a chance to reciprocate, or to pay

back half to the subject. If partners decided not to reciprocate, or defected, subjects could

choose to administer punishment. At this point, their brains were scanned.

De Quervain and co-workers first asked whether choosing to punish a defector would

recruit brain circuits implicated in reward processing. They found that when subjects

administered a monetary punishment to defectors, a subcortical region of the brain called

the striatum increased its consumption of oxygen (that is, was "activated"). The

investigators interpreted this to indicate that punishing a defector activates brain regions

related to feeling good about revenge rather than brain regions related to feeling bad

about having been violated. Indeed, these striatal foci lie near brain areas that rats will

work furiously to stimulate electrically (4). The investigators then asked whether the

striatum would be activated even when administering the punishment carried a personal

cost. They found that the striatum was still activated when subjects chose to administer

punishment at a personal cost, as was a region in the medial prefrontal cortex (MPFC)

that has been implicated in balancing costs and benefits (5). Although these findings

suggested a connection between striatal activation and the satisfaction one might derive

from punishing a defector, they do not establish a directional relationship between the

two. Thus, in a clever internal analysis, the investigators observed that the degree of

striatal activation during no-cost punishment predicted the extent to which subjects chose

to punish at a personal cost (that is, under less satisfying conditions). This finding

suggested to the investigators that striatal activation indexed subjects' anticipation of

satisfaction, rather than satisfaction per se.

These findings fit a fresh piece into the rapidly expanding puzzle of reward processing as

revealed by brain imaging. Ironically, punishment of defectors in this study activated the

same regions (that is, striatum and MPFC) that were activated when people rewarded

cooperators in a recent functional magnetic resonance imaging (fMRI) study (6). These

seemingly diametrically opposite social behaviors are united by a common psychological

experience--both involve the anticipation of a satisfying social outcome. As presaged by

comparative research (7), humans also show increased striatal activity during anticipation

of nonsocial rewards such as monetary gains (8) and pleasant tastes (9). Together, these

findings imply that for certain parts of the striatum, it's the feeling that counts.

As with any compelling study, the findings raise additional questions for future research.

Although PET measures absolute metabolism (and can even provide neurochemical

information), its spatial and temporal resolution are limited (in this case, to 15 mm3/min).

Thus, although they were able to visualize activation at the head of the caudate, the

investigators may not have been able to track activity in the smaller ventral part of the

striatum--the part most directly implicated in motivation (10). Fortunately, event-related

fMRI can resolve activity in smaller regions (~4 mm3) on a second-to-second basis (11).

Techniques like this may enable future investigators to make even more specific

observations regarding when and where activation occurs during altruistic punishment.

Second, while the present PET study of defectors included male subjects, the

aforementioned fMRI study of cooperators included females. Future research will

undoubtedly need to explore which social interactions most powerfully motivate men

compared with women (as well as members of different social groups). Regardless, the

findings do powerfully illustrate the importance of considering proximal emotional

mechanisms in brain imaging studies of social behavior (12). The new results also

suggest that, depending on social learning, some of the same emotions that bring us

together can also break us apart.

The findings of de Quervain et al. also chip yet another sliver from the rational model of

economic man. In fact, their subjects illustrated at least two types of irrationality: reacting

on the basis of emotional considerations and spending costly personal resources to ensure

that defectors got their due. Beyond providing a compelling justification for adding social

justice concerns to existing economic models, the findings serve as a harbinger of future

"neuroeconomic" studies that strive to descriptively reconstruct these models using

neurobehavioral data. One can imagine the new models accommodating both

"passionate" and "rational" forces, as well as specifying when and how they come

together to influence individual choice.

Back in traffic, brake lights flare ahead. You realize that your smile was short-sighted.

Your car skids to a halt. Fortunately, the smile didn't cost a pile-up. This time.

References

1. R. H. Frank, Passions Within Reason: The Strategic Role of the Emotions (Norton,

New York, 1988).

2. R. Trivers, Q. Rev. Biol. 46, 35 (1971).

3. D. J.-F. de Quervain et al., Science 305, 1254 (2004).

4. J. Olds, P. Milner, J. Comp. Physiol. Psychol. 47, 419 (1954).

5. A. Bechara, H. Damasio, A. R. Damasio, Cereb. Cortex 10, 295 (2000) [Medline].

6. J. K. Rilling et al., Neuron 35, 395 (2002) [Medline].

7. S. Ikemoto, J. Panksepp, Brain Res. Rev. 31, 6 (1999) [Medline].

8. B. Knutson, C. M. Adams, G. W. Fong, D. Hommer, J. Neurosci. 21, RC159

(2001) [Medline].

9. J. P. O'Doherty, R. Deichmann, H. D. Critchley, R. J. Dolan Neuron 33, 815

(2002) [Medline].

10. D. Martinez et al., J. Cereb. Blood Flow Metab. 23, 285 (2003) [Medline].

11. B. Knutson, G. W. Fong, C. M. Adams, J. L. Varner, D. Hommer, NeuroReport

12, 3683 (2001) [Medline].

12. P. D. MacLean, The Triune Brain in Evolution (Plenum Press, New York, 1990).

The author is in the Department of Psychology, Stanford University, Stanford, CA 94305,

USA. E-mail: knutson@psych.stanford.edu 10.1126/science.1102822

Include this information when citing this paper.

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Primate Brain Evolution

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That the cerebral hemispheres are requisite for the spontaneous, directed activities of terrestrial vertebrates has been well known since the last century. As Ferrier (1876) noted, if a decerebrated animal “be left to itself, undisturbed by any form of external stimulus, it remains fixed and immovable on the same spot, and unless artificially fed, dies of starvation....” As has since been repeatedly confirmed, the neuraxis below the level of the hemispheres contains the neural apparatus required for posture and locomotion and the integrated performance of bodily actions involved in self-preservation and procreation. Since the cerebral hemispheres are essential for psychological functions, they may appropriately be referred to as the psychencephalon.

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Robert H. Frank

Passions Within Reason: The Strategic Role of the Emotions.

Article

Dec 1990

Robert H. Frank

"Passions Within Reason" re-evaluates the traditional models of human behavior in light of "a simple paradox," as Frank states, "namely, that in many situations the conscious pursuit of self-interest is incompatible with its attainment." The self interest theory inspires self-interest; we expect the worst of others and act accordingly. But Frank shows, with many eloquent examples taken from a whole range of human behavior, that pure self interest leads to disaster, for oneself and society. In "Passions Within Reason" Frank incorporates new developments from biology, psychology, and game and bargaining theory into a micro-economic theory that transcends the traditional "rational choice" model. (PsycINFO Database Record (c) 2012 APA, all rights reserved)

Jan 2004
1254

.-F De Quervain

D. J.-F. de Quervain et al., Science 305, 1254 (2004).

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D Martinez

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Jan 1971
Q REV BIOL
35

R Trivers

R. Trivers, Q. Rev. Biol. 46, 35 (1971).

Jan 2002

J P O'doherty
R Deichmann
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J. P. O'Doherty, R. Deichmann, H. D. Critchley, R. J. Dolan Neuron 33, 815 (2002) [Medline].

Jan 1954
J Comp Physiol Psychol
419

J Olds
P Milner

J. Olds, P. Milner, J. Comp. Physiol. Psychol. 47, 419 (1954).

Jan 2001
J NEUROSCI

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C M Adams
G W Fong
D Hommer

B. Knutson, C. M. Adams, G. W. Fong, D. Hommer, J. Neurosci. 21, RC159 (2001) [Medline].

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