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Abstract

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.
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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  • .-F De Quervain
D. J.-F. de Quervain et al., Science 305, 1254 (2004).
  • A Bechara
  • H Damasio
  • A R Damasio
A. Bechara, H. Damasio, A. R. Damasio, Cereb. Cortex 10, 295 (2000) [Medline].
  • D Martinez
D. Martinez et al., J. Cereb. Blood Flow Metab. 23, 285 (2003) [Medline].
  • R Trivers
R. Trivers, Q. Rev. Biol. 46, 35 (1971).
  • J P O'doherty
  • R Deichmann
  • H D Critchley
  • R J Dolan
J. P. O'Doherty, R. Deichmann, H. D. Critchley, R. J. Dolan Neuron 33, 815 (2002) [Medline].
  • J Olds
  • P Milner
J. Olds, P. Milner, J. Comp. Physiol. Psychol. 47, 419 (1954).
  • B Knutson
  • C M Adams
  • G W Fong
  • D Hommer
B. Knutson, C. M. Adams, G. W. Fong, D. Hommer, J. Neurosci. 21, RC159 (2001) [Medline].