PII: S0896-6273(01)00491-3


Neuron, Vol. 32, 537–551, November 8, 2001, Copyright 2001 by Cell Press

Beautiful Faces Have Variable Reward Value:
fMRI and Behavioral Evidence

1994). The strong motivational influence of beauty has
been shown in studies of labor markets suggesting that
there is a ”beauty premium” and “plainness penalty”

Itzhak Aharon,1,2,7 Nancy Etcoff,3,7 Dan Ariely,4,7

Christopher F. Chabris,1,2,5,7 Ethan O’Connor,4

and Hans C. Breiter1,2,3,6

(Hamermesh and Biddle, 1994) such that attractive indi-1Motivation and Emotion Neuroscience Center
viduals are more likely to be hired, promoted, and to earnDepartment of Radiology
higher salaries than unattractive individuals (Marlowe etMassachusetts General Hospital and
al., 1996; Frieze et al., 1990, 1991). Darwinian ap-Harvard Medical School
proaches to the study of facial attractiveness posit thatBoston, Massachusetts 02129
the features of beautiful faces are important biological2Athinoula A. Martinos Center for Biomedical
signals of mate value that motivate behavior in othersImaging
(Etcoff, 1999; Grammer and Thornhill, 1994; Perrett etMassachusetts General Hospital
al., 1998; Symons, 1995).Massachusetts Institute of Technology and

Given the association between beauty and motivatedHarvard Medical School
behavior in individuals assessing it, it is possible that theBoston, Massachusetts 02129
brain circuitry implicated in reward function underlying3Department of Psychiatry
motivated behavior is activated by the social signalsMassachusetts General Hospital and
contained in beautiful faces. Research with another so-Harvard Medical School
cial stimulus, namely money, has implicated an ex-Building 149, 13th Street
tended set of brain reward regions with the anticipationCharlestown, Massachusetts 02129
and reception of monetary outcomes (Breiter et al.,4Massachusetts Institute of Technology
1996b, 2001; Delgado et al., 2000; Elliott et al., 2000;Cambridge, Massachusetts 02139
Knutson et al., 2000, 2001; O’Doherty et al., 2001; Thut5Department of Psychology
et al., 1997). Although money and beautiful faces canHarvard University
both elicit motivated behaviors, money cannot elicit aes-Cambridge, Massachusetts 02138
thetic evaluations. In contrast, it is possible that beauti-
ful faces may stimulate both reward assessments and
aesthetic assessments, each leading to different pat-
terns of brain activity.Summary

Extensive neuroscience research has focused on the
visual processing of faces (e.g., Kanwisher, et al., 1997)The brain circuitry processing rewarding and aversive
and facial expression (e.g., Breiter et al., 1996a; Morrisstimuli is hypothesized to be at the core of motivated
et al., 1996; Phillips et al., 1999; Thomas et al., 2001),behavior. In this study, discrete categories of beautiful
while other work has evaluated the visual processing offaces are shown to have differing reward values and
symmetry (Grammer and Thornhill, 1994; Perrett et al.,to differentially activate reward circuitry in human sub-
1999) and attractiveness (Perrett et al., 1998; Bartelsjects. In particular, young heterosexual males rate pic-
and Zeki, 2000; Nakamura et al., 1998). In this study, wetures of beautiful males and females as attractive, but
wished to evaluate faces as potential objects of reward.exert effort via a keypress procedure only to view pic-
Most visual stimuli are not primary reinforcers; indeed,

tures of attractive females. Functional magnetic reso-
the sensory representation of an object is different from

nance imaging at 3 T shows that passive viewing of
its rewarding properties (Rolls, 1999). When animals or

beautiful female faces activates reward circuitry, in
humans respond to rewarding stimuli, they respond to

particular the nucleus accumbens. An extended set of
multiple informational features extracted from distinct

subcortical and paralimbic reward regions also appear
representations of these goal-objects, including the

to follow aspects of the keypress rather than the rating
rate, latency, incidence, intensity, amount, category,

procedures, suggesting that reward circuitry function
and proximity of the reinforcing stimuli (Breiter and Ro-

does not include aesthetic assessment. sen, 1999; Gallistel, 1990; Shizgal, 1999). The response
of animals and humans to these features appears to be

Introduction dependent on their hedonic deficit state regarding such
reinforcers (Cabanac, 1971). In the absence of a defined

Beauty in human faces has long been considered within deficit state regarding attractive faces, it remains a sa-
the general category of aesthetic theory (Ruskin, re- lient question whether they could be considered to be
printed 1997; Kant, reprinted 1960) and only recently rewarding.
within the domain of biology and neuroscience. Recent To evaluate this issue, we carried out a study with
research on facial beauty suggests that the perception three components, each component using the same
of beauty is innate (Slater et al., 1998; Langlois et al., categories of faces: beautiful females, average females,
1987, 1991) and universal across race and culture (Jones beautiful males, and average males (Figure 1A). One
and Hill, 1993; Cunningham et al., 1995; Perrett et al., component involved a rating measure from 1 (“very unat-

tractive”) to 7 (“very attractive”) to evaluate the aesthetic
quality of these images. Another component used a6 Correspondence: hbreiter@partners.org

7 These authors contributed equally to this work. novel “keypress” task to operationalize the amount of



Neuron
538

et al., 1997, 2001; Delgado et al., 2000; Elliott et al., 2000;
Knutson et al., 2000, 2001; Rogers et al., 1999; Small et
al., 2001; Stein et al., 1998; Thut et al., 1997), including
the nucleus accumbens (NAc), sublenticular extended
amygdala (SLEA) of the basal forebrain, amygdala, hy-
pothalamus, orbitofrontal cortex (GOb), and ventral teg-
mentum (VT) of the midbrain. To control for variable
attention to stimuli, BOLD signal in a control region
known to be modulated by attention, namely the fusi-
form gyrus (GF) (Wojciulik et al., 1998), was also eval-
uated.

Results

Data from Behavioral Measures
Two different groups of heterosexual male subjects
were exposed to two distinct behavioral tasks. One
group of subjects rated facial attractiveness, and an-
other group used the keypress procedure to control the
duration of their exposure to these faces.
Rating Face Attractiveness
Eight young heterosexual males viewed the stimuli se-
quentially, rating each face’s attractiveness on a scale
of 1 (“very unattractive”) to 7 (“very attractive”). The
results (Figure 1B) showed a general effect of beauty
[F(1,7) � 569.9, p � 0.0001], a general effect of gender
[F(1,7) � 23.4, p � 0.0001], and an interaction [F(1,7) �
5.8, p � 0.05]. Within the male and female sets, the
differences between beautiful and average faces were
significant (p � 0.000001) for each comparison. Most
importantly, for our purpose, the difference between the
beautiful males and beautiful females was not significant
[t(7) � 0.99, p � 0.36].

The ratings varied with exposure, such that the differ-
ence in ratings between average and beautiful female
faces increased from 2.96 on the first exposure to 3.39
and 3.54 on the second and third exposures; this trend

Figure 1. Rating and Keypress Results
had a significant linear component, p � 0.003. This oc-

(A) A sample of the four picture types used in these tasks (from
curred because the ratings for the average faces de-left to right): beautiful female, average female, beautiful male, and
creased (2.33, 2.00, and 1.91 across exposures), whileaverage male.

(B) Eight heterosexual males rated picture attractiveness on a 1–7 the ratings for the beautiful faces increased slightly
scale. The overall mean ratings were: beautiful female 5.38 (SD 0.55), (5.29, 5.39, and 5.45). By contrast, for the male faces,
beautiful male 5.46 (0.53), average female 2.08 (0.42), average male ratings of beautiful and average faces both increased
2.79 (0.66).

slightly with exposure, with the difference remaining
(C) A separate cohort of 15 heterosexual males performed a task

fairly steady (2.72, 2.61, and 2.70).where picture viewing time was a function of the number of their
Keypressing Paradigmkeypresses. Within each gender, the 80 faces were always pre-

sented in a new random order, with beautiful and average faces A separate cohort of 15 young heterosexual males com-
intermixed (Ariely et al., 2001). The mean viewing times were: beauti- pleted the keypress task with a mean number of key-
ful female 8.67 s (SD 2.1 s), beautiful male faces 5.9 (1.63), average presses per subject of 6726 (SD 4287), which translated
female 5.25 (1.35), average male 5.33 (1.43).

into large effects on image viewing times. The results
(Figure 1C) showed that subjects expended effort only
to increase the viewing time of beautiful female faces.work subjects performed in order to change the relative

duration they viewed the different images. The keypress For all other categories, they keypressed to make the
faces disappear faster. There was a significant effect oftask evaluated whether these categories of faces had

reward values that distinguished them (i.e., along the beauty [F(1,14) � 21.7, p � 0.001], a significant effect
of gender [F(1,14) � 22.4, p � 0.001], and a significantdimension of reward intensity; Shizgal, 1999). For the

neuroimaging component of the study, reward region interaction [F(1,14) � 24.3, p � 0.001]. Most importantly
(and in contrast to the rating task), there was a significantactivity was evaluated using fMRI at 3 T to determine if

signal changes followed the results of the behavioral difference between the beautiful males and beautiful
females [t(14) � 5.1, p � 0.0002]. Because the overalltasks. Six brain regions were targeted that have been

associated with reward function in animals (Everitt and duration of the study was fixed (40 min—allowing sub-
jects to control only the allocation of time between theRobbins, 1992; Rolls, 1999; Schultz and Dickinson, 2000;

Shizgal, 1999) and humans (Berns et al., 2001; Breiter different categories), the number of exposures was not



Beauty and Reward
539

Table 1A. Random Effects Analysis in A Priori Regions

Tal Coordinates

Anatomy ROI R/L A/P S/I ANOVA Paired Contrasts

NAc A �6 3 �3 p � 0.0060 FBvsFA (p � 0.07)
FBvsMB (p � 0.03)

VT B 12 �12 �3 p � 0. 0901 —
SLEA C �28 9 �15 p � 0.0643 —
SLEA D �18 �12 �3 p � 0.9820 —
SLEA E 31 6 �12 p � 0.9933 —
GOb F �34 21 �21 p � 0.7860 —

1B. Random Effects Analysis in Control Region

Tal Coordinates

Anatomy ROI R/L A/P S/I ANOVA Paired Contrasts

GF G �37 �54 �15 p � 0.6117 —
GF H 34 �75 �6 p � 0.2991 —

Region of interest (ROI) based analysis of fMRI data from targeted brain regions. The Talairach coordinates (Talairach and Tournoux, 1988)
of maxima for the six a priori and two control ROIs are expressed in mm from the anterior commissure: x, right (�)/left (�); y, anterior (�)/
posterior (�); z, superior (�)/inferior (�). ANOVA results from the interaction of Gender and Attractiveness are tabulated; paired contrasts are
listed for ANOVA results with p � 0.05/6 clusters in hypothesized reward regions � 0.0083. GF clusters were considered separately and had
to meet the same threshold. FB stands for beautiful female, FA for average female, and MB for beautiful male.

constant across subjects. On average, subjects viewed ROI-Based Random Effects Analysis
the entire set of 80 images three to four times, with the Foci of Signal Change in Targeted Anatomic Regions.
pattern of results not changing with repeated viewing. Data obtained at all time points during the face and

fixation point phases of the paradigm were evaluated by
statistical parametric analysis. Six ROIs were identified,Data from Neuroimaging
one in the left GOb, two in the left SLEA, one in theInitial data analysis focused on six brain regions: the
right SLEA, one in the left NAc, and one in the right VT.nucleus accumbens (NAc), sublenticular extended
Furthermore, two foci in opposite hemispheres wereamygdala (SLEA) of the basal forebrain, amygdala, hy-
found in the control region of the fusiform gyrus (GF).pothalamus, orbitofrontal cortex (GOb), and ventral teg-

Hypothesis Testing via ANOVA and Contrasts: A Priorimentum (VT) of the midbrain. For these targeted regions,
Reward Regions. Gender and beauty served as the pre-a region-of-interest based (ROI-based) analysis was ini-
dictors in the two-way ANOVA of individual time coursestially performed using individual data (henceforth re-
sampled from each ROI. The ANOVA results from theferred to as “random effects analysis”), followed by a
interaction of gender and beauty are described in Tablevoxel-by-voxel post-hoc analysis of data from the aver-
1A. Only the ROI in the left NAc (see Figures 2 and 4)aged cohort. For the ROI-based random effects analy-
exhibited a significant general effect [F(1,5) � 20.9, p �sis, we selected all clusters of activated voxels in the
0.0060], although two other ROIs suggested trends to-targeted regions that were significant in the comparison
ward such an effect [i.e., the VT and SLEA(C)]. The pairedbetween the four face categories and the fixation point
contrasts of the NAc time courses were significant forbaseline. These clusters were then used as regions of
the beautiful female versus average female conditionsinterest (ROIs) to sample individual data for an analysis
and for the beautiful female vs. beautiful male conditionsof variance. For the ROI-based random effects analysis,
(Table 1A). The bar graphs of average percent signaltype II errors (false negative) might be expected in the
change across subjects for these conditions (Figure 2)case of (1) opponent responses to different face condi-
supports the results of the paired contrasts in the NAc.tions, which would tend to cancel as a result of the

These data (Figure 2) support a number of other salientaveraging of all face categories, or (2) responses con-
observations. For instance, with regard to the NAc, thefined to a small proportion of face conditions, which
signal change in the average male condition is secondwould tend to be diluted by such averaging. Thus, a
only to that of the beautiful female faces and is notpost-hoc parametric analysis (i.e., using t statistics) was
significantly different than it. It is also notable that signalperformed on a voxel-by-voxel basis using data aver-
profiles in the VT and one focus in the SLEA(C) resembleaged across the cohort (henceforth referred to as “fixed
the signal profiles between the beautiful female condi-effects analysis”) to determine if differential patterns of
tion and the average female plus beautiful male condi-reward circuitry activation paralleled results from the
tions in the NAc, even if not significant by the analysistwo behavioral studies. General effects for beauty and
of variance (Table 1A). One other focus of signal changegender were each evaluated, followed by their corre-
in the SLEA(D) also qualitatively resembles those in thesponding specific effects: beautiful female versus aver-
NAc [and VT plus SLEA(C)], but differs with regard toage female and beautiful male versus average male (i.e.,
signal change in the average male condition. In general,beauty effects), along with beautiful female versus beau-
there is a qualitative resemblance between the keypresstiful male and average female versus average male (i.e.,

gender effects). results for the beautiful female, average female, and



Neuron
540

Figure 2. Bar Graphs of Mean Percent Signal
Change and Standard Deviation from the Six
ROIs Selected for the Random Effects
Analysis

Percent signal change is presented, relative
to the experimental baseline, for each of the
stimulus conditions: beautiful female, aver-
age female, beautiful male, and average male
faces. Note the similar signal profiles for the
first three bars in each graph for the NAc(A),
VT(B), SLEA(C), and SLEA(D).

beautiful male conditions, and signal changes for these 9 of Table 2) contains ROI C (Table 1A) of the random
effects analysis. All of these foci of signal change, withthree conditions in the NAc, SLEA(C), SLEA(D), and VT.

Hypothesis Testing via ANOVA and Contrasts: Control the exception of the right SLEA focus of negative signal
change (Table 2, #A8), coincided with foci of signalRegion. The ANOVA results from the interaction of gen-

der and beauty are described in Table 1B, and no ROIs change observed in the comparisons for the two specific
effects that follow.exhibited a significant general effect.

Fixed Effects (Post-Hoc) Analysis of Average Data Specific Effect for Beauty: Beautiful versus Average
Female Comparison. For this contrast, four clustersA number of reward regions produced significant signal

change (p � 0.00011) for the general effects of beauty were observed with significant positive signal changes:
two in the right GOb, one in the left GOb, and one inand gender and the specific effects of the interactions

between beauty and gender. The following sections are the right NAc (Table 2). Four foci of subthreshold positive
signal change were further observed in the left NAc,organized around the general effects with specific ef-

fects (interactions) following. bilateral SLEA, and right VT. Three foci of significant
negative signal change were observed: one in the rightGeneral Effect of Beauty: All Beautiful versus All Aver-

age Face Comparison. The general comparison of all GOb, and two in the left GOb.
Of these activation foci, four directly correspond tobeautiful versus average faces revealed four clusters of

significant positive signal change in the right GOb, right foci observed in the general contrast for beauty. In par-
ticular, activation in the VT, SLEA (see Figure 3), andSLEA, and bilateral VT. One focus of subthreshold posi-

tive signal change (p � 0.001) was further noted in the GOb (Table 2, #B5, B7, B9, B11) is common to both,
although one SLEA focus is countered by an activationleft SLEA. Two foci of significant negative signal change

were observed in the bilateral SLEA, one of which (row of opposite valence from the beautiful male versus aver-



Beauty and Reward
541

T
a

b
le

2
.

P
o

st
-H

o
c

F
ix

e
d

E
ff

e
c

ts
A

n
a

ly
si

s

C
o

n
tr

a
st

A
B

C
D

E
F

G
e
n

e
ra

l
B

e
a
u

ty
B

F
–A

F
B

M
–A

M
G

e
n

e
ra

l
G

e
n

d
e
r

B
F

–B
M

A
F

–A
M

A
n

a
to

m
y

N
u

m
b

e
r

R
–L

A
–P

S
–I

p
V

a
lu

e
R

–L
A

–P
S

–I
p

V
a
lu

e
R

–L
A

–P
S

–I
p

V
a
lu

e
R

–L
A

–P
S

–I
p

V
a
lu

e
R

–L
A

–P
S

–I
p

V
a
lu

e
R

–L
A

–P
S

–I
p

V
a
lu

e

N
A

c
a
n

d
o

th
e
r

V
S

1
1
6

1
8

�
5

3
.3

E
�

6
7

1
2

2
�

6
.4

E
�

6
7

9
�

2
1
.4

E
�

4
*

1
6

1
8

�
5

�
1
.0

E
�

4
2

�
6

1
5

�
2

5
.9

E
�

4
*

�
1
2

9
2

�
3
.3

E
�

7
�

9
9

5
6
.6

E
�

7
�

9
6

2
�

4
.0

E
�

5
3

�
1
2

3
�

2
3
.8

E
�

5
V

T
4

�
3

�
8

�
1
5

1
.4

E
�

5
�

3
�

1
8

�
1
1

3
.0

E
�

6
�

6
�

1
8

�
8

3
.4

E
�

4
*

�
6

�
1
8

�
8

1
.9

E
�

5
5

3
�

1
8

�
1
5

4
.4

E
�

5
1
3

�
1
5

�
5

2
.4

E
�

4
*

1
3

�
1
5

�
5

4
.9

E
�

6
1
0

�
2
4

�
5

2
.5

E
�

4
*

6
1
9

�
2
1

�
2

4
.8

E
�

5
S

L
E

A
7

1
6

�
9

�
8

2
.2

E
�

5
1
6

�
9

�
8

2
.1

E
�

4
*

8
2
2

3
�

1
5

�
5
.3

E
�

6
1
9

9
�

1
5

5
.9

E
�

6
9

�
1
5

9
�

1
1

�
2
.1

E
�

7
�

2
4

3
�

1
8

2
.5

E
�

4
*

�
1
8

9
�

1
5

�
1
.5

E
�

1
0

�
1
8

9
�

1
5

1
.4

E
�

5
�

1
8

9
�

1
5

�
1
.4

E
�

5
1
0

�
1
2

0
�

8
�

2
.0

E
�

6
�

3
0

�
3

�
8

�
2
.2

E
�

5
G

O
b

1
1

1
6

4
5

�
1
1

1
.0

E
�

4
1
9

4
8

�
1
1

8
.5

E
�

6
2
8

4
5

�
5

�
1
.4

E
�

7
2
2

5
1

�
2

3
.3

E
�

6
1
2

�
2
1

3
3

�
8

2
.0

E
�

6
�

2
1

1
8

�
8

9
.5

E
�

8
1
3

�
2
1

4
5

�
5

�
3
.9

E
�

9
�

1
8

4
5

�
5

�
7
.8

E
�

9
�

2
4

4
2

2
1
.2

E
�

6
1
4

3
4

4
2

�
2

�
8
.6

E
�

1
1

3
4

4
2

�
2

5
.1

E
�

5
1
5

1
3

5
4

�
8

1
.9

E
�

8
1
6

�
3
3

2
4

2
�

6
.2

E
�

5
�

3
3

2
4

�
5

1
.9

E
�

6
A

m
yg

1
7

�
1
2

�
3

�
2
4

�
2
.3

E
�

4
*

�
1
8

0
�

1
5

�
6
.3

E
�

4
*

1
8

�
2
7

�
6

�
2
1

9
.2

E
�

4
*

�
2
7

�
6

�
2
1

5
.0

E
�

4
*

1
9

2
8

3
�

2
8

1
.6

E
�

4
*

2
0

0
3

�
1
5

�
1
.9

E
�

4
*

H
yp

o
2
1

7
�

1
2

�
8

5
.6

E
�

4
*

3
�

1
2

�
8

2
.4

E
�

5

A
c
ti

va
ti

o
n

c
lu

st
e
rs

a
re

id
e
n

ti
fi
e
d

b
y

p
o

st
-h

o
c

vo
x
e
l-

b
y-

vo
x
e
l

a
n

a
ly

si
s.

“A
n

a
to

m
y”

lis
ts

th
e

si
x

ta
rg

e
te

d
re

w
a
rd

re
g

io
n

s,
in

c
lu

d
in

g
p

u
ta

ti
ve

B
ro

d
m

a
n

A
re

a
(B

A
)

w
h

e
re

a
p

p
ro

p
ri

a
te

.
A

c
ti

va
ti

o
n

s
a
re

id
e
n

ti
fi
e
d

b
y

ro
w

n
u

m
b

e
r

(N
u

m
b

e
r)

a
n

d
sp

e
c
if
ic

su
b

tr
a
c
ti

o
n

(A
–F

).
T

h
e
se

su
b

tr
a
c
ti

o
n

s
in

c
lu

d
e

th
e

g
e
n

e
ra

l
c
o

m
p

a
ri

so
n

s
fo

r
b

e
a
u

ty
a
n

d
g

e
n

d
e
r

a
n

d
th

e
ir

a
ss

o
c
ia

te
d

sp
e
c
if
ic

c
o

n
tr

a
st

s:
b

e
a
u

ti
fu

l
fe

m
a
le

ve
rs

u
s

a
ve

ra
g

e
fe

m
a
le

(B
F

–A
F

),
b

e
a
u

ti
fu

l
m

a
le

ve
rs

u
s

a
ve

ra
g

e
m

a
le

(B
M

–A
M

),
b

e
a
u

ti
fu

l
fe

m
a
le

ve
rs

u
s

b
e
a
u

ti
fu

l
m

a
le

(B
F

–B
M

),
a
n

d
a
ve

ra
g

e
fe

m
a
le

ve
rs

u
s

a
ve

ra
g

e
m

a
le

(A
F

–A
M

).
T

a
la

ir
a
c
h

c
o

o
rd

in
a
te

s
(T

a
la

ir
a
c
h

a
n

d
T

o
u

rn
o

u
x
,

1
9
8
8
)

o
f

th
e
se

a
c
ti

va
ti

o
n

fo
c
i

a
re

lis
te

d
,

a
n

d
m

a
x
im

a
p

va
lu

e
s

a
re

ta
b

u
la

te
d

,
w

h
e
re

“E
”

st
a
n

d
s

fo
r

e
x
p

o
n

e
n

t,
su

c
h

th
a
t

1
.0

E
�

4
m

e
a
n

s
1
.0

�
1
0

�
4 .

A
c
ti

va
ti

o
n

c
lu

st
e
rs

a
re

lis
te

d
th

a
t

p
ro

d
u

c
e
d

si
g

n
if
ic

a
n

t
p

o
st

-h
o

c
e
ff

e
c
ts

p
e
r

a
p

va
lu

e
th

re
sh

o
ld

c
o

rr
e
c
te

d
fo

r
th

e
vo

lu
m

e
o

f
vo

x
e
ls

sa
m

p
le

d
in

a
p

ri
o

ri
ta

rg
e
te

d
re

g
io

n
s.

A
c
ti

va
ti

o
n

s
w

it
h

a
st

e
ri

sk
s

d
id

n
o

t
m

e
e
t

th
is

c
o

rr
e
c
te

d
th

re
sh

o
ld

b
u

t
h

a
d

m
a
x
im

a
w

it
h

1
.1

�
1
0

�
4

�
p

�
9
.9

�
1
0

�
4 .

A
c
ti

va
ti

o
n

s
a
re

re
c
o

rd
e
d

in
th

e
sa

m
e

ro
w

if
th

e
ir

fo
c
i

a
re

w
it

h
in

2
c
m

o
f

e
a
c
h

o
th

e
r;

so
m

e
c
o

n
tr

a
st

s
h

a
ve

m
u

lt
ip

le
fo

c
i

p
ro

x
im

a
te

to
fo

c
i

in
o

th
e
r

c
o

n
tr

a
st

s,
in

w
h

ic
h

c
a
se

,
th

e
fo

c
u

s
w

it
h

th
e

c
lo

se
st

m
a
x
im

u
m

to
th

e
o

th
e
rs

is
p

la
c
e
d

in
th

e
ro

w
w

it
h

th
e
m

.



Neuron
542

Figure 3. Post-Hoc Analysis (for General Ef-
fects of Beauty, along with Its Specific Con-
trasts)

Bilateral activation of the SLEA in the general
contrast of all faces versus baseline (first row)
and the general and specific effects of beauty
(rows 2–5). Rows 2 and 3 are the positive
and negative results of the general effect of
beauty (B versus A). Row 4 shows the positive
activation for the comparison of beautiful fe-
male faces versus average female faces (BF
versus AF), and the negative activation (row
five) for the comparison of beautiful male
faces versus average male faces (BM versus
AM). The SLEA activation (rectangles) in the
contrast of all faces versus baseline and the
general effect B versus A, coincided with
the foci of signal changes observed in the
comparison for the specific effects (BF versus
AF, and BM versus AM). Note that activations
in the specific contrasts are additive and are
thus observed in the general contrast.

age male conditions. Also, clusters in rows 2, 5, and 9 One focus of positive signal change and one focus of
negative signal change directly correspond to foci of(Table 2) contain ROIs A–C (Table 1A) of the random

effects analysis. positive and negative signal change observed in the
general contrast for beauty. In particular, activation inSpecific Effects for Beauty: Beautiful versus Average

Male Comparison. For this comparison, one focus of the VT and SLEA (see Figure 3 and Table 2, #C4 and
C9) is common to both. Also, clusters in rows 2 and 9significant positive signal change was identified in the

left VT (Table 2). Four clusters of significant negative (Table 2) contain ROIs A and C (Table 1A) of the random
effects analysis.signal change were further observed in the left SLEA

(n � 2), and the bilateral NAc/ventral striatum. The NAc/ General Effect of Gender: All Female versus All Male
Face Comparison. The general comparison of all femaleventral striatum foci had maxima in the ventral striatum

with their clusters covering the NAc (e.g., see Figure 3, versus all male faces revealed no foci of significant acti-
vation. Subthreshold foci of positive signal change werebottom row images for one such example).



Beauty and Reward
543

observed in the left amygdala, right hypothalamus, and tified measures of reward valuation, particularly for
beautiful male faces. This dissociation between assess-left VT. A subthreshold focus of negative signal change

was also observed in the left amygdala (Table 2). All of ments of attractiveness and quantified measures of re-
ward resembles that described by Berridge (1996, 2000)these foci of signal change coincided with foci of signal

change observed in the comparisons for the specific regarding the processes of “liking” and “wanting” (also
see Ariely and Loewenstein, 2000). Second, the key-effects that follow.

Specific Effect for Gender: Beautiful Female versus press procedure revealed that a category of visual stim-
ulus that is not linked to any post experiment asset orBeautiful Male Comparison. For this contrast, seven

clusters were observed with significant positive signal reward, namely beautiful female faces, can be rewarding
without being associated with any clear hedonic deficitchange in the left GOb, bilateral SLEA, left NAc/ventral

striatum, left NAc, and right VT (n � 2) (Table 2). One state.
Third, the fMRI experiment revealed a significant re-focus of subthreshold signal change was observed in

the right NAc. Three foci of significant negative signal sponse in the nucleus accumbens to the beautiful fe-
male faces by both random effects and fixed effectschange were observed in the bilateral GOb and left

SLEA, while one focus of subthreshold signal change analyses. The fixed effects analysis further indicated
that regions such as the ventral striatum proximate to thewas noted in the amygdala.

Although none of these activation clusters account NAc, along with the VT, SLEA, and GOb, also produced
significant activation with regard to the same stimulusfor the foci observed for the general effect of gender, five

of them directly overlap foci of opposite signal change conditions. Both the random effects (Figure 2) and fixed
effects analyses (Table 2) revealed relative positive sig-observed in the contrast of average female versus aver-

age male faces described below. An example of this nal changes in the NAc for heterosexual males viewing
rewarding faces (i.e., beautiful female versus averagecountervalanced signal change in the left NAc/ventral

striatum can be observed in Figure 4. Also, clusters in female conditions) and relative negative signal changes
for nonrewarding faces (i.e., beautiful male versus aver-rows 2, 5, and 9 (Table 2) contain ROIs A–C (Table 1A)

of the random effects analysis. age male conditions). These results have some analogy
to the negative deflection in BOLD signal reported forSpecific Effects for Gender: Average Females versus

Average Males. For this comparison, six foci of signifi- part of the NAc in response to painful thermal stimulation
versus a nonaversive baseline (Becerra et al., 2001).cant positive signal change were identified in the right

GOb (n � 2), left GOb (n � 2), right hypothalamus, and In conjunction with results of human neuroimaging
work using drug, gustatory, tactile, and monetary stim-left VT (Table 2). Subthreshold positive signal change is

observed in the bilateral amygdala and right VT. Regard- uli, these beauty results strongly support a fourth point,
that at the spatial scale of subcortical nuclei and theiring significant foci of negative signal change, three foci

are observed: in the right NAc, left NAc/ventral striatum, cortical projection fields, there appears to be a general-
ized circuitry processing rewarding stimuli.and left SLEA. One focus of subthreshold negative signal

change is noted in the left amygdala. Lastly, the fMRI data suggest a hypothesis for further
study regarding the potential effect of “liking” andOf these activation foci, three foci of positive signal

change and one of negative signal change directly corre- “wanting” on these brain reward regions (Berridge, 1996,
2000). Specifically, we observed patterns of activationspond to foci of subthreshold signal change observed

in the general contrast for gender. In particular, activa- from four of six ROIs in the NAc, SLEA, and VT that
generally follow the keypress results for the beautifultion in the amygdala, hypothalamus, and VT (Table 2,

#F4, F17, F18, F21) is common to both. The negative female, average female, and beautiful male conditions
(Figures 1C and 2). The observation of similar signalsignal change in the right NAc and left NAc/ventral stria-

tum (Table 2, #F1 and F2; see Figure 4), along with three profiles across multiple reward regions resembles re-
ports of similar signal changes across a distributed setother foci of negative and positive signal change (Table

2, #F9, F11, F13), directly overlay oppositely valanced of reward regions with money (Breiter et al., 2001). Al-
though the outcomes for the behavioral tasks and fMRIfoci of signal change in the contrast of attractive female

versus attractive male faces described above. It is also procedure were not perfectly symmetric, no reward re-
gion per se mirrored the outcomes of the rating experi-notable that clusters in rows 2, 5, and 9 (Table 2) contain

ROIs A–C (Table 1A) of the random effects analysis. ment (Figure 5). The fixed effects analysis supported the
random effects analysis by showing that components of
the NAc, SLEA, and VT paralleled the keypress data withDiscussion
regard to subtractions between the beautiful female,
average female, and beautiful male conditions (FigureOverview
5). These results suggest that reward regions respondThe goal of this study was to provide evidence for sepa-
primarily to the reinforcing characteristics of a subgrouprable measures of aesthetic versus rewarding qualities
of the faces rather than to their aesthetic components.in beautiful faces and to provide an initial understanding

of the neural mechanisms that underlie these qualities.
To reach this goal, we carried out both behavioral and Dissociation of Rewarding and Aesthetic

Behavioral ResponsesfMRI experiments involving the visual assessment of
beautiful and average faces. The results of these experi- Heterosexual male subjects rated beautiful male faces

as very attractive but did not expend effort to increasements produced five primary points.
First, the rating and keypress tasks revealed a dissoci- the viewing times of these faces. The most reasonable

inference is that they found them aesthetically pleasingation between assessments of attractiveness and quan-



Neuron
544

Figure 4. Post-Hoc Analysis (for General Effects of Gender, along with Its Specific Contrasts)

Activation of the left NAc in at least two of three contiguous brain slices for the contrast of all faces versus baseline (row 1) but not the general
effect of gender (rows 2 and 3 for positive and negative signal changes, respectively). Row 4 shows the positive signal changes from the
comparison of beautiful female faces versus beautiful male faces (BF versus BM), while row 5 shows the negative signal changes of the
comparison of average female faces versus average male faces (AF versus AM). Activation in the left NAc (in boxes) can be observed as foci
of opposite signal change (positive BF versus BM, and negative AF versus AM). This explains the absence of this activation in the general
effect of gender.

but not rewarding, in contrast to their ratings and behav- static, intrinsic property, but is rather a function of the
animal’s internal state at the time and of its past experi-ior regarding beautiful female faces. These observations

suggest that the ratings procedure and the keypress ence with the stimulus. Primary homeostatic functions
lead to drives such as eating, drinking, and thermal regu-procedure measure aesthetic value and reward value

respectively. The keypress results further indicate that lation on the basis of deficit states, or changes in physio-
logical conditions. In the current study, the beautifulvisual stimuli can have reward value by an objective

measure, namely work performed to increase or de- female faces were rewarding without reference to a spe-
cific deficit state, post experiment asset position, orcrease exposure time to different images. In general,

the reward value associated with a stimulus is not a object that could potentially impact on internal physio-



Beauty and Reward
545

men like to watch beautiful women’s faces; however, it
was not obvious that this class of stimuli would activate
the classical reward circuitry that has previously been
associated with drug rewards, homeostatic rewards,
and monetary rewards, all of which have direct physio-
logical implications or can be readily transformed into
goal-objects with physiological effects. This is a critical
issue since many literatures outside of neuroscience
consider facial attractiveness as a social construct that
is not necessarily tied into the function of fundamental
reward circuitry (reviewed in Etcoff, 1999).

In the random effects analysis of ROI data from the six
targeted reward regions, only the NAc met our corrected
statistical threshold and produced subsequent pair-
wise comparisons for contrasts involving signal col-
lected during the observation of beautiful female faces.
The NAc, like the fusiform gyrus (GF), was one of the
few brain regions to even meet a Bonferroni thresholdFigure 5. A Summary of the Behavioral and BOLD Signal Results
(p � 7.1 � 10�6) for the general contrast of all facefor the Specific Effects of Beauty and Gender
conditions versus baseline used in the ROI-selectionThe left table in the figure shows “p � 0.05” when the difference in

the results from the rating and keypress tasks is statistically signifi- procedure (Breiter et al., 1997, 2001). The NAc achieved
cant and shows “NS” when it is not. The table on the right describes this despite having counterposed activation for condi-
the BOLD signal changes in the following reward regions: (1) right tions that were nonrewarding versus conditions that
NAc (activation clusters listed in row 1 of Table 2), (2) region of the were rewarding (see Figure 4). In contrast to the NAc,
left ventral striatum proximate to the NAc, including the NAc (NAc/

the fusiform gyrus (GF) evidenced two foci of BOLDVS) (this includes the maxima that was localized in the NAc via the
signal change in the comparison of all face conditionsROI selection procedure for the random effects analysis as ROI A
versus baseline; however, the sex by beauty interactionin Table 1A, and the cluster localized over a larger area from the

fixed effects analysis that is listed in row 2 of Table 2), (3) left SLEA was not significant for either of these ROIs in the analysis
(this is ROI C in Table 1A that was localized in the SLEA via the of variance. BOLD signal change in the GF in response
ROI selection procedure for the random effects analysis, and the to faces has been reported to be affected by alterations
activation clusters listed in row 9 of Table 2 from the fixed effects

in attention (Wojciulik et al., 1998). The absence of signif-
analysis), and (4) right and left VT (this is ROI B in Table 1A that

icant contrasts between conditions in the GF for thiswas localized in the right VT via the ROI selection procedure for the
sample of subjects argues that the significant effectsrandom effects analysis, and the activation clusters in rows 5 and

4 of Table 2 from the fixed effects analysis for the right and left VT, observed in the NAc were not strictly due to differences
respectively). Activation in brackets were subthreshold per Table in subject attention to stimuli.
2. In viewing this summary table, it is important to consider the Given the keypress results, the observation of NAc
comparisons as tentative, since there is not perfect parallelism be-

activity in response to beautiful female faces implicates
tween the behavioral data and imaging data (see Discussion). With

it in the assessment of reward value. Since the classicthis in mind, the BOLD signal in the NAc, NAc/ventral striatum (NAc/
formulation of a dedicated reward circuitry (Wise et al.,VS), SLEA, and VT produce positive signal changes when p � 0.05
1978; Louilot et al., 1989), the meso-accumbens dopa-for the keypress task (emphasized with text in bold tone). These

regions also alternate signal valence across conditions, while VT mine pathway has been considered a central component
activation switches laterality; these observations suggest a need of circuitry processing the reinforcing effects of most
for greater dynamic range in the behavioral tasks to fully determine goal-objects. Recent work further suggests that the NAc
their correspondence with reward circuitry signal change.

has complex reward functions, including the assess-
ment of reward expectancy (Schultz et al., 1997; Berns
et al., 1997; Breiter and Rosen, 1999; Breiter et al., 2001;

logical signals. Further work is clearly needed to evalu- Schultz and Dickinson, 2000; Knutson et al., 2001). The
ate alliesthesia effects (Cabanac, 1971, 1979) for this current work extends the set of categories of stimuli
category of stimuli. Further behavioral tasks are also producing NAc activity beyond homeostatic, monetary,
needed to evaluate informational features not assessed and drug rewards, to include rewards with direct social
in the current study. For instance, it is possible that relevance, such as beautiful faces.
young heterosexual males experience the perception Fixed effects analysis of averaged data was further
of beautiful males in a more aversive fashion than the performed to determine if other reward regions pro-
perception of average males, as suggested by the corre- duced differential patterns of activation that paralleled
spondence of NAc signal change between beautiful the dissociation of effects for the beautiful face condi-
male and average male faces, to NAc signal change tions in the behavioral studies. Indeed, distinct profiles
between aversive and nonaversive thermal stimuli (Be- of signal change were observed for the general contrasts
cerra et al., 2001). regarding beauty and gender in other reward regions

besides the NAc and proximate ventral striatum (i.e.,
Reward Circuitry Activation to Facial Stimuli NAc/ventral striatum), namely the SLEA, VT, and GOb.
One goal of this study was to determine if beautiful Of these regions, no focus of signal change met our
faces, or a subgroup thereof, motivated behavior on post-hoc corrected statistical threshold for the general
one hand, while on the other producing reward circuitry effect of gender (Table 2). This appears to be partly due

to the counterposing of activations (see Figure 4) in theactivity when passively observed. It is not surprising that



Neuron
546

specific contrasts of beautiful women versus beautiful effects analysis in that three of these clusters overlap
men and average women versus average men (Table 2), ROIs in the NAc(A), VT(B), and SLEA(C) used in the ran-
thus reducing their additive effect for the general effect dom effects analysis (Table 1A and Figure 2). If one
of gender. In the case of beauty, the general effect looks at all of the contrasts for the specific effects of
largely reflected additive inputs (see Figure 3) between beauty and gender, one notes that the BOLD signal in
responses for beautiful women versus average women the NAc, NAc/ventral striatum, and SLEA alternate signal
and beautiful men versus average men (Table 2). valence across conditions, while VT activation switches

Alongside the observations in the NAc, NAc/ventral laterality (Table 2 and Figure 5). Suggestions that these
striatum, and VT, the post-hoc observations of signal activations follow the outcomes of the keypress task
change in the GOb and SLEA is consistent with exten- are not warranted, though, since there is a potential
sive animal experimentation. GOb neurons in the rat discrepancy between BOLD signal produced in the NAc,
(Schoenbaum et al., 1999) and monkey (Rolls, 1999; SLEA, and VT (e.g., ROIs A–C in Figure 2) during the
Schultz and Dickinson, 2000) fire during the anticipation average male condition and the keypress results for that
and experience of positive and negative outcomes. Fur- experimental condition (Figure 1C). Behavioral work to
thermore, the responses of GOb neurons may represent characterize responses to the average male faces may
relative reward preferences (Schultz and Dickinson, be helpful in this regard. Furthermore, future studies
2000). This latter observation has particular relevance with more sensitive behavioral experiments might con-
to the current data showing GOb activation for subtrac- sider use of the same subjects for both behavioral and
tions involving beautiful female faces compared to other imaging tasks to allow quantitative evaluation via multi-
face conditions. The presence of GOb activity in the variate analysis of these observations.
average female versus average male subtraction may The keypress task indicated a significant difference
also be similarly interpreted if one assumes the behav- between categories of faces when one of the categories
ioral tasks did not have enough dynamic range to distin- was that of the beautiful female faces (which was the
guish a preference for average females over average only condition to be positively reinforcing). The other
males. Alternately, the GOb activation associated with three categories of faces were actively suppressed (thus
this contrast could reflect the assessment of conflict indicating that they were mildly aversive). The presence
between options connected to the stimuli, as has been of positive and negative NAc signals for contrasts involv-
shown to be important for choices between gambling ing reinforcing rewards versus contrasts involving non-
positions (Bechara et al., 1998). rewards (i.e., aversive outcomes) has an intriguing paral-

Neurons in the SLEA are activated by rewarding brain lel to data indicating positive BOLD signal changes to
stimulation in the rat (Arvanitogiannis et al., 1996, 2000; rewards (such as cocaine and morphine; Breiter et al.,
Flores et al., 1997; Nakahara et al., 1999; Shizgal, 1997). 1997, 2000), and the report of negative BOLD signal
Furthermore, lesions of the SLEA reduce the rewarding changes to painful stimuli (Becerra et al., 2001). Given
effect of stimulation to the medial forebrain bundle (Ar- that the changes in signal observed for rewarding and
vanitogiannis et al., 1996), reduce cocaine self-adminis- nonrewarding outcomes is dependent on expectancy
tration (Robledo and Koob, 1993), and disrupt operant conditions (Breiter et al., 2001), such differences in sig-
performance for sucrose pellets in rats (Brown et al., nal valence in the NAc and other reward regions may not
1996). Data from other human studies also suggests that be absolute but represent a relative ordering of signal
the SLEA, GOb, and VT may respond to nonrewarding associated with the experimental conditions.
stimuli: transient activation in these regions has been
reported following painful thermal stimulation (Becerra

General Circuitry of Reward and Its Activityet al., 2001).
during Aesthetic AssessmentThe patterns of signal change observed in reward
A similar set of brain reward regions appears to respondregions with the random effects and the fixed effects
in common to very distinct categories of reward. At theanalyses suggest some potential parallels with the be-
spatial scale offered by current neuroimaging methodol-havioral tasks (Figures 1C, 2, and 5). Such comparisons
ogy, at least five brain regions (plus or minus the hypo-must be considered tentative since there is not perfect
thalamus, and the ventral striatum proximate to the NAc)parallelism between the behavioral data and imaging
have been implicated in the perceptual assessment ofdata in that the imaging data has a broader scale of
rewarding stimuli. In particular, the NAc, SLEA, amyg-measurement and thus greater sensitivity (suggesting a
dala, GOb, and VT have all been implicated in expec-need for greater sensitivity of measurement in future
tancy functions (Breiter et al., 2001) and to various de-behavioral tasks). Signal change from some of the ROIs
grees in the processing of positive and negative(e.g., ROIs A–D from Table 1A and Figure 2) used in the
outcomes. In human neuroimaging studies, stimuli lead-random effects analysis suggest a qualitative similarity
ing to significant signal changes in these regions haveto a subset of results from the keypress procedure (i.e.,
included drugs such as cocaine, nicotine, amphetamine,the beautiful female, average female, and beautiful male
and morphine, pleasant or aversive tastants, pleasantconditions) (Figure 1C). The results of the fixed effects
tactile stimuli, and monetary rewards (Berns et al., 2001;analysis support this observation, in that clusters of
Breiter et al., 1996b, 1997, 1998, 2000, 2001; Breiter andactivation in the right NAc (row 1 of Table 2), left NAc/
Rosen, 1999; Delgado et al., 2000; Drevets et al., 2001;ventral striatum (row 2 of Table 2), left SLEA (row 9 of
Elliott et al., 2000; Francis et al., 1999; Knutson et al.,Table 2), and right VT (row 5 of Table 2) produce positive
2000, 2001; O’Doherty et al., 2001; Rogers et al., 1999;signal changes for comparisons between conditions
Small et al., 2001; Stein et al., 1998; Thut et al., 1997;that are significant for the keypress task (Figure 5).

These results support the observations of the random Zald et al., 1998). Such congruence of findings between



Beauty and Reward
547

brain regions producing responses at the spatial scale Limitations
A number of limitations apply to this fMRI study (seeof cubic millimeters of tissue and reward stimuli that
Breiter et al., 1996a, 1996c, 1997, 2001). These issuesinduce activity in these brain regions supports the thesis
include the limited signal-to-noise ratios of BOLD sig-of a common generalized circuitry that processes re-
nals recorded from small subcortical structures, spatialward information across category and dissects discrete
resolution after data analysis, and magnetic suscepti-features of such stimuli for the planning of behavior
bility.(Breiter and Rosen, 1999; Breiter et al., 2001). Future

Particular to this study, it is important to note thatstudies face the challenge of dissecting the relative con-
participants in all three experiments were young hetero-tributions of these distributed brain regions to the as-
sexual males. Recent evidence suggests that women’ssessment of reward and aversion, and the organization
facial preferences may change across the menstrualof behavior around these assessments.
cycle. Penton-Voak et al. (1999) have found that womenTogether with the contrasting results of the rating and
in the follicular phase of the menstrual cycle are morekeypress procedures, our fMRI results suggest a hy-
attentive to phenotypic markers indicating immunocom-pothesis that aesthetic evaluation may be separate from
petence and therefore prefer stereotypically “mascu-reward assessment; although both might follow a com-
line” faces more than they do at other times of theirmon early step in valuation of potential goal-objects (i.e.,
cycle. Given the more complex results of human femaleof their reward intensity) (Breiter and Rosen, 1999). Initial
preferences, we decided to conduct this initial investiga-inspection of results from the fixed effects analysis sug-
tion with male subjects only. Thus, these results shouldgests that the VT, SLEA, and GOb may be associated
not be generalized to women, nor to individuals with awith the general effect of beauty. Of these regions, one
different sexual orientation.focus in the SLEA (Table 2, #A8), in particular, is unique

Finally, it is possible that the difference between theto the general effect and cannot be accounted for by
two behavioral tasks was not caused by a differencethe subsequent specific effects. Such an interpretation
between aesthetic evaluations and motivation but ratherwould be supported by the fact that the SLEA and VT
was a result of scaling changes in the ratings task. It

share connections through the medial forebrain bundle,
is possible that when using ratings as the response

which is an important site of brain stimulation reward
measure, our subjects rated males relative to other

effects (Olds and Milner, 1954) and has been theorized
males and females relative to other females (Ariely and

to be important for assessment of reward intensity (Shiz-
Loewenstein, 2000). The keypress method does not suf-

gal, 1999). VT dopamine neurons have also been inter-
fer from this changing scale problem because effort is

preted to respond to salient sensory events, regardless
a scale that is constant across all images presented.

of their relationship to reward (Breiter et al., 2001; Hor-
Further work is needed in order to better understand if

vitz, 2000).
the rating task results are a response language artifact

Arguing against a common basis for aesthetic and or a real effect.
reward assessments, though, is the observation that of
the two behavioral tasks, only the keypress procedure

Conclusion
produced responses that paralleled to some degree re-

This study sought to determine if social stimuli distinct
sponses in reward regions such as the NAc, SLEA, and

from money, namely categories of faces segregated by
VT (Figures 1C, 2, and 5). No reward region responded

gender and attractiveness, had different reward values,
in a similar fashion to the outcomes of the rating proce-

and in turn induced reward circuitry activity when ob-
dure. These results are consistent with predictions of served. The keypress procedure demonstrated that a
the incentive salience or Bindra/Toates model described social stimulus that was not linked to any post experi-
by Berridge and colleagues (Berridge, 1996, 2000), ment asset or reward, had a distinct valuation that could
which discusses “wanting,” but not “liking,” in terms of be objectively quantified. fMRI of subjects passively
meso-accumbens dopaminergic function (Wyvell and viewing these faces demonstrated a significant effect
Berridge, 2000). by analysis of variance across individual subjects in the

A longstanding debate in aesthetics concerns the NAc, particularly in response to the beautiful female
question of whether perception of beauty can be “disin- faces. By the post-hoc analysis, no one region re-
terested,” or separate from desire (Kant, reprinted 1960). sponded in a similar fashion to the rating study alone,
The post-hoc analysis of our data did not show com- but a number of reward regions produced signal change
pletely separated patterns of activation in reward re- with approximate similarity to the keypress data. These
gions for aesthetic assessments and reward assess- results suggest that aesthetic judgement may not be
ments, but instead demonstrated a set of regions that mediated by reward systems.
resembled aspects of the keypress results alone. This The observations of this study build upon prior neuro-
suggests that beautiful faces produce a valuation signal imaging work with multiple categories of reward stimuli
(potentially involving the SLEA), which is processed in to argue that, at the spatial resolution of current imaging
different brain regions for reward functions and aes- techniques, an extended set of deep gray matter and
thetic judgements in young heterosexual male subjects. paralimbic regions serves as a generalized circuitry to
Given that it may be particularly difficult to dissociate process goal-related stimuli. In a previous study using
rewarding from aesthetic effects with faces, future stud- monetary reward and a game of chance, our group ob-
ies with non-face stimuli and nonbiological categories served this extended set of reward regions to display
of goal-objects may help determine if these effects are differential activation to expectancy conditions and to

the monetary gains and losses embedded in themdissociable.



Neuron
548

selected from print media. Each set consisted of 20 male and 20(Breiter et al., 2001). The segregation of expectancy and
female faces.outcome responses demonstrated that reward/motiva-

tion systems could be dissected into their constituent
Experimental Designfunctional subsystems, but left open the issue of their
Behavioral Tasks

involvement in valuation processes. The current study
Rating Procedure. The rating task measured the attractiveness of

suggests that the same set of regions implicated in the the female and male faces for the experimental subjects. Subjects
processing of expectancies and outcomes, may also be viewed the 80 faces three times each, on each occasion rating each

face’s “attractiveness” on a scale of 1–7, with 1 representing “veryinvolved with valuation functions. A challenge for future
unattractive” and 7 representing “very attractive.” Faces were orga-work is to determine the varied contributions of this
nized in blocks by gender, and the order of gender was counterbal-distributed set of reward regions to the processes of
anced across subjects. Within each block (by gender), the 40 beauti-

expectancy, valuation, and their combination for moti-
ful and average faces were always presented in a new randomly

vation. generated order.
Studies are further warranted to address issues raised Keypress Procedure. The keypress task examined the reward

value of average and beautiful faces. Subjects were told that theyby the design and focus of the current work. For in-
would be exposed to a series of pictures that if not interfered with,stance, there is the issue that differences in the gender
would change every eight seconds. However, if they wanted a pic-or sexual orientation of the volunteers used for this study
ture to disappear faster, they could alternate pressing the “z” and

might lead to different behavioral and imaging results.
“x” keys, whereas if they wanted a picture to stay longer on the

The signals from reward regions in response to average screen, they could alternate pressing the “n” and “m” keys. The
male faces did not resemble the results of the two be- dependent measures of interest were the amount of work in units

of key press that subjects exerted in response to the different cate-havioral tasks, suggesting the need for assessing other
gories of stimuli, and their resulting viewing durations.subjective dimensions. Another question arises about

Each pair of keypresses increased or decreased the total viewingwhether the results produced by beautiful faces general-
time according to the following formula:

ize to those produced by bodies, or nonanimate stimuli.
Lastly, there is the issue of what brain regions might NewTotalTime � OldTotalTime � (ExtremeTime �
process information regarding “aesthetic” beauty (i.e.,

OldTotalTime)/K,
follow the pattern of the rating task results), as opposed
to processing information regarding “desirable” beauty. where ExtremeTime was 0 s for keypresses reducing the viewing

time, ExtremeTime was 16 s for keypresses increasing the viewingIn pursuing these issues regarding brain function, it is
time, and K was a scaling constant set to 40. If the elapsed timepossible we may begin to approach an understanding
for the picture surpassed the total time determined by keypressing,of Ruskin’s concept of the “sublime” (reprinted 1997)
the picture was removed and the next trial began. A “slider” was

with regard to the grandeur imbedded in the function
displayed left of each picture indicating total viewing time at any

of motivation. moment, and changing with every keypress (Ariely et al., 2001). This
procedure was controlled by Authorware (Macromedia).

Subjects were informed that the task would last 40 min and thatExperimental Procedure
this length was independent of their behavior during the task, as
was their overall payment of $14.Subjects
NeuroimagingAll subjects in the three experiments gave informed consent to
Subject Instructions Prior to Scanning. Subjects were told that theyparticipate in these procedures following the rules of the Subcom-
would see rapid presentations of faces intermixed with fixationmittee on Human Studies at the Massachusetts General Hospital,
points, that sometimes the faces would change, and that they werethe Institutional Review Board at the Massachusetts Institute of
to focus on the fixation points while getting an overall sense ofTechnology, and the Institutional Review Board at Harvard Uni-
the faces. One to two minutes prior to imaging, subjects viewed aversity.
separate set of average faces with neutral expressions for imageBehavioral Tasks
focusing and centering.A group of eight male subjects, ages 21–35 years (mean 24.0, SD

Functional Imaging. Subjects were scanned on an Instascan de-4.4), all heterosexual and right-handed by self-report, participated
vice (3 T General Electric Signa, modified by Advanced NMR Sys-in the rating study, and were paid $15. A separate group of fifteen
tems) using a head coil, bite-bar, and standard protocol (Breitermale subjects between the ages of 21 and 25 years (mean 23.0, SD
et al., 2001). This protocol included: (1) a sagittal localizer scan2.3), also all heterosexual and right-handed by self-report, partici-
[conventional T1-weighted spoiled gradient refocused gradientpated in the “keypress” study and were paid $14 for their partici-
echo (SPGR) sequence; through-plane resolution � 2.8 mm; 60pation.
slices] to orient, for subsequent scans, 16 contiguous axial obliqueNeuroimaging
7 mm slices along the AC-PC line, (2) an automated shimming routineTen male volunteers, who had not participated in the behavioral
with second order shims to optimize magnetic field homogeneitytasks, volunteered for the fMRI experiment. All subjects were medi-
(mean FWHM � 26.6Hz, SD 2.6), (3) an SPGR T1-weighted flow-cally, neurologically, and psychologically normal by self-report and
compensated scan (resolution � 1.6 mm � 1.6 mm � 7 mm), (4) aphysician-directed medical review of systems. All subjects were
T1-weighted echo planar inversion recovery sequence (TI � 1200right-handed and heterosexual by self-report. fMRI data collected
ms, in-plane resolution � 1.6 mm), and (5) a gradient echo, T2*-from three participants had significant signal spiking, along with
weighted functional sequence (TR � 2000 ms, TE � 30 ms; flip �uncorrectable motion, and could not be analyzed; data from one
60�; FOV � 40 � 20 cm; in-plane resolution � 3.125 mm; 110participant was excluded due to noncompliance with instructions.
images per slice; disdaq � 4).The six remaining participants were aged 21–28 (mean 25.2, SD 2.5).

Experimental Paradigm. Each experimental run included five 28 s
baseline epochs interleaved with four 20 s face epochs (e.g., block
design). To minimize attentional modulation of gaze (Breiter et al.,Stimuli

Two sets of 40 nonfamous human faces [digitized at 600 dpi in 8-bit 1996a), face stimuli were presented in a tachistoscopic fashion for
200 ms (face, or empty oval with a fixation point for baseline), fol-grayscale, spatially downsampled, and cropped to fit in an oval

“window” sized 310–350 pixels wide by 470 pixels high using Pho- lowed by a blank screen for 3800 ms. During each run, either male
or female faces were presented, with alternating epochs of averagetoshop 4.0 software (Adobe Systems)] classified as “beautiful” and

“average” (according to pilot test results) (see Figure 1A), were and beautiful faces. Epochs of average and beautiful faces were



Beauty and Reward
549

counterbalanced within run, with an *A*B*B*A* or *B*A*A*B* order an overall � � 0.05, activation clusters had to meet a corrected p
value threshold (Breiter et al., 1996a, 1996c, 2001) for the volume(A � average, B � beautiful, * � fixation point baseline). The gender

of the faces shown and block sequence was counterbalanced of tissue (30.97cc) sampled in the six a priori regions (i.e., p � 0.05/
453 voxels, or p � 1.1 � 10�4) (Makris et al., 1999).across the eight runs administered to each subject. This resulted

in each face being viewed twice. A break of approximately 2–4 min Anatomic Localization
Statistical maps of group-averaged data were superimposed overwas taken between runs.

Subject Debriefing. After functional imaging, subjects filled out a high-resolution conventional T1-weighted images that had been
transformed into the Talairach domain and averaged. Primary ana-questionnaire about what they had seen and thought, and com-

pleted the Beck Anxiety and Depression Inventories (BAI: mean 2.2, tomic localization of activation foci was based on the Talairach
coordinates (Talairach and Tournoux, 1988) of the maximum voxelSD 1.7, range 0–4 out of 63; BDI: mean 3.7, SD 3.8, range 0–12 out

of 63). Three of the six subjects spontaneously reported noticing from each activation cluster, with secondary confirmation of this via
inspection of the juxtaposition of statistical maps with structuralthat the faces differed in attractiveness.
scans. Localization followed the region of interest conventions de-
scribed previously (Breiter et al., 1997) for the NAc, SLEA, amygdala,

Data Analysis hypothalamus, VT, and GOb (BA 11/47) (Breiter et al., 2001), and
Transformation of fMRI BOLD Data before the ventral striatum proximate to the NAc (Drevets et al., 2001). All
Statistical Mapping clusters of activation were checked against the functional image
Motion Correction and Talairach Transformation. These procedures data using an objective method to ascertain that they did not overlap
followed those detailed elsewhere (Breiter et al., 2001). any areas of susceptibility artifact (Breiter et al., 1997, 2001).

Signal Normalization and Filtering. For all eight runs, fMRI data
in the Talairach domain were intensity scaled on a voxel-by-voxel

Acknowledgments
basis to a standard value of 1000 and detrended. The mean signal
intensity for each voxel over all runs was removed on a time point

This work was supported by grants to Dr. Breiter from the National
by time point basis.

Institutes of Drug Abuse (grants #00265 and #09467), the Office of
Concatenating and Averaging across Subjects. Pairs of identical

National Drug Control Policy and Counterdrug Technology Assess-
110-time point runs of Talairach-transformed functional data were

ment Center (ONDCP-CTAC), and Drs. Breiter and Aharon from the
averaged within each subject (i.e., given four types of runs—female

National Center for Responsible Gaming (NCRG). Dr. Breiter was
faces: *A*B*B*A*, female faces: *B*A*A*B*, male faces: *A*B*B*A*,

also supported by the National Foundation for Functional Brain Im-
male faces: *B*A*A*B*). The resulting four average runs were concat-

aging. Dr. Etcoff was supported by the Lynn M. Reid Fellowship of
enated within each subject. These 440 time point sequences were

Harvard Medical School, and Dr. Chabris by a postdoctoral fellow-
then averaged across subjects, as were individual structural images.

ship from the National Institutes of Health through the MGH-NMR
Statistical Mapping, ROI-Based Analysis

Center. We would like to thank Alex Pentland and Elizabeth Huffman
Statistical Mapping of General Effects as ROIs. Individual data was

for their help and assistance and Mark E. Glickman for statistical
evaluated to confirm the presence of a normal signal distribution.

consultation.
Then, a t statistic map was created from the data averaged across
subjects, using time point (n � 440) as the random factor, and

Received June 5, 2001; revised October 12, 2001.contrasting all time points during face events versus all time points
during fixation point events.

ReferencesWithin this map, clusters of activation that had maxima (i.e., mini-
mum p value) in one of the six targeted reward regions were identi-
fied using a cluster-growing algorithm (Bush et al., 1996), and se- Ariely, D., and Loewenstein, G. (2000). The importance of duration
lected as ROIs for analyses of variance with subject (n � 6) as the in ratings of, and choices between, sequences of outcomes. J. Exp.
random factor (i.e., “random effects” analysis). In order to maintain Psychol. 129, 508–523.
an overall � � 0.05, this algorithm specifically localized activations Ariely, D., Breiter, H.C., and Aharon, I. (2001). From mice to men: a
that met a corrected p value threshold of p � 0.0083 for the number continuous measurement of motivation. MIT Working Paper 4158.
of hypothesized brain regions interrogated (0.05/6 � 0.0083). See

Arvanitogiannis, A., Waraczynski, M., and Shizgal, P. (1996). Effects
Breiter et al. (2001) for specific cluster constraints.

of excitotoxic lesions of the basal forebrain on MFB self-stimulation.
Hypothesis Testing of Individual Data: ANOVAs and Paired Con-

Physiol. Behav. 59, 795–806.
trasts. ROIs in targeted reward regions were then used to sample

Arvanitogiannis, A., Tzschentke, T.M., Riscaldino, L., Wise, R.A., andsignal (as percentage signal change) from each of the eight runs in
Shizgal, P. (2000). Fos expression following self-stimulation of theeach subject. Separate, repeated-measures analyses of variance
medial prefrontal cortex. Behav. Brain Res. 107, 123–132.for each ROI were computed, with Gender (male or female) and

Attractiveness (beautiful or average) as the dependent measures. Bartels, A., and Zeki, S. (2000). The neural basis of romantic love.
The result of primary interest in the ANOVA was the gender � attrac- NeuroReport 11, 3829–3834.
tiveness interaction. Given that ANOVAs were carried out for six Becerra, L., Breiter, H.C., Wise, R., Gonzalez, R.G., and Borsook,
different ROIs in hypothesized reward regions, we used a more D. (2001). Activation of reward circuitry following noxious thermal
stringent � level (p � 0.0083). In cases that met the criterion � level, stimuli. Neuron, in press.
the pair-wise contrasts were computed (Table 1).

Bechara, A., Damasio, H., Tranel, D., and Anderson, S.W. (1998).Statistical Mapping, Post-Hoc Voxel-by-Voxel Parametric
Dissociation of working memory from decision making within theAnalysis on Averaged Data
human prefrontal cortex. J. Neurosci. 18, 428–437.A post-hoc analysis on the averaged data was undertaken on a
Berns, G.S., Cohen, J.D., and Mintun, M.A. (1997). Brain regionsvoxel-by-voxel basis to check for potential activations missed in
responsive to novelty in the absence of awareness. Science 276,the ROI-based analysis (see “Data from Neuroimaging” in Results).
1272–1275.Parametric statistical maps (using voxel-by-voxel t tests) were gen-

erated on data that had been averaged by the four types of runs Berns, G.S., McClure, S.M., Pagnoni, G., and Montague, P.R. (2001).
across subject and concatenated. Prior to concatenation, functional Predictability modulates human brain response to reward. J. Neu-
data were intensity scaled (i.e., normalized to the first run). General rosci. 21, 2793–2798.
contrasts were computed for all beautiful face conditions versus all

Berridge, K.C. (1996). Food reward: brain substrates of wanting and
average face conditions (i.e., general effect of beauty) and for all

liking. Neurosci. Behav. Rev. 20, 1–25.
female faces versus all male faces (i.e., general effect for gender).

Berridge, K.C. (2000). Reward learning: reinforcement, incentivesThe four specific contrasts following off of these general effects are
and expectations. In The Psychology of Learning and Motivation,listed in Table 2.
Vol. 40. D.L. Medin, ed. (New York: Academic Press).Clusters of positive and negative signal change were identified

for each contrast in the six targeted regions. In order to maintain Breiter, H.C., and Rosen, B.R. (1999). Functional magnetic reso-



Neuron
550

nance imaging of brain reward circuitry in the human. Ann. NY Acad. Frieze, I.H., Olson, J.E., and Russell, J. (1991). Attractiveness and
income for men and women in management. J. Appl. Soc. Psychol.Sci. 877, 523–547.
21, 1039–1057.Breiter, H.C., Etcoff, N.L., Whalen, P.J., Kennedy, W.A., Rauch, S.L.,

Buckner, R.L., Strauss, M.M., Hyman, S.E., and Rose, B.R. (1996a). Gallistel, C.R. (1990). The Organization of Learning (Cambridge, MA:
Response and habituation of the human amygdala during visual MIT Press).
processing of facial expression. Neuron 17, 875–887. Grammer, K., and Thornhill, R. (1994). Human (Homo sapiens) facial
Breiter, H., Berke, J., Kennedy, W., Rosen, B., and Hyman, S. (1996b). attractiveness and sexual selection: the role of symmetry and aver-
Activation of striatum and amygdala during reward conditioning: an ageness. J. Comp. Psychol. 108, 233–242.
fMRI study. Neuroimage 3, S220. Hamermesh, D.S., and Biddle, J.E. (1994). Beauty and the labor
Breiter, H.C., Rauch, S.L., Kwong, K.K., Baker, J.R., Weisskoff, R.M., market. American Economic Review 84, 1174–1194.
Kennedy, D.N., Kendrick, A.D., Davis, T.L., Jiang, A., Cohen, M.S.,

Horvitz, J.C. (2000). Mesolimbocortical and nigrostriatal dopamine
et al. (1996c). Functional magnetic resonance imaging of symptom

responses to salient non-reward events. Neuroscience 96, 651–656.
provocation in obsessive-compulsive disorder. Arch. Gen. Psychia-

Jones, D.M., and Hill, K. (1993). Criteria of facial attractiveness intry 53, 595–606.
five populations. Human Nat. 4, 271–296.

Breiter, H.C., Gollub, R.L., Weisskoff, R.M., Kennedy, D.N., Makris,
Kant, I. (1960). Observations on the Feeling of the Beautiful andN., Berke, J.D., Goodman, J.M., Kantor, H.L., Gastfriend, D.R., Rior-
Sublime (Trans. Goldthwait, J.T.U. California Press, originalden, J.P., et al. (1997). Acute effects of cocaine on human brain
1763–64).activity and emotion. Neuron 19, 591–611.
Kanwisher, N., McDermott, J., and Chun, M. (1997). The fusiformBreiter, H.C., Gollub, R.L., Edmister, W., Talavage, T., Makris, N.,
face area: a module in human extrastriate cortex specialized for theMelcher, J., Kennedy, D., Kantor, H., Elman, I., Riorden, J., et al.
perception of faces. J. Neurosci. 17, 4302–4311.(1998). Cocaine induced brainstem and subcortical activity ob-

served through fMRI with cardiac gating. Paper presented at: Inter- Knutson, B., Adams, C.M., Fong, G.W., and Hommer, D.J. (2001).
national Society for Magn. Reson. Med. (Sydney, Australia). Anticipation of increasing monetary reward selectively recruits nu-

cleus accumbens. J. Neurosci. 15, 1–5.Breiter, H.C., Becerra, L., Gonzalez, R.G., Jenkins, L., Huffman, E.,
Harter, K., Comite, A., and Borsook, D. (2000). Morphine induced Knutson, B., Westdorp, A., Kaiser, E., and Hommer, D. (2000). FMRI
reward and pain circuitry activation in drug naı̈ve humans. Paper visualization of brain activity during a monetary incentive delay task.
presented at: American Pain Society (Atlanta, USA). Neuroimage 12, 20–27.
Breiter, H.C., Aharon, I., Kahneman, D., Dale, A., and Shizgal, P. Langlois, J.H., Roggman, L.A., Casey, R.J., Ritter, J.M., Rieser-Dan-
(2001). Functional imaging of neural responses to expectancy and ner, L.A., and Jenkins, V.Y. (1987). Infant preferences for attractive
experience of monetary gains and losses. Neuron 30, 619–639. faces: rudiment of a stereotype? Dev. Psychol. 23, 363–369.
Brown, V.J., Latimer, M.P., and Winn, P. (1996). Memory for the Langlois, J.H., Ritter, J.M., Riggman, L.A., and Vaughn, L.S. (1991).
changing cost of a reward is mediated by the sublenticular extended Facial diversity and infant preferences for attractive faces. Dev.
amygdala. Brain Res. Bull. 39, 163–170. Psychol. 27, 79–84.
Bush, G., Jiang, A., Talavage, T., and Kennedy, D. (1996). An auto- Louilot, A., Taghzouti, K., Simon, H., and LeMoal, M. (1989). Limbic
mated system for localization and characterization of functional MRI system, basal ganglia and dopaminergic neurons. Brain Behav. Evol.
activations in four dimensions. Paper presented at: Second Interna- 33, 157–161.
tional Conference on Functional Mapping of the Human Brain (Or-

Makris, N., Meyer, J.W., Bates, J.F., Yeterian, E.H., Kennedy, D.N.,lando, FL, Academic Press).
and Caviness, V.S. (1999). MRI-based topographic parcellation of

Cabanac, M. (1971). Physiological role of pleasure. Science 173,
human cerebral white matter and nuclei II. Rationale and applica-

1103–1107.
tions with systematics of cerebral connectivity. Neuroimage 9,

Cabanac, M. (1979). Sensory pleasure. Q. Rev. Biol. 54, 1–29. 18–45.
Cunningham, M., Roberts, A.R., Barbee, A.P., Cruen, P.B., and Wu, Marlowe, C.M., Schneider, S.L., and Nelson, C.E. (1996). Gender
C.-H. (1995). Consistency and variability in the cross-cultural per- and attractiveness biases in hiring decisions: are more experienced
ception of female physical attractiveness. J. Personality and Social managers less biased? J. Appl. Psychol. 81, 11–21.
Psychol. 68, 261–279.

Morris, J.S., Frith, C.D., Perrett, D.I., Rowland, D., Young, A.W.,
Delgado, M.R., Nystrom, L.E., Fissell, K., Noll, D.C., and Fiez, J.A. Calder, A.J., and Dolan, R.J. (1996). A differential neural response
(2000). Tracking the hemodynamic responses for reward and pun- in the human amygdala to fearful and happy facial expression. Na-
ishment in the striatum. J. Neurophys. 84, 3072–3077. ture 383, 812–815.
Drevets, W.C., Gautier, C., Price, J.C., Kupfer, D.J., Kinahan, P.E., Nakahara, D., Ishida, Y., Nakamura, M., Kuwahara, I., Todaka, K.,
Grace, A.A., Price, J.L., and Mathis, C.A. (2001). Amphetamine- and Nishimori, T. (1999). Regional differences in desensitization of
induced dopamine release in human ventral striatum correlates with c-Fos expression following repeated self-stimulation of the medial
euphoria. Biol. Psych. 49, 81–96. forebrain bundle in the rat. Neuroscience 90, 1013–1020.
Elliott, R., Friston, K.J., and Dolan, R.J. (2000). Dissociable neural

Nakamura, K., et al. (1998). Neuroanatomical correlates of the as-
responses in human reward systems. J. Neurosci. 20, 6159–6165.

sessment of facial attractiveness. NeuroReport 9, 753–757.
Etcoff, N. (1999). Survival of the Prettiest (New York: Doubleday).

O’Doherty, J., Kringelbach, M.L., Rolls, E.T., Hornack, J., and An-
Everitt, B.J., and Robbins, T.W. (1992). In The Amygdala: Neurobio- drews, C. (2001). Abstract reward and punishment representations
logical Aspects of Emotion, Memory, and Mental Dysfunction. J.P. in the human orbitofrontal cortex. Nat. Neurosci. 4, 95–102.
Aggleton, ed. (New York: Wiley-Liss), pp. 401–429.

Olds, J., and Milner, P.M. (1954). Positive reinforcement produced
Flores, C., Arvanitogiannis, A., and Shizgal, P. (1997). Fos-like immu- by electrical stimulation of septal area and other regions of rat brain.
noreactivity in forebrain regions following self- stimulation of the J. Comp. Physiol. Psychol. 47, 419–427.
lateral hypothalamus and the ventral tegmental area. Behav. Brain

Penton-Voak, I.S., Perrett, D.I., Castles, D.I., Kobayashi, T., Burt,
Res. 87, 239–251.

D.M., Murray, L.K., and Minamisawa, R. (1999). Menstrual cycle
Francis, S., Rolls, E.T., Bowtell, R., McGlone, F., O’Doherty, J., Brow- alters face preference. Nature 399, 741–742.
ning, A., Clare, S., and Smith, E. (1999). The representation of pleas-

Perrett, D.I., et al. (1998). Effects of sexual dimorphism on facialant touch in the brain and its relationship with taste and olfactory
attractiveness. Nature 394, 884–887.areas. Neuroreport 10, 453–459.
Perrett, D.I., May, K.A., and Yoshikawa, S. (1994). Facial shape andFrieze, I.H., Olson, J.E., and Good, D.C. (1990). Perceived and actual
judgments of female attractiveness. Nature 368, 239–242.discrimination in the salaries of male and female managers. J. Appl.

Soc. Psychol. 20, 46–67. Perrett, D.I., Burt, M.D., Penton-Voak, I.S., Lee, K.J., Rowland, D.A.,



Beauty and Reward
551

et al. (1999). Symmetry and human facial attractiveness. Evol. Hu-
man Behav. 20, 295–307.

Phillips, M.L., Williams, L., Senior, C., Bullmore, E.T., Brammer, M.J.,
Andrew, C., Williams, S.C.R., and David, A.S. (1999). A differential
neural response to threatening and non-threatening negative facial
expressions in paranoid and non-paranoid schizophrenics. Psych.
Res. Neuroimag. 92, 11–31.

Robledo, P., and Koob, G.F. (1993). Two discrete nucleus accum-
bens projection areas differentially mediate cocaine self-administra-
tion in the rat. Behav. Brain Res. 55, 159–166.

Rogers, R.D., et al. (1999). Choosing between small, likely rewards
and large, unlikely rewards activates inferior and orbital prefrontal
cortex. J. Neurosci. 20, 9029–9038.

Rolls, E.T. (1999). The Brain and Emotion (Oxford: University of Ox-
ford Press).

Ruskin, J. (1997). Lectures on Art. Reprint edition (Allsworth Press).

Schoenbaum, G., Chiba, A.A., and Gallagher, M. (1999). Neural en-
coding in orbitofrontal cortex and basolateral amygdala during ol-
factory discrimination learning. J. Neurosci. 19, 1876–1884.

Schultz, W., Dayan, P., and Montague, P.R. (1997). A neural sub-
strate of prediction and reward. Science 275, 1593–1599.

Schultz, W., and Dickinson, A. (2000). Neuronal coding of prediction
errors. Annu. Rev. Neurosci. 23, 473–500.

Shizgal, P. (1997). Neural basis of utility estimation. Curr. Opin. Neu-
robiol. 7, 198–208.

Shizgal, P. (1999). In Well Being: The Foundations of Hedonic Psy-
chology. D. Kahneman, E. Diener, and N. Schwarz, eds. (New York:
Russell Sage Foundation), pp. 502–526.

Slater, A., Von der Schulenburg, C., Brown, E., Badenoch, M., Butter-
worth, G., Parsons, S., and Samuels, C. (1998). Newborn infants
prefer attractive faces. Infant Behav. Devel. 21, 345–354.

Small, D.M., Zatorre, R.J., Dagher, A., Evans, A.C., Jones-Gotman,
M. (2001). Changes in brain activity related to eating chocolate: from
pleasure to aversion. Brain 124, 1720–1733.

Stein, E.A., et al. (1998). Nicotine-induced limbic cortical activation
in the human brain: a functional MRI study. Am. J. Psychiatry 155,
1009–1015.

Symons, D. (1995). Beauty is in the adaptations of the beholder: the
evolutionary psychology of human female sexual attractiveness. In
Sexual Nature, Sexual Culture. P.R. Abramson and S.D. Pinkerton,
eds. (Chicago: University of Chicago Press).

Talairach, J., and Tournoux, P. (1988). Co-planar stereotaxic atlas
of the human brain. (New York: Thieme Medical Publishers).

Thomas, K.M., Drevets, W.C., Whalen, P.J., Eccard, C.H., Dahl, R.E.,
Ryan, N.D., and Casey, B.J. (2001). Amygdala response to facial
expressions in children and adults. Biol. Psychiatry 49, 309–316.

Thut, G., et al. (1997). Activation of the human brain by monetary
reward. Neuroreport 8, 1225–1228.

Wise, R., Spinder, J., DeWit, H., and Gerber, G. (1978). Neuroleptic-
induced “anhedonia” in rats: pimozide blocks the reward quality of
food. Science 201, 262–264.

Wojciulik, E., Kanwisher, N., and Driver, J. (1998). Covert visual
attention modulates face-specific activity in the human fusiform
gyrus: fMRI study. J. Neurophysiol. 79, 1574–1578.

Wyvell, C.L., and Berridge, K.C. (2000). Intra-accumbens amphet-
amine increases the conditioned incentive salience of sucrose re-
ward: enhancement of reward “wanting” without enhanced “liking”
or response reinforcement. J. Neurosci. 20, 8122–8130.

Zald, D.H., Lee, J.T., Fluegel, K.W., and Pardo, J.V. (1998). Aversive
gustatory stimulation activates limbic circuits in humans. Brain 121,
1143–1154.