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NeuroImage 34 (2007) 1708 1722
Developmental differences in the neural bases of the face

inversion effect show progressive tuning of face-selective
regions to the upright orientation
A.M. Passarotti, a, J. Smith, a M. DeLano, b and J. Huang b
a
Department of Psychology, Cognitive Science and Neuroscience Program, Michigan State University, Psychology Bld., East Lansing, MI 48824, USA
Department of Radiology, Michigan State University, East Lansing, MI 48824, USA
Received 12 October 2005; revised 5 July 2006; accepted 6 July 2006

Available online 22 December 2006
Face inversion hinders face processing in adults, while not affecting

children in the same way. This fMRI study examines the neural
underpinnings of the behavioral face inversion effect (FIE) from
childhood to adulthood, and how face-selective regions in the brain
may change with development. Adults, children, and teens performed
a facial expression decision on upright and inverted face stimuli. In the
right hemisphere (RH) all age groups showed similar profiles of neural
activation for upright faces, but important developmental differences
occured for inverted faces. For inverted faces, adults, and to a lesser
degree teens, exhibited decreased levels of activity in the face-selective,
right lateral fusiform gyrus (LFG). However, children exhibited
greater activation for inverted than for upright faces in the same
region. We found similar, but less robust, developmental trends in the
right superior temporal sulcus (STS) and medial fusiform gyrus
(MFG). Furthermore, the present study identifies the right LFG as the
primary neural correlate of the behavioral FIE, and therefore of face
processing expertise, by showing a significant correlation between the
behavioral FIE and the neural FIE only in this region. Finally, the
present findings shed some light on at least one of the possible
mechanisms underlying the development of face processing expertise,
by suggesting a progressive tuning of face-selective regions in the right
hemisphere to the upright orientation, that extends well into
adolescence.
2006 Elsevier Inc. All rights reserved.
The ability to recognize and discriminate between different

faces is one of the most important human social skills. Behavioral
and neurophysiological research suggests early brain specialization
for face processing (Tzourio-Mazoyer et al., 2002) and newborn
preference for upright faces compared to non-face patterns (De
Haan et al., 2002; Morton and Johnson, 1991) or inverted face-like
stimuli (Valenza et al., 1996). Nonetheless, there is also evidence
for steady neural (Passarotti et al., 2003; Aylward et al., 2005;
Corresponding author. Fax: +574 631 8883.
E-mail address: apassaro@nd.edu (A.M. Passarotti).
Available online on ScienceDirect (www.sciencedirect.com).
1053-8119/$ - see front matter 2006 Elsevier Inc. All rights reserved.
doi:10.1016/j.neuroimage.2006.07.045
Gathers et al., 2004) and behavioral (Carey, 1992; Diamond and

Carey, 1977; Mondloch et al., 2003; Taylor et al., 2004)
development of face processing expertise through the teen years.
While adults are experts at processing upright faces, their
performance worsens when faces are inverted. This phenomenon is
called the face inversion effect (FIE) (Yin, 1969; Valentine,
1988; Moscovitch et al., 1997), and is much more pronounced for
faces than objects (Yovel and Kanwisher, 2004). A widely accepted
explanation for the FIE is that adult expertise relies mostly on
configural processing (i.e., processing of the relationship between
facial features, rather than processing of single facial features) and
that configural properties are extracted less efficiently when faces
are upside down (Carey, 1992; Diamond and Carey, 1977; Freire et
al., 2000; Mondloch et al., 2003; Farah et al., 1995). In fact,
experimental evidence suggests that configural information is more
salient than featural information when processing faces. Studies
using the composite-face effect paradigm suggest that recognizing that the top and bottom portions of a face in a composite
actually belong to different faces is harder when the two parts are
fused than when they are spatially separated (Young et al., 1987),
probably because we are biased to integrate face parts into a
meaningful facial configuration. Also, only for faces but not for
other objects, it is easier to recognize single face features when
they are within a whole face, than when the features are isolated
(Tanaka and Farah, 1993). Furthermore, people are still fairly
accurate at identifying blurred faces even when the internal
features are not very visible, whereas the opposite is not true.
These findings suggest that configural information is more salient
than featural information when we try to identify faces (Sergent,
1984; Hayes, 1988).
With regard to hemispheric specialization for face processing
recent neuroimaging evidence suggests that the right hemisphere
(RH) is specialized for configural processing (Rossion et al., 2000).
Supporting this view, the RH superiority in performance for faces
decreases or disappears with face inversion (Hillger and Koenig,
1991). In addition, a MEG study (Watanabe et al., 2003) suggests a
RH preference for upright faces since it found that latencies in the
A.M. Passarotti et al. / NeuroImage 34 (2007) 17081722
M170 (a face-selective component that possibly originates in the

fusiform gyrus) are shorter in the RH for upright faces than for
inverted faces. On the other hand, some evidence suggests that
both configural and featural processing contribute to expert face
processing and are affected by face inversion. Recent findings with
normal subjects (Riesenhuber et al., 2004; Yovel and Kanwisher,
2004) and subjects with developmental prosopagnosia (Yovel and
Duchaine, 2006) suggest that face-selective mechanisms process
faces holistically, by extracting both configural and featural
information as a whole, and that holistic processing is disrupted by
inversion.
Either way, since the FIE is considered an indicator of face
processing expertise, understanding whether and how the behavioral FIE emerges with age would provide a crucial insight on the
development of face processing expertise. The literature examining
the behavioral FIE in childhood does not provide clear-cut results,
probably because of the use of different paradigms and measures of
performance (Brace et al., 2001). Some studies suggest a
qualitative change in FIE with age, while others suggest only
quantitative changes or no change at all with age. Carey (Carey,
1992; Carey and Diamond, 1977) reported a significant reversed
behavioral FIE (i.e., better performance for inverted than for
upright faces) in children younger than age 10, while Brace et al.
(2001) reported this result only in children younger than age 5.
These studies would suggest a qualitative switch from featural
processing (which is less sensitive to orientation) to configural
processing (which is sensitive to orientation) with age. But other
studies found inversion effects in younger children (Baenninger,
1994; Chun and Thomson, 1995; Flin, 1985) and suggest that
during development either the size of the FIE increases (Mondloch
et al., 2002) or remains stable (Young and Bion, 1980; Pascalis et
al., 2001). The neural underpinnings of the behavioral FIE have
been explored almost exclusively in adults. Most fMRI studies on
inverted face processing have found a small but significant
reduction in activation in the face fusiform area (FFA) (Yovel
and Kanwisher, 2004; Gauthier et al., 1999; Haxby et al., 1999;
Kanwisher et al., 1998), sometimes accompanied by increased
activation in inferior temporo-occipital regions that usually process
features (Haxby et al., 1999; Kanwisher et al., 1998; Leube et al.,
2003). Neuropsychological evidence also suggests that for inverted
faces the FFA may need additional input from object-processing
regions (Haxby et al., 1999; Leube et al., 2003; Rossion et al.,
2003). In fact, a patient with object agnosia (i.e., with object
processing deficits) could process upright faces but showed
impaired processing of objects and inverted faces (Moscovitch et
al., 1997), whereas patients with prosopagnosia (i.e., with deficits
in discriminating between faces) usually exhibit the opposite
pattern (Farah et al., 1995).
Recent neurophysiological findings suggest that the neural
correlates of the behavioral FIE undergo protracted developmental
changes. The N170 is a face-specific, negative event-related
potential (ERP) component, which may have its anatomical
sources in the inferior occipito-temporal areas (Taylor et al.,
2004; Bentin et al., 1996). In adults face inversion causes larger
N170 latencies and greater amplitudes in the RH (Taylor et al.,
2004). The N170 occurs as early as age 4, and even younger
children show some evidence of FIE in their N170 profiles (Taylor
et al., 1999). Nevertheless, different face processing strategies
exhibit a different developmental timeline. Taylor et al. (2001)
found that for featural face processing the N170 reaches adult-like
profiles by age 11, while configural processing develops more
1709
slowly and improves through adolescence (Taylor et al., 2001,

2004). Moreover, different from the findings for featural processing, findings for inverted faces showed that the typical adult N170
latencies (with greater right hemisphere amplitudes) emerged only
in mid-adolescence, suggesting that children did not just use
feature processing with inverted faces, but probably used a
combination of both feature and configural processing (Taylor et
al., 2001, 2004). The view of gradual, quantitative changes in the
neural substrates of face processing (Taylor et al., 2001, 2004) is
confirmed by developmental fMRI studies on upright face
processing which found more bilateral activation and widespread
right fusiform activation in children than in adults (Passarotti et al.,
2003), with differences in activation until late adolescence
(Passarotti et al., 2001), as well as a progressive increase in right
fusiform selectivity for faces compared to objects (Gathers et al.,
2004; Aylward et al., 2005).
Whereas these studies did not examine the neural underpinnings of the behavioral FIE, the present fMRI study is the first,
to our knowledge, to establish the neural segregation and
organization of the neural correlates of the behavioral FIE, from
childhood to adulthood. We wished to address the crucial question
of whether the effects of inversion on the functioning of faceselective regions may differ with development, and if so, in what
fashion. By using fMRI during processing of upright and inverted
faces we wanted to clearly localize the anatomical underpinnings
of the FIE in children and adults. Furthermore, we tested children
in the 811 age range and adolescents to address the existing
debate on whether there is an abrupt, qualitative change in face
processing skills around age 10 (Carey, 1992; Carey and Diamond,
1977) or whether development of face processing expertise is more
gradual and quantitative in nature (Baenninger, 1994; Chun and
Thomson, 1995; Taylor et al., 2004). With regard to the adult
group, for inverted face processing we predicted a decrease in
performance accompanied by a decrease in activation of faceselective regions in the right hemisphere, for inverted compared to
upright faces (Yovel and Kanwisher, 2004; Leube et al., 2003). We
expected teens to exhibit similar but somewhat weaker profiles of
activation in face-selective regions as the adults, since expert
configural processing is not reached until late adolescence (Taylor
et al., 2004). As for the younger children, we predicted that their
functional activation in face-selective regions may not differ
significantly for upright and inverted faces, because children may
use face-specific strategies less efficiently than adults, or they may
use more general processing strategies that are not as sensitive to
orientation (Baenninger, 1994; Taylor et al., 2001).
To test our predictions we collected behavioral and fMRI
data from adults, teens and children during a face-emotion processing task with inverted and upright face presentations. Face
emotion processing, like face identity processing, relies mostly
on configural or holistic strategies and shows comparable face
inversion effects (Calder et al., 2000; McKelvie, 1995). We
used angry and happy expressions because the ability to
recognize them is fully developed by age 6 (Markham and
Adams, 1992).
Methods
Participants
Thirteen adults (aged 2030 years), ten teens (aged 13
17 years), and fourteen children (aged 811 years) were recruited
1710
from the local community and Michigan State University. All

participants were right-handed as assessed by a handedness
questionnaire (Oldfield, 1971) and had normal or corrected to
normal vision. They had no known-neurological or cognitive
impairment. Adult participants were either volunteering or were
given class credit. Children and teens received a monetary
compensation ($10) for their 2-h participation. Before testing,
adult participants and child parents/guardians signed an informed
consent, while children and teens signed an assent form. A
medical clearance questionnaire was administered to each
participant to ensure scanning safety. All our forms and research
protocols were approved by the Michigan State University
Committee for Research with Human Subjects. fMRI data from
2 adults and 1 child were discarded because of technical
problems, whereas data from 1 adult, 1 teenager, and 2 children
were excluded because of low performance levels or excessive
motion. The final fMRI dataset included 10 adults (5 F, 5 M;
mean 25.3 4 years), 9 teens (7 F, 2 M; mean 14.9 1.6 years),
and 11 children (5 F, 6 M; mean 10 1.6 years). Due to technical
difficulties with button press recordings, we did not collect
behavioral data from one male child. Therefore our behavioral
dataset included 10 children.
emotions (i.e., happy or angry). Each 5-s trial began with a

1000 ms fixation cross, followed by central presentation of a face
picture for 2000 ms and a response time of 2000 ms. We decided
to give participants a whole 2 s to process stimuli, to ensure that
even the younger children would perform well. In addition,
depending on the run the face stimuli were presented either upright
or upside-down (see Fig. 1a for an example of an inverted face
trial). On each trial of the control task participants gave a simple
motor response (i.e., a key press) when the face stimulus (i.e.,
neutral face) appeared. These control trials were blocked and no
cognitive decision was required. Order of task conditions
(inverted, upright faces) and target emotion (happy, angry) was
counterbalanced across participants.
Brain imaging procedures

Participants learned the experimental tasks during a training
session preceding scanning. In addition, children and teens
listened to audio recordings of scanner noises to become more
familiar and comfortable with them. Then, the scanning session
started and lasted approximately 40 min. We adopted a standard
block design to maximize signal-to-noise ratio for short imaging
sessions. We alternated six 40-s blocks of each task and control in
4 min and 8 s. Eight trials (each lasting 5 s) were presented for
each block, for a total of 48 trials in each run. Visual stimuli were
projected directly on a small MR-compatible LCD screen (view
angle: 12 vertically and 16 horizontally) positioned on the head
coil inside the MRI scanner. Our visual stimuli were presented
through the IFIS-SA System (Psychology Software Tools Inc.,
Milwaukee, WI). Button presses were performed with a special
mouse, part of the IFIS-SA system, and were recorded at millisecond accuracy.
BOLD images were acquired on a 3 T magnet (G.E. Medical
Systems, Pittsburgh, PA) using a standard GE quadrature head
coil. After an initial coronal localizer and manual shimming, T2*weighted single-shot gradient-echo planar images (EPI) were
acquired with TR = 2 s, TE = 40 s, FOV = 220 mm, flip
angle = 80, 25 contiguous 5.5 mm axial slices, 120 images,
64 64 matrix, in-plane resolution, 3.4 3.4 5.5 mm. For each
participant, these images were registered to high-resolution T1weighted structural images (116 sagittal fast SPGR images, FOV
256, 1.5 mm slices). We used padding materials to stabilize
participants heads, and earplugs to attenuate the scanner noise.
We showed to children and teens cartoon videos during the initial
localizer protocols and during anatomical acquisitions, to keep
them relaxed and still.
Behavioral task
During scanning, on each trial participants saw a color picture
of a female face presented centrally on a black background, and,
depending on the run, responded selectively to one of two face
Fig. 1. Example trial and behavioral results. (a) An example of the visual
display and trial timeline. Here we present an inverted face trial. Our face
pictures were taken from the NimStim Face Stimulus Set. (b) Mean
proportion correct for upright and inverted face trials in children (N = 10),
teens (N = 9), and adults (N = 10). (c) Mean RT (ms) for performance on
upright and inverted face trials in children, teens, and adults. Asterisk
indicates significance at p < .05. Error bars in panels b, c represent the
SEM.
fMRI image processing

Anatomical and functional images were processed in AFNI
(Cox, 1996). To control for initial magnetic field inhomogeneities,
1711
the first four time points of all functional runs were discarded a
priori. In-plane (slice-wise or 2D) and volumetric (3D) motion
correction was performed on the dataset using the AFNI programs
2dImReg and 3dvolreg, respectively, using the third acquisition as
Table 1
Significant clusters of activation, their laterality, and their Talairach coordinates (Talairach and Tourneaux, 1988) for the upright and inverted face conditions, in
children (N = 11), teens (N = 9), and adults (N = 10)
Upright faces
Inverted faces
BA
Hemisphere
Region
BA
Hemisphere
Region
Adults (N = 10)
34
39
58
63
47
63
57
33
58
59
64
9
11
45
40
55
44
42
30
37
84
66
60
28
24
24
18
19
12
12
17
3
0
7
2
6
9
35
33
20/37
20/37
20/21
20/21
9
20/22
20/22
18/19/37
18/19/37
22
22
20
20
L
R
L
R
L
L
R
L
R
L
R
L
R
LFG
LFG
IT gyrus
IT gyrus
MF gyrus
MT gyrus
MT gyrus
IOG
IOG
STS
STS
MFG
MFG
Teens (N = 9)
40
38
21
14
45
52
56
58
58
27
42
42
64
45
41
36
31
43
48
32
16
32
84
60
43
9
15
13
30
33
40
7
15
20
13
7
6
4
11
37
37
20
20
40
20/22
20/21
20/21
20/22
18/19/37
18/19/37
22
22
L
R
L
R
R
R
L
R
L
L
R
L
R
LFG
LFG
MFG
MFG
IP lobule
MT gyrus
IT gyrus
IT gyrus
MT gyrus
IFG
IFG
STS
STS
45
36
7
15
18
52
22
64
56
45
45
20
57
42
48
41
42
54
55
96
14
42
16
9
49
48
81
67
47
51
9
14
3
4
5
45
62
15
20
2
2
5
3
1
3
37
37
20
20
18
9
7
20/21
20/21
20/22
20/22
18/19/37
18/19/37
22
22
L
R
L
R
R
R
R
L
R
L
R
L
R
L
R
LFG
LFG
MFG
MFG
Ling. gyrus
MF gyrus
SP lobule
IT gyrus
IT gyrus
MT gyrus
MT gyrus
IOG
IOG
STS
STS
44
35
9
11
56
48
32
55
4
10
55
40
59
58
63
57
39
58
57
56
19
45
40
21
14
52
56
59
67
19
46
54
48
44
36
7
15
27
35
6
30
52
56
47
49
29
40
51
47
49
40
24
24
16
10
2
9
72
87
54
20
49
29
30
37
86
60
39
42
38
47
38
36
31
53
33
49
46
92
73
46
51
44
42
54
55
23
48
49
68
43
39
8
25
81
72
50
49
20
21
35
33
13
28
38
18
41
43
13
20
13
14
3
0
7
2
8
9
28
20
21
30
33
13
15
1
2
6
8
2
4
11
12
3
4
5
8
9
58
13
13
35
14
4
4
1
5
37
37
20
20
47
21
20/22
20/22
7
7
22
22
20/21
20/21
20/22
20/22
18/19/37
18/19/37
22
22
24
37
37
20
20
20/21
20/21
20/22
20/22
18/19/37
18/19/37
22
22
37
37
20
20
47
9
23
7
20/21
20/21
20/22
20/22
18/19/37
18/19/37
22
22
L
R
L
R
R
L
L
L
R
L
R
L
L
R
L
R
L
R
L
R
R
L
R
R
L
L
R
L
R
L
R
L
R
L
R
L
R
L
L
L
L
L
R
L
R
L
R
L
R
LFG
LFG
MFG
MFG
IF gyrus
IT gyrus
MT gyrus
MT gyrus
Precuneus
Precuneus
ST gyrus
ST gyrus
IT gyrus
IT gyrus
MT gyrus
MT gyrus
IOG
IOG
STS
STS
Cing. gyrus
LFG
LFG
MFG
MFG
IT gyrus
IT gyrus
MT gyrus
MT gyrus
IOG
IOG
STS
STS
LFG
LFG
MFG
MFG
IF gyrus
MF gyrus
Post. Cing.
SP lobule
IT gyrus
IT gyrus
MT gyrus
MT gyrus
IOG
IOG
STS
STS
Children (N = 11)
The Talairach coordinates (in the x, y, z axes) for our axial images indicate the center of mass of each significant cluster of activity. X = right to left; Y = anterior to
posterior; Z = superior to inferior. Note that in our X coordinates the right (R) hemisphere has a positive sign and the left (L) hemisphere has a negative sign.
Abbreviations: lateral fusiform gyrus = LFG; medial fusiform gyrus = MFG; inferior temporal gyrus = IT gyrus; middle temporal gyrus = MT gyrus; inferior
occipital gyrus = IOG; superior temporal sulcus = STS; inferior parietal lobule = IP lobule; superior parietal lobule = SP lobule; inferior frontal gyrus = IFG; middle
frontal gyrus = MF gyrus; Ligual gyrus = Ling. gyrus; cingulate gyrus = Cing. gyrus; posterior cingulate = Post. Cing.
1712
the fiducial volume. The signal was then orthogonalized to the

obtained parameters of rigid body rotation and global drift was
removed on a voxel-wise basis over each functional run. For
volumetric motion correction, an iterated, weighted linear least
squares algorithm with Fourier interpolation (Cox and Jesmanowicz, 1999) was utilized to register all dataset volumes to the third
acquired T2*-weighted functional volume and time shifted to the
fiducial volume in order to account for slice acquisition offset. We
considered the algorithm iterations convergent when maximum
movement was less than .02 voxels and maximum rotation was less
than .03. There were no time points at which these constraints
were exceeded; angular and linear drift along and around the x, y,
and z axes of the dataset were quantified as vector components and
used as regressors in further analyses.
High- and low-bandpass filters were applied to the data (using
the AFNI program 3dFourier) at .20 Hz and .60 Hz, respectively,
in order to suppress predictable pulsatile physiologic noise such as
cardiac and respiratory rhythms. Stimulus-related activation was
detected by examining the time-course correlation of each voxels
signal intensity with a family of idealized hemodynamic response
waveforms (Bandettini et al., 1993). High- and low-bandpass
filters were applied to the data (using the AFNI program
3dFourier) at .20 Hz and .60 Hz, respectively, in order to
suppress predictable pulsatile physiologic noise such as cardiac
and respiratory rhythms. Stimulus-related activation was detected
by examining the time-course correlation of each voxels signal
intensity with a family of idealized hemodynamic response
waveforms (Bandettini et al., 1993). Voxels correlating at a
coefficient threshold of .23 (p < .001, uncorrected) were retained.
For each individual, statistical maps were then overlaid on the coregistered high-resolution normalized anatomical dataset (Talairach and Tourneaux, 1988). Child brain normalization is an
accepted protocol in developmental fMRI studies, since total
brain size does not increase significantly between ages 9 and 18
(Klingberg et al., 2002). Therefore data from 8 to 9 year olds and
adults can be effectively transformed into the same stereotactic
space (Schlagger et al., 2002; Kang et al., 2003) with minimal agerelated difference. The average motion (roll, pitch, yaw) for
children was .049, for adults .020, and for teens .017. The
average motion for children was .055 mm, for adults .017 mm, and
for teens .022 mm. Students t-tests revealed that the child group
differed significantly (p < .05) from the other two groups.
However, tolerance for motion correction in AFNI was
.07 mm .03 between slices and only subjects in any age cohort
who did not exceeded these tolerance parameters were kept in our
analyses.
For each subject we obtained mean volume and % signal
separately for upright and inverted face emotion trials using a
cross-correlation analysis (r > .23) in which we identified contiguous voxels that correlated to a modified waveform with threshold
at p < .01. We followed the same procedure for neutral trials. Our
analyses focus on upright and inverted face emotion trials, since
these are the trials that required a cognitive decision and therefore
ensured accurate processing. Then, Cluster analyses were carried
out in AFNI. Minimum alpha (confidence) levels were computed
using Monte Carlo noise simulations in the AFNI program
AlphaSim (Ward, 1997). In this step, adjacent voxels with p
values falling below .001 had to form connected regions of at least
195 mm3 for significant activation. In addition to individual cluster
analyses, an additional cluster analysis was performed on each
groups statistical maps.
ROI definition
We examined three core regions in extrastriate cortex that have
been defined as part of a distributed face processing system (Haxby
et al., 2000). Although the functional role of these regions and how
they interact with each other is still not completely understood,
several studies suggest that the lateral fusiform gyrus (LFG) is a
face-selective region that processes invariant aspects of faces, such
as identity (Haxby et al., 1999; Haxby et al., 2002; Kanwisher et
al., 1997), whereas the superior temporal sulcus (STS) processes
changeable aspects of faces, such as gaze orientation or face
expressions (Hoffman and Haxby, 2000; Puce et al., 1998; Rolls,
1984) and may be one of the sources of the N170 (Puce et al.,
1998). The inferior occipital gyrus (IOG) processes single face
features (Haxby et al., 1999) and may either feed featural
information onto the STS and LFG (Hoffman and Haxby, 2000;
Haxby et al., 1999), or receive feed-back signals from the LFG to
guide fine-grained feature analyses (Rossion et al., 2003). In
addition, we examined the medial fusiform gyrus region (MFG),
which is involved in object processing in adults (Ishai et al., 1999),
but has been found to contribute considerably to face processing in
children (Passarotti et al., 2003). All our participants showed
bilateral clusters of activation in these regions (see Table 1).
Our ROIs were defined anatomically, using anterior and
posterior boundaries as defined in previous studies (Gauthier et
al., 1999). Since there is evidence of minimal age-related
differences in spatial transformation after age 8 (e.g., Kang et al.,
2003; Schlagger et al., 2002) we did not trace the ROIs for each
subject individually, rather we defined each ROI anatomically on a
template (Talairach and Tourneaux, 1988), and applied it to the
normalized brains within each group, as several developmental
fMRI studies did (e.g., Nelson et al., 2003; Passarotti et al., 2003).
For the LFG ROI we first isolated in each subject a significant
continuous cluster of activation with center of mass coordinates
that were similar to the ones given by Grill-Spector and Kanwisher
(2005) and Haxby et al. (2002). We then placed an eight-voxel
bounding box around the individuals cluster center of mass, which
corresponded to the spatial extent of the FFA given in Rossion et
al. (2003) and Kanwisher et al. (1997), and averaged the masked
individual clusters across subjects within each of the age groups.
For each group we had therefore an averaged cluster, which we
found to overlap with the anatomically defined lateral fusiform
region (Haxby et al., 2002; Grill-Spector and Kanwisher, 2005;
Rossion et al., 2003). Therefore we adopted the anatomically
defined LFG as our ROI. The IOG, STS and medial fusiform gyrus
(MFG) were also derived from functional clusters and ultimately
anatomically defined (Talairach and Tourneaux, 1988). Separate
ROIs were obtained for the left and the right hemisphere.
Results
Behavioral performance and behavioral FIE
Separate ANOVAs were carried out for Reaction time (RT) and
Accuracy data. Incorrect button presses were excluded from the RT
analyses but were included in the Accuracy analyses. Face
orientation (upright, inverted) was the within-subjects factor
whereas Age (children, teens, and adults) was the between-subjects
factor. When an Age effect was found separate ANOVAs by Age
were also carried out to further examine performance within each
age group.
Accuracy
The Accuracy results are summarized in Fig. 1b. Accuracy
levels were above 90% in each age group. The teens accuracy did
not differ from that of children and adults (F values < 1), but adults
had a significantly higher accuracy than children [F(1,18) = 5.34;
p = .03]. In an ANOVA with Age (children, teens, adults) and
Orientation (upright, inverted) as factors a significant Face
orientation effect [F(1,26) = 5.56; p = .03] demonstrated that overall
Accuracy was significantly higher for upright (.97) than for
inverted faces (.94). Nevertheless, the interaction of Age Orientation was not significant (F < 1), suggesting that there were no
robust age differences in FIE for the accuracy data. Separate
ANOVAs by Age confirmed that accuracy for upright and inverted
faces did not differ significantly in either children [F(1,9) = 1.95.
p = .19], teens [F(1,8) = 2.61 p = .14], or adults (F < 1).
Since participants had quite a long time to process stimuli and
to respond (i.e., 2 s), it is possible that some ceiling effects
occurred and weakened Age Orientation effects in the accuracy
data. Therefore these data need to be considered with caution. We
1713
turn now our attention to the RT data, which have been found to be
more useful in limiting ceiling effects (Ellis, 1990).
Reaction time
The RT results are summarized in Fig. 1c. As expected, a
significant main effect of Age indicated that RT improved
steadily with age for both upright and inverted face presentations
[F(2,26) = 19.28; p = .00007]. Planned comparisons showed that
the three groups differed significantly from each other (p < .001).
An inspection of the individual data revealed that whereas in 80%
of the adults RT was elongated for inverted faces, in children and
teens RT was more variable and did not show a consistent cost
for face inversion (there was a RT cost for inversion only in
about 40% of children and 44% of teens). The majority of
children (60%) exhibited a trend for faster RT with inverted than
with upright faces. In spite of these trends, the interaction of
Age Orientation was not significant (F < 1).
Separate ANOVAs by Age confirmed that the adult RT was
significantly higher for inverted faces (858 ms) than for upright
Fig. 2. fMRI maps of significant (p < .01, corrected) group cluster activation in children (N = 11), teens (N = 9), and adults (N = 10) for the upright face task (left
side) and the inverted face task (right side). See also Table 1. The particular axial slice represented in this figure shows the right and left Fusiform Gyrus.
Significant functional clusters of activation were overlaid on a T1 anatomical image from one participant. The Z coordinate (Z = 11) indicates the distance in
mm of the axial slices (i.e., according to a superior to inferior axis) from the intercommissural plane (anterior commissure posterior commissure). The color bar
on the top right side represents the scale of percent signal change increases in the experimental tasks compared to the control task. Note that brain images follow
the radiological convention [i.e., the left side of the brain picture represents the right hemisphere (R), the right side of the brain picture represents the left
hemisphere (L)].
1714
faces (767 ms) [F(1,9) = 7.48, p = .02]. The size of the adult
behavioral FIE (about 12%) is comparable to that found in
other studies (Aguirre et al., 1999; Diamond and Carey, 1986;
Itier and Taylor, 2004; Valentine, 1988). Conversely, in children
[F(1,9) = .11, p = .74] and teens [F(1,8) = .12, p = .74] RT did not
differ significantly for upright and inverted faces.
ROI analyses and neural FIE
As expected, significant clusters of activity were found in the
face-selective region LFG (BA 37), in STS (BA 22), in IOG (BA
19), and MFG (BA 20) (see Fig. 2, and Table 1). We report below
percent signal change analyses separately for each ROI. An initial
ANOVA was run with Age group (children, teens, adults) as a
between-subjects factor and Hemisphere (left, right) and Orientation (inverse, upright) as within-subjects factors. When the factor
of Hemisphere interacted significantly with other factors we carried
out separate analyses by hemisphere.
Lateral fusiform gyrus (LFG) ROI
In an initial ANOVA the three-way interaction of Age Hemisphere Orientation was significant [F(2,27) = 5.22, p = .01].
Planned comparisons on this interaction indicated that only
children [F(1,10) = 8.83, p = .006] but not adults [F(1,9) = 1.92,
p = .18] and teens (F < 1) demonstrated significant hemispheric
differences in profiles of activation for upright and inverted faces.
Moreover, it was only in the right LFG that the child FIE profile
differed significantly from that of teens [F(1,27) = 10.77, p = .003]
and adults [F(1,27) = 15.71, p = .0005], who did not differ from
each other (F < 1). Given these findings, we proceeded to examine
LFG data separately for each hemisphere.
Importantly for our hypotheses, for the right LFG, we found
a significant interaction of Age Face Orientation [F(2,27) = 9.19,
p < .0009]. Planned comparisons revealed that only for inverted
faces did children show significantly higher percent signal change
than adults [F(1,27) = 13.54, p < .001] and teens [F(1,27) = 9.59,
p < .005], who in turn did not differ from each other (F < 1). No
significant age differences in levels of activation were found for
upright faces (F < 1). With regard to the neural FIE (i.e., the
difference between % signal change for upright faces and % signal
change for inverted faces), in accord with the RT data adults
exhibited the expected FIE, with a higher percent signal change for
upright (.28%) than for inverted (.09%) faces [F(1,27) = 4.81,
p < .04]. This adult pattern was similar to the one found in other
studies (Yovel and Kanwisher, 2004, 2005) and is usually attributed
to hindrance of face-specific processes, defined either as configural
(Haxby et al., 1999; Leube et al., 2003) or holistic (Yovel and
Kanwisher, 2004; Riesenhuber et al., 2004) processes. Like in
adults, also in teens activation was higher for upright (.26%) than
for inverted (.15%) faces, although not significantly [F(1,8) = 4.81,
p < .20]. On the contrary, in children there was a reversed neural
FIE, in that children actually showed a higher percent signal
(.49%) for processing of inverted faces than of upright faces
(.22%) [F(1,10) = 11.86, p < .002] (Fig. 3a). The child neural FIE
differed significantly from that of adults [F(1,27) = 15.71,
p = .0005] and teens [F(1,27) = 10.77, p = .003], who did not differ
from each other (F < 1).
With regard to the left LFG, a significant Age effect [F(2,27)=4.02,
p < .03] revealed that children exhibited significantly more
activation than teens (p<.03), and marginally more activation
than adults (p<.06) (Fig. 3b). The interaction of AgeOrienta-
tion was not significant (F<1). Separate ANOVAs by Age showed

that also in the left LFG adults exhibited a higher percent signal for
upright (.17%) than for inverted (.07%) faces [F(1,9)=7.89, p=.02],
although the size of the FIE in the LH was about half of that in the
RH [F(1,9)=6.06, p=.04]. Children and teens exhibited very similar
activation levels for the two conditions (F values<1). Finally, similar
to the right LFG results, separate ANOVAs by Orientation showed
evidence of age differences in activation only for inverted [F(2,27)=5.07,
p < . 013] but not for upright faces [F(1,27) = 1.43, = .26]. Planned
comparisons on the inverted face data revealed that children
activated significantly more than adults [F(1,27) = 9.01, p = .006]
and teens [F(1,27) = 5.47, p = .03], who did not differ from each
other (F < 1).
Our results suggest that developmental differences in profiles of
neural FIE for our face emotion processing task1 occurred
specifically in the right LFG, but not in left LFG. As an additional
way of representing these findings, we calculated for each
participant a score of neural FIE (i.e., % signal for upright faces
% signal for inverted faces). We did this separately for RH and LH.
Our Results are reported in Fig. 3c. Similar to findings in our ROI
analyses, an ANOVA on the right LFG scores revealed a
significant Age effect [F(2,27) = 7.78, p = .02] such that only
children revealed a negative neural FIE score (.25) (i.e., mean
group activation was higher for inverted faces), whereas teens (.12)
and adults (.19) revealed a positive neural FIE score (i.e., higher
activation for upright faces). Planned comparisons revealed that the
childrens pattern differed significantly from that of adults [F(1,27)
= 13.14, p = .001] and teens [F(1,27) = 8.98, p = .006], who in turn did
not differ (F < 1). On the contrary, for the left LFG there were no age
differences (F < 1).
Relation between behavioral and neural FIE in right LFG
As expected our adults, and to a lesser degree teens, showed
greater right LFG activation for upright faces, which suggests a
preference, or sharper tuning, for upright faces. On the contrary,
children exhibited a higher activation for inverted faces, which
according to the same rationale would mean a preference for the
inverted orientation. But one may also argue that the child data
patterns may result from a general increase in neural and cognitive
effort in order to extract relevant facial information with an
unusual orientation. If this were true, the neural effort resulting
from inverted face processing would be most likely associated with
higher RT for inverted faces. In order to test the preference or
effort hypotheses for children, we examined the relation between
the behavioral FIE (i.e., RT) and the neural FIE for the right LFG
in each individual. We were able to identify four different neural/
behavioral FIE profiles, and to ascertain that the majority of
To check that our developmental FIE results for the right LFG are not
caused by attentional effects (OCraven et al., 1999) due to the emotional
content of our stimuli, we compared the % signal change for neutral face
trials (which have no emotional content) to that of face emotion trials
(which have an emotional content) in an ANOVA with the factors of Age,
Type of trials, Hemisphere and Orientation. The interaction of Type of
trial Hemisphere Orientation, which would identify FIE patterns for the
two types of trials, was not significant [F(1,27) = .24, p = .63]. Moreover,
the three-way interaction of Age Type of trial Orientation was also not
significant [F(2,27) = 1.76, p = .19], suggesting that across all ages the FIE
patterns in LFG did not differ significantly for neutral faces and emotion
faces. No other significant interactions of Type of trial with the other factors
were found.
children did not exhibit an effort profile, rather a preference profile

for inverted faces. Fig. 4 shows the age group distribution for the
four FIE profiles. For our purposes we will focus especially on the
two preference profiles which had overall the highest occurrence
(they were present in 2/3 of subjects) and showed a clear age
dissociation. In fact, the adult group was characterized by the
typical FIE profile, with a preference for the upright orientation.
About 60% of the adults exhibited this pattern, while 33% of the
teens and only 10% of children did so. Conversely, the child group
was mainly characterized by a reversed FIE profile, showing a
preference for the inverted face orientation. In fact, 60% of the
1715
Fig. 4. Relation between Behavioral and Neural FIE in the right LFG: age
differences across four different profiles. The Upright face preference
profile corresponds to the typical FIE profile in our data (i.e., faster RT for
upright faces, higher activation for upright faces). The Inverted face
preference profile corresponds to the reversed FIE profile (i.e., faster RT
for inverted faces, higher activation for inverted faces). The Upright face
effort profile presents higher RT and higher activation for upright faces. The
Inverted face effort profile presents higher RT and higher activation for
inverted faces. The age groups differed significantly in their frequency
distributions across the four categories (see results section). The proportions
are based on 10 children, 9 teens and 10 adults.
children showed this profile, while only 22% of teens, and no

adults did so. In addition, there were two minor FIE profiles that
did not show a preference for upright or inverted faces, rather some
effects of neural and cognitive effort due to orientation. An Upright
face effort profile exhibited higher RT and higher activation for
upright faces, while an Inverted face effort profile exhibited higher
RT and higher activation for inverted faces. We found that only 1/3
of children, and a little less than 1/2 of the adults and teens fell in
these two categories. A Chi-square (2) test revealed that the age
groups differed significantly in their frequency distributions across
the four categories [2 (6, N = 29) = 14.44, p = .03]; more specifically,
the child and adult frequency distributions for the reversed and
typical FIE patterns differed significantly from each other [Yates
2 (1, N = 20) = 6.41, p = .01].
Superior temporal sulcus (STS) ROI
In a first ANOVA the interaction of Hemisphere Orientation
was significant [F(1,27) = 5.65, p = .02]. Planned comparisons
demonstrated that overall the left STS had a higher signal
change than the right STS for inverted face trials [F(1,27) = 6.79,
p = .01], but not for upright face trials (F < 1). The Age Hemisphere interaction showed a non-significant trend [F(1,27) = 2.78,
p = .08] such that children [F(1,27) = 3.67, p = .07] and teens
Fig. 3. ROI analyses results for the right and left Lateral fusiform Gyrus.
Mean percent signal change for upright and inverted face trials as obtained
from the functionally defined LFG ROI in children (N = 11), teens (N = 9),
and adults (N = 10). (a) Right LFG. Note that whereas in adults the percent
signal change is greater for upright than inverted faces [F(1,27) = 4.81,
p < .04] children exhibit significantly more activation for inverted than for
upright faces [F(1,10) = 11.86, p < .002]. Teens activate more for upright
presentations, but not significantly so (p < .20). (b) Left LFG. Only in adults
percent signal is significantly higher for upright than inverted faces
[F(1,9) = 7.89, p = .02], whereas children and teens do not show differences
for the two conditions (F values < 1). Asterisk indicates significance at
p < .05. Error bars in panels a, b represent the SEM. (c) Mean upright face
activation advantage in right and left LFG (Neural FIE). Positive scores
indicate higher selectivity for upright faces than for inverted faces, whereas
negative scores indicate the opposite. Note that for the right LFG there is a
significant Age effect [F(2,27) = 7.78, p = .02]. Children differed significantly from adults [F(1,27) = 13.14, p = .001] and teens [F(1,27) = 8.98,
p = .006], who in turn did not differ (F < 1). Asterisk indicates significance at
p < .05. Double asterisk indicates significance at p < .001.
1716
[F(1,27) = 4.39, p = .05] had higher activation in the left STS,

while adults had similar activation levels in the two hemispheres
(F < 1). Next, we analyzed right and left STS data separately in
each age group. In the right STS adults showed a significant
neural FIE, with higher percent signal for upright faces (.49%)
than for inverted faces (.44%) [F(1,9) = 49.41, p < .00006],
confirming previous findings of STS preference for the upright
orientation, which has been attributed to its involvement in
configural processing (Haxby et al., 1999; Leube et al., 2003).
Conversely, the right STS in children (F < 1) and teens (F < 1) did
not show significant orientation preferences (Fig. 5a). For the left
STS there were no significant results (F values < 1) (Fig. 5b). The
present findings indicate that similar to the right LFG, the right
STS increases its sensitivity to the upright face orientation with
age. The younger groups engage their left STS more than adults
do, which suggests that they may rely more on levels of analyses
that are not face-specific.
Finally, like the right LFG, the right STS also exhibited age
differences in the upright activation advantage [F(2,27) = 10.30,
p = .005], while the left STS did not (F < 1). For the right STS
planned comparisons revealed that adults (.05%) and teens (.006%)
exhibited a positive upright orientation advantage, but this pattern
was significant only in adults [F(2,27) = , p = .008]. Adults also
differed from children [F(2,27) = 20.47, p = .0001] who exhibited a
non-significant preference (F < 1) for the inverted orientation
( .24).
Inferior occipital gyrus (IOG) ROI
An initial ANOVA revealed a significant interaction of
Age Hemisphere [F(2,27) = 6.72, p = .004] and Hemisphere Orientation [F(1,27) = 5.84, p = .02]. Therefore we analyzed our data
separately by hemisphere. For the right IOG no significant effects
were found (Fig. 6a). For the left IOG a main effect of Age was
significant [F(2,27) = .004], in that children (.55) and teens (.53)
exhibited greater activation (p < .05) than adults (.45) for both
orientations. No interaction of Age Orientation was found (Fig.
6b). Separate ANOVAs by Age demonstrated a significant interaction of Hemisphere Orientation both in children [F(1,10) = 5.6,
p = .04] and in teens [F(1,8) = 8.03, p = .02]. Planned comparisons on the child data showed no orientation effects in the left
[F(1,10) = 1.13, p = .31] or right IOG (F values < 1). Planned
comparisons on the teen data revealed that the left IOG
activated more for upright faces (.55%) than inverted ones
(.51%) [F(1,8) = 5.01, p = .05], whereas the right IOG did not
show significant orientation effects (F < 1). Moreover, planned
comparisons on the child data showed that activation was
higher in the left (.56%) than in the right IOG (.53%) only for
upright faces [F(1,10) = 5.09, p = .047]. The teens showed a similar
but non-significant trend [F(1,8) = 4.03, p = .08]. Adults exhibited
significantly more activation in the right IOG (.51%) than the left
IOG (.46%) [F(1,9) = 13.95, p = .005], but no other effects or
interactions were significant for this group (F < 1). Finally, when we
compared each group with one another the only significant finding
was that children (.56%) [F(1,27) = 12.7, p = .002] and teens (.51%)
[F(1,27) = 8.13, p = .008] exhibited higher activation than adults
only in the left IOG.
Medial fusiform gyrus (MFG) ROI
In an initial ANOVA Age effects were significant in this region
[F(1,27) = 7.30, p = .003], in that percent signal was significantly
higher in children (.53%) than in adults (.18%) [F(1,27) = 11.79,
Fig. 5. ROI analyses results for the right and left Superior Temporal Gyrus
(STS), showing the mean percent signal change obtained for upright and
inverted faces from the functionally defined STS ROI in children (N = 11),
teens (N = 9), and adults (N = 10). (a) Right STS. Only adults exhibited a
significantly higher percent signal change for upright than for inverted faces
[F(1,9) = 49.41, p < .00006]. (b) Left STS. No significant results were found
(F values < 1). Asterisks indicates significance at p < .001. Error bars in
panels a, b represent the SEM.
p = .002] and teens (.21%) [F(1,27) = 9.46, p = .005], who did not
differ from each other (F < 1). Although children showed a trend
for more activation with inverted faces, and adults showed a trend
for more activation with upright faces, the interaction of
Age Orientation did not reach significance [F(2,27) = 2.20,
p = .13] (Fig. 7). Different from the other ROIs, the factor of
Hemisphere did not interact with other factors in MFG. Finally,
separate ANOVAs by Orientation revealed a significant Age effect
only for inverted faces [F(2,27) = 6.34, p < .006] in that for these
trials the percent signal in MFG was significantly higher in
children (.53%) than in adults (.18%) [F(1,27) = 10.02, p = .004]
and teens (.21%) [F(1,27) = 7.58, p = .01], who did not differ from
each other (F < 1).
1717
Comparison between LFG and MFG levels of activation

Finally, we wished to examine whether the present fMRI data may
show a developmental shift in neural engagement for face processing
from medial fusiform regions to face-selective lateral fusiform
regions. We performed an ANOVA with Age as the between-subjects
factor and ROI (MFG, LFG), Hemisphere and Orientation as
the within-subjects factors. A significant four-way interaction
[F(2,27) = 5.12, p < .01] revealed that for upright faces, in the RH
none of the groups showed a difference between levels of activation in
LFG and MFG. The age groups did not differ in right LFG activation
(F values < 1), but childrens levels of activation in the right MFG were
marginally higher than those of the other two groups [F(1,27) = 3.18,
p = .08]. For upright faces, in the LH only children showed higher
percent signal change for MFG than LFG [F(1,27) = 37.8, p = .0001].
Fig. 7. Results for MFG ROI analyses. We present our results collapsed
across Hemisphere since we did not obtain significant hemispheric
differences. These results show the mean percent signal change obtained
for children (N = 11), teens (N = 9), and adults (N = 10), for upright and
inverted face Age was significant [F(1,27) = 7.30, p = .003], indicating that
children activated significantly more than adults [F(1,27) = 11.79, p = .002]
and teens [F(1,27) = 9.46, p = .005]. Error bars represent the SEM.
Finally, with inverted faces, in both hemispheres only children showed

higher percent signal for MFG than LFG (in RH: [F(1,27) = 4.71,
p = .04]; in LH [F(1,27) = 22.23, p = .0007]), while the other two
groups did not show this difference (F values < 1). In summary, robust
age differences were found only for inverted faces; only children
engaged more their medial fusiform regions than their lateral fusiform
regions in both hemispheres with inverted faces.
Correlation between Age and Neural FIE

We performed Pearson correlation analyses (2-tailed) to further
examine the relationship between Age and the upright face
processing advantage in each of our ROIs. Confirming our results
from the ROI analyses, only for the right LFG there was a
significant positive correlation between neural FIE and Age
(r = .60, p = .001). This correlation was not significant for the left
LFG (r = .10, p = .62), the left IOG (r = .11, p = .56), the right
IOG (r = .14, p = .46), and the left STS (r = .09, p = .45). Moreover,
we found a correlation trend for the right STS (r = .32, p = .09),
which did show a significant increase in preference for upright
orientation with age in the ROI analyses, and for the MFG (LH and
RH combined; r = .33, p = .08), which had also shown a similar
trend in the ROI analyses, though not significant.
Correlation between Behavioral FIE and Neural FIE
Fig. 6. ROI analyses results for the right and left inferior occipital gyrus
(IOG), showing the mean percent signal change obtained from the
functionally defined IOG ROI in children (N = 11), teens (N = 9), and adults
(N = 10) for the upright and inverted faces. (a) Right IOG. No significant
effects of orientation were found. (b) Left IOG. A main effect of Age was
significant [F(2,27) = .004], in that children and teens activated significantly
more (p < .05) than adults for both orientations. Error bars in panels a, b
represent the SEM.
Finally, we carried out correlation analyses across all our

participants to examine the relationship between the behavioral FIE
(inverted face RT upright face RT) and the neural FIE (% signal
for upright faces % signal for inverted faces). We did this for each
of our ROIs to identify which one (s) may be the closest neural
correlate(s) of the behavioral FIE. We found that only for the right
LFG (r = .39, p = .04) there was a significant positive correlation
between the behavioral and the neural FIE patterns. That is,
participants who exhibited faster RT for upright faces than for
1718
inverted faces also exhibited higher activation for upright than for
inverted faces in the right LFG, and vice versa. This was true
across all ages, but as we reported above while the majority of
adults exhibited a preference for the upright orientation only 33%
of teens and 10% of children did so. Fig. 8 shows a scatter plot on
the correlation between the neural FIE and behavioral FIE for the
right LFG in each age group.
No significant correlations were found for the left LFG (p = .47),
the left STS (p = .83), the right IOG (p = .55), the left IOG (p = .47),
and for the MFG (LH and RH combined; p = .48), which confirms
that these regions provide a level of analysis that is not face-specific
(Haxby et al., 1999; Ishai et al., 1999). Therefore, in accord with the
current ROI findings, and similar to a study with adults by Yovel and
Kanwisher (2005) the correlation analyses indicate that the right
LFG may be the closest neural correlate of the behavioral FIE.
Interestingly, we found a marginally significant correlation also
between the neural FIE and the behavioral FIE in the right STS
(r = .36, p = .053). Moreover, the right LFG and the right STS FIE
patterns correlated significantly with each other (r = .51, p = .005),
but not with any other ROI, which confirms that these two regions
interact closely during face processing and exhibit similar neural FIE
patterns. Therefore the right STS may be a secondary correlate for
the behavioral FIE when, like in our study, the task taps specifically
onto STS functions by requiring processing of facial expressions
(Puce et al., 1998; Winston et al., 2004).
Lastly, we performed separate correlations by Age, to obtain
some insight on whether the neural correlates of the behavioral FIE
may change with age. Although our results were not significant,
(possibly due to our small samples) they were suggestive of a
developmental trend, such that, in adults there was a marginal
correlation between the behavioral FIE and the neural FIE in right
LFG (r = .56, p = .08), whereas teens did not show any significant
results (p > .05), and children showed a marginal correlation only in
right MFG (r = .55, p = .09) but not in right LFG (p = .15) (see Fig. 8).
Discussion
The main goal of the present study was to establish the neural
correlates of the behavioral FIE from childhood to adulthood. Our
Fig. 8. This scatterplot shows the correlation between the neural FIE in right
LFG (% change for upright faces % change for inverted faces) and the
behavioral FIE (RT for inverted faces RT for upright faces) in each age
group. Note that positive numbers in neural and behavioral FIE indicate a
preference for upright faces, whereas negative numbers indicate a preference
for inverted faces.
findings provide one of the first pieces of evidence that links the
development of the neural bases of the behavioral FIE to specific
face-selective regions in the right hemisphere. Moreover, they
show evidence of progressive tuning of these regions to the upright
orientation with development.
Starting with the behavioral FIE results, performance for all
groups showed accuracies well above 90%. While previous
developmental studies provided contrasting results in terms of
whether FIE increases with age (Mondloch et al., 2003) or not
(Young and Bion, 1980; Pascalis et al., 2001), the present RT
results are suggestive of developmental changes in FIE profiles,
because it is not until adulthood that we see a consistent cost in RT
with face inversion. Moreover, similar to other developmental
studies (Chun and Thomson, 1995; Flin, 1985; Taylor et al., 2004)
even our teens did not exhibit an adult-like FIE, which indicates
that changes in face processing strategies continue well beyond the
age of 10, as was initially proposed (Carey, 1992; Carey and
Diamond, 1977).
With regard to our fMRI results, we found developmental
differences in the neural bases of the FIE, and these differences
were specifically for the right LFG, which has been found to be
specialized for whole-based face processing (an indicator of face
processing expertise), but not the left LFG, which seems to be
more involved in part-based face processing (Rossion et al., 2000).
In general, while overall children showed higher profiles of
functional activation than teens and adults (see also Passarotti et
al., 2003; Gathers et al., 2004), significant age differences in activation were found only for inverted faces. Our analyses revealed
that adults exhibited the expected pattern of neural FIE (i.e., a
preference for the upright orientation), with higher percent signal
change for upright than for inverted faces. Also teens exhibited
higher activation for upright than for inverted faces in the right
LFG, but not significantly so, which is indicative of prolonged
neural and functional development of this face-selective region
well beyond childhood. Importantly for our study, younger
children exhibited a different neural FIE pattern than adults and
teens in the right LFG. In fact, they showed evidence of a
reversed neural FIE, in that their percent signal change in right
LFG was actually significantly higher for inverted than for upright
faces. This dramatic difference was somewhat unexpected, given
that children did not exhibit significant orientation effects in the
behavioral performance. But an inspection of the individual RT
data revealed that also for the behavioral performance children
exhibited a trend for an inverted orientation preference (i.e., faster
RT for inverted than for upright faces), although not significantly
so. It is noteworthy that a number of developmental studies
(Schlagger et al., 2002; Passarotti et al., 2003) have also found
significant age differences in neural activation in the absence of
significant behavioral differences. This suggests that developing
brain systems are somewhat immature or inefficient in children,
and may require more functional activity or a different profile of
functional activity compared to adults, to reach similar levels of
behavioral performance (Nelson et al., 2003).
We will now briefly report FIE contributions of additional areas
in the distributed face processing system (Haxby et al., 2000). Of
these regions, only the face-selective, right STS showed a
developmental shift from a trend for higher activation with the
inverted orientation in children to a significant upright face
preference in adults. Children exhibited more bilateral activation
and relied more than adults on the left STS, which suggests that
they were relying on processing strategies that are not face-specific
(Rossion et al., 2000) more than adults. Furthermore, in accord

with previous findings (Leube et al., 2003; Yovel and Kanwisher,
2005), we did not find an orientation effect in IOG at any age,
confirming that this region does not engage in face-specific
processes (Ishai et al., 1999) and therefore does not undergo robust
developmental FIE changes. Similar to what we found for the
LFG, the MFG data revealed less robust, non-significant trends for
higher activation with inverted faces in children and teens, and
higher activation for upright faces in adults. Lastly, while for
upright faces none of the age groups exhibited differences between
right MFG and LFG levels of activity, with inverted faces only in
children MFG activation was higher than that in LFG, suggesting
that with inverted faces children may rely more on this region,
which does not use face-specific processing strategies (Ishai et al.,
1999).
Turning to our main developmental FIE finding, one possible
explanation for the higher right LFG activity with inverted faces in
children could be that it is caused by a general increase in neural
effort in order to extract relevant information from faces that are in
an unusual and unfamiliar orientation. That is, since children are
still developing their face processing skills (Taylor et al., 2004;
Baenninger, 1994) they may not be able to adjust their strategies
efficiently depending on face orientation. If this were true, the
neural effort resulting from inverted face processing would be most
likely associated with higher RT. On the contrary, this is not the
case in the current data, because most children were actually
somewhat faster with inverted than with upright faces, while still
exhibiting high accuracies for both orientations. When we
examined the relation between behavioral and neural FIE in the
individual data for the right LFG we found two FIE profiles that
were represented either mostly by adults or mostly by children.
Specifically, the majority of adults (60%) exhibited the typical
FIE profile, with a preference for the upright orientation (i.e.,
faster RT and higher activation for upright faces), while only 10%
of children and 33% of teens did so. Most children (60%) actually
exhibited a reverse FIE profile (i.e., faster RT and higher
activation for inverted faces), while no adults and only 22% of the
teens did so. Clearly then, the general effort explanation for the
children data does not hold, because the majority of children did
not exhibit the effort profile, rather they exhibited a relative
preference for inverted faces in RT and a significant preference for
inverted faces in the fMRI data.
Further research with larger samples and more differentiated
age groups will be necessary to gain a deeper understanding of
these intriguing developmental results. At this point we can only
speculate on the mechanisms that underlie this relative preference
for the inverted face orientation in children, and the neural and
cognitive changes that lead to adult expertise in face processing.
Some studies suggest that developmental changes in holistic and
configural processing (Baenninger, 1994; Taylor et al., 2004;
Gathers et al., 2004, Aylward et al., 2005). Whatever these changes
are, our results provide some clues on at least one possible
mechanism that may lead to the adult expertise, that is a
progressive selectivity of face-selective regions to the upright
orientation.
While it is clear that in adults a behavioral preference for
upright faces is associated with face processing expertise
(Valentine, 1988), there is growing neurophysiological evidence
that also the neural bases of face processing favor the upright face
orientation, at least in adults. Yovel and Kanwisher (2005) found
sharper FFA tuning to upright than to inverted faces by using an
1719
fMRI-adaptation paradigm with adults. In addition, a recent study

by Tsao et al. (2004), that combined fMRI and single-unit
recordings, identified for the first time a whole cortical region in
the infero-temporal cortex of the macaque brain consisting entirely
of face-selective cells, which also showed an inversion effect.
Moreover, both neuropsychological studies with brain-damaged
patients (Moscovitch et al., 1997; Farah et al., 1995) and a recent
behavioral study that examined after-effects for upright and
inverted face pictures (Rhodes et al., 2004), suggest that different
mechanisms may be responsible for processing of upright and
inverted faces. We still do not know whether within the middle
fusiform gyrus there is only one population of neurons that
responds preferentially to upright faces, or whether there are
different populations that respond preferentially either to the
upright or the inverted orientation (see also Yovel and Kanwisher,
2005 for a discussion of this issue). Based on the current results,
we can only speculate that if there is one neural population in right
infero-temporal regions that is selective to faces in the upright
orientation, this level of selectivity may progressively increase
during development. A progressive shift in orientation preference
may be one of the mechanisms that enable acquisition of face
processing expertise with age. Alternatively, if there are indeed
distinct neural populations that prefer either one orientation or the
other, or have no preference, we could hypothesize that younger
children may engage relatively more the neural populations that
rely on non-face specific processing levels (which are more
efficient for inverted than for upright faces). These neural
populations may also interact more with medial and posterior
fusiform regions, with which they may share similar processing
strategies (i.e., featural or part-based processing). With age and
progressive specialization the neural circuitry that favors the
upright orientation may develop more efficient face-selective
processes, and eventually become the elected circuitry for expert
face processing.
Another important goal of the present study was to identify
which region is the closest neural correlate of the behavioral FIE
(hence of face processing expertise). We were able to identify the
right LFG as the closest neural correlate, by showing a significant
positive correlation between the behavioral FIE and the neural FIE
only in this ROI. Yovel and Kanwisher (2005) found similar results
for adults in the FFA, although they did not find hemispheric
differences. Our paradigm was able to further segregate the neural
bases of the behavioral FIE to the right hemisphere, which is
specialized for configural face processing (Haxby et al., 1999;
Kanwisher et al., 1997) or holistic processing (Yovel and
Kanwisher, 2004). In addition, our results indicate that although
the typical FIE profile was present much more in adults than in
teens and children, across ages those individuals who exhibited a
RT advantage for upright faces also exhibited a preference for
upright orientation in the right LFG activity, and vice versa. This
finding indicates that across development, there is a link between a
preference for upright orientation and efficiency of face processing.
We also found that the neural FIE in STS presented a marginally
significant correlation with the behavioral FIE, and also correlated
with the FIE in the right LFG, which confirms that these two-face
selective regions in the right hemisphere interact closely during
face processing. In addition, this finding suggests that the STS may
be a secondary correlate of the behavioral FIE if the experimental
task taps specifically onto STS function such as processing of
facial expressions (Puce et al., 1998). In fact, Yovel and Kanwisher
(2005) did not find a significant correlation with the behavioral FIE
1720
for STS, because their face identification task did not rely
specifically on STS processing (Puce et al., 1998; Winston et al.,
2004).
Having identified the correlates of the behavioral FIE, the next
crucial developmental question is whether they may change with
age. In fact, previous fMRI studies (Gathers et al., 2004; Passarotti
et al., 2003) found that younger children engaged not only the
LFG but also other medial and posterior fusiform regions to
process faces. Although we cannot draw any strong conclusions
from our marginally significant results, our findings hint at a
developmental change of the direct neural correlate for the behavioral FIE, in that while adults exhibited a marginally significant
correlation between behavioral FIE and right LFG, teens showed
no significant results, and in children it was actually the right
MFG, but not the right LFG, that showed a marginally significant
correlation. This is an interesting result, since our ROI analyses
did find that for upright faces children activated their right MFG
more than the other two groups (although not significantly so), and
for inverted faces they activated more their right MFG than the
right LFG. While larger samples are needed to further clarify these
trends, the present findings suggest that different from the adult
profile, the child behavioral preference for inverted orientation
may be associated with relatively more engagement of the right
MFG, a region that employs non-face-specific processing
strategies (Ishai et al., 1999).
Turning now our attention to a more general issue, one may ask
whether we can generalize our developmental findings to face
processing that does not involve emotions. We can reasonably
exclude that our developmental FIE results were driven by the
emotional content of our face stimuli, or by attentional effects due
to the emotional content, for the following reasons. First, there is
evidence that the right LFG response to faces is not affected by the
type of face processing employed, as long as the stimuli employed
are perceived as faces (Kanwisher et al., 1997). Second, although
some attentional modulation of the FFA has been found when
attentional shifts from one attribute of a composite object to
another were required (OCraven et al., 1999), other studies
involving a face emotion processing paradigm found FIE patterns
that were comparable to those for face-identity tasks that did not
have emotional information and therefore should not have any
attentional confound (Calder et al., 2000; McKelvie, 1995).
Moreover, the current adult and teen fMRI FIE profiles closely
replicate findings from other adult studies that used a face-identity
task instead of our face-emotion task (Yovel and Kanwisher, 2004;
Haxby et al., 1999; Kanwisher et al., 1998). Even our child data for
upright faces are very similar to findings from a face-matching task
that did not involve facial emotions (Passarotti et al., 2003; Gathers
et al., 2004). Third, a recent fMRI-adaptation study (Winston et al.,
2004) found a neuro-anatomical dissociation for processing of face
identity in LFG, and face expressions in STS; therefore our FIE
results in LFG should not be affected by facial emotions.
Moreover, any general attentional effects in our data would be
present both for upright and inverted face trials, and therefore when
comparing functional activation for upright and inverted faces any
attentional effect would be canceled out. Similarly, when we
compared our FIE patterns for emotional face trials (which have an
emotional content) and neutral face trials (with no emotional
content) we did not find any significant differences (see Footnote
1).
It is important to note that while the present study provides
evidence on the development of the neural correlates of the
behavioral FIE, it also presents some limitations and leaves open

questions that call for more research. For instance, this study
cannot tell us whether the developmental inversion effects that we
found in right LFG and STS are specific to faces, or may reflect
more general mechanisms, in which case our FIE results would
extend to other non-face stimuli in children. Moreover, it will be
important that future studies clarify the changes in processing
strategies (e.g., improvements in configural and holistic processing) that contribute to the progressive neural tuning to upright
orientation with age. In the meantime, useful insights come from a
developmental fMRI study that indeed contrasted neural activity
for upright faces and objects in children, and found that while 5 to
8 year olds exhibited selectivity for upright faces versus objects
outside of the fusiform gyrus, by age 911 selective fusiform
activation for faces versus objects emerged (Gathers et al., 2004).
Similarly, Aylward et al. (2005) found that the selective fusiform
engagement for faces versus houses increased up to adolescence.
These results suggest that the right fusiform gyrus undergoes
prolonged development before it becomes more engaged for
upright faces than objects, and that the emergence of this
preference is possibly associated with improvements in facespecific processes (Gathers et al., 2004; Aylward et al., 2005;
Taylor et al., 2004).
Finally, these important changes in the brain circuitry for face
processing are most likely the result of an interaction between
neural maturation and experience. Studies with infants indicate
very precocious preference for faces over objects (Morton and
Johnson, 1991) and very early engagement of right hemisphere
regions for face processing (Tzourio-Mazoyer et al., 2002). At the
same time, specific early visual input during critical periods of
development is necessary for the right hemisphere to fully develop
face processing expertise later in life 8. In fact, a developmental
study by LeGrand et al. (2003) found that children whose right
hemisphere was deprived of any visual input because of congenital
unilateral cataract, exhibited impairment in face configural
processing (but not featural processing) even years after the
cataracts were removed. Moreover, maturation, myelination,
synapse overproduction and pruning continue until mid-adolescence (Luna et al., 2004) and contribute to a progressive
localization of cognitive functions (Gathers et al., 2004; Passarotti
et al., 2003) and improvements in processing speed and efficiency
(Mondloch et al., 2003; Taylor et al., 2004). At the same time,
these neurophysiological changes are also enabled and guided by
experience (Stiles et al., 2003). An example of fusiform gyrus
plasticity to experience and learning is provided by Gauthiers
findings that in adults the right lateral fusiform gyrus may show
increased sensitivity to non-face stimuli for which an individual
has acquired processing expertise (Gauthier et al., 1999) (but see
McKone and Kanwisher, 2005 for an alternative explanation of
Gauthiers results). Altogether these findings suggest that development and fine tuning of the cortical regions that will later enable
face processing expertise require an orchestrated interaction of
neural maturation and experience.
Conclusions
The present developmental fMRI study established the functional and anatomical organization of the neural FIE in children
and teenagers. In addition, it identified the right LFG, and to a
lesser degree the right STS, as the closest neural correlate of the
behavioral FIE, while also providing some initial clues that FIE
correlates may change with age. Finally, in agreement with

behavioral (Baenninger, 1994, Chun and Thomson, 1995) and ERP
studies (Taylor et al., 2001, 2004), our current findings suggest that
there is a gradual, progressive tuning of face-selective regions in
the right hemisphere to the upright orientation until late
adolescence.
Acknowledgments
We wish to thank the children and families who participated in
our study and the Department of Radiology at Michigan State
University for providing the scanning facilities. Many thanks to
Lauren Harris and Marie Banich for helpful comments on previous
drafts of this paper. Face stimuli were taken from the NimStim Face
Stimulus Set. Development of the MacBrain Face stimulus set was
overseen by Nim Tottenham and supported by the JD and CT
MacArthur Foundation Research Network on Early Experience
and Brain Development.
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Developmental differences in the neural bases of the face

Received 12 October 2005; revised 5 July 2006; accepted 6 July 2006

Face inversion hinders face processing in adults, while not affecting

The ability to recognize and discriminate between different

Gathers et al., 2004) and behavioral (Carey, 1992; Diamond and

A.M. Passarotti et al. / NeuroImage 34 (2007) 17081722

M170 (a face-selective component that possibly originates in the

slowly and improves through adolescence (Taylor et al., 2001,

A.M. Passarotti et al. / NeuroImage 34 (2007) 17081722

from the local community and Michigan State University. All

emotions (i.e., happy or angry). Each 5-s trial began with a

Brain imaging procedures

A.M. Passarotti et al. / NeuroImage 34 (2007) 17081722

fMRI image processing

A.M. Passarotti et al. / NeuroImage 34 (2007) 17081722

the fiducial volume. The signal was then orthogonalized to the

A.M. Passarotti et al. / NeuroImage 34 (2007) 17081722

A.M. Passarotti et al. / NeuroImage 34 (2007) 17081722

tion was not significant (F<1). Separate ANOVAs by Age showed

A.M. Passarotti et al. / NeuroImage 34 (2007) 17081722

children did not exhibit an effort profile, rather a preference profile

children showed this profile, while only 22% of teens, and no

A.M. Passarotti et al. / NeuroImage 34 (2007) 17081722

[F(1,27) = 4.39, p = .05] had higher activation in the left STS,

A.M. Passarotti et al. / NeuroImage 34 (2007) 17081722

Comparison between LFG and MFG levels of activation

Finally, with inverted faces, in both hemispheres only children showed

Correlation between Age and Neural FIE

Finally, we carried out correlation analyses across all our

A.M. Passarotti et al. / NeuroImage 34 (2007) 17081722

A.M. Passarotti et al. / NeuroImage 34 (2007) 17081722

(Rossion et al., 2000) more than adults. Furthermore, in accord

fMRI-adaptation paradigm with adults. In addition, a recent study

A.M. Passarotti et al. / NeuroImage 34 (2007) 17081722

behavioral FIE, it also presents some limitations and leaves open

A.M. Passarotti et al. / NeuroImage 34 (2007) 17081722

correlates may change with age. Finally, in agreement with

Flin, R.H., 1985. Development of face recognition: an encoding switch? Br.

A.M. Passarotti et al. / NeuroImage 34 (2007) 17081722

adults and school-age children in the processing of single words. Science

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