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Temporal Cortex Activation in Humans Viewing Eye and
Mouth Movements
Aina Puce,
1,2
Truett Allison,
1,3
Shlomo Bentin,
5
John C. Gore,
4
and Gregory McCarthy
1,2,3
1
Neuropsychology Laboratory, Veterans Administration Medical Center, West Haven, Connecticut 06516, Departments of
2
Neurosurgery,
3
Neurology, and
4
Diagnostic Radiology, Yale University School of Medicine, New Haven, Connecticut
06510, and
5
Department of Psychology and Center for Neural Computation, Hebrew University, Jerusalem 91905, Israel
We sought to determine whether regions of extrastriate visual
cortex could be activated in subjects viewing eye and mouth
movements that occurred within a stationary face. Eleven sub-
jects participated in three to five functional magnetic resonance
imaging sessions in which they viewed moving eyes, moving
mouths, or movements of check patterns that occurred in the
same spatial location as the eyes or mouth. In each task, the
stimuli were superimposed on a radial background pattern that
continually moved inward to control for the effect of movement
per se. Activation evoked by the radial background was as-
sessed in a separate control task. Moving eyes and mouths
activated a bilateral region centered in the posterior superior
temporal sulcus (STS). The moving check patterns did not
appreciably activate the STS or surrounding regions. The acti-
vation by moving eyes and mouths was distinct from that
elicited by the moving radial background, which primarily acti-
vated the posterior-temporal-occipital fossa and the lateral
occipital sulcus—a region corresponding to area MT/V5. Area
MT/V5 was also strongly activated by moving eyes and to a
lesser extent by other moving stimuli. These results suggest
that a superior temporal region centered in the STS is prefer-
entially involved in the perception of gaze direction and mouth
movements. This region of the STS may be functionally related
to nearby superior temporal regions thought to be involved in
lip-reading and in the perception of hand and body movement.
Key words: extrastriate cortex; eye movement; mouth move-
ment; temporal lobe; superior temporal sulcus; gaze direction
Face recognition and analysis of facial expression form an impor-
tant part of everyday interaction for humans and other primates.
Electrophysiological studies in humans have demonstrated that
discrete regions within the fusiform gyrus respond preferentially
to faces and that stimulation of those regions can lead to transient
prosopagnosia (Allison et al., 1994a,c). Neuroimaging data have
provided further support for the role of ventral occipitotemporal
cortex and, in particular, the fusiform gyrus in face perception
(Sergent et al., 1992a; Haxby et al., 1994; Puce et al., 1995, 1996;
Clark et al., 1996; Kanwisher et al., 1997; McCarthy et al., 1997).
A close correspondence of ventral regions activated by faces in
neuroimaging and electrophysiological studies has been recently
demonstrated in the same individuals (Puce et al., 1997a). Activa-
tion by faces is not, however, limited to ventral occipitotemporal
cortex. For example, in previous neuroimaging studies, we have
shown discrete foci of activation to faces in lateral temporal cortex,
particularly in the right hemisphere (Puce et al., 1995, 1996). We
have also recorded event-related potentials (ERPs) sensitive to
faces directly from lateral temporal cortex (Puce et al., 1997a).
Studies in nonhuman primates have suggested a functional
differentiation of regions responsive to faces. Face-sensitive neu-
rons are found within monkey inferior temporal (IT) cortex and
within the superior temporal sulcus (STS) (Desimone, 1991;
Gross, 1992; Perrett et al., 1992; Rolls, 1992). However, neurons
within the STS are also sensitive to gaze and head direction and
to face parts (Perrett et al., 1985, 1992; Yamane et al., 1988;
Hasselmo et al., 1989). Some cells in the STS also respond to
moving views of the head and body (Perrett et al., 1990) and to
“biological motion” (Oram and Perrett, 1994) using point-light
displays (Johansson, 1973).
It is possible that a similar functional distinction exists between
ventral and lateral regions responsive to faces in humans. ERPs
recorded directly from ventral cortex, primarily the fusiform gyrus,
are larger to full faces than to isolated eyes (Allison et al., 1994b).
By contrast, ERPs recorded over the lateral temporal scalp are
larger to isolated eyes than to full faces (Bentin et al., 1996).
Neuropsychological studies also suggest that portions of the tem-
poral lobe are sensitive to face parts. For example, some patients
with temporal lobe lesions are deficient in determining gaze direc-
tion, whereas others can no longer lip-read (Campbell et al., 1986;
Perrett et al., 1988). Taken together, these results suggest the
existence of neuronal systems sensitive to face parts located in
lateral occipitotemporal cortex, in addition to face-perception
mechanisms located in ventral occipitotemporal cortex.
In this study, we investigated the cortical activation patterns of
subjects viewing faces in which the eyes repeatedly changed their
direction of gaze or the mouth opened and closed. The results
demonstrate that a region of superior temporal cortex, located
primarily in the STS, is activated preferentially by moving eyes
and mouths.
A preliminary report of these results has appeared (Puce et al.,
1997b).
MATERIALS AND METHODS
Subjects. Eleven right-handed, neurologically normal subjects (six males)
with an average age of 33.7 (range, 25–47) years participated in these
studies. All subjects gave their informed consent for a protocol approved
Received Oct. 7, 1997; revised Dec. 22, 1997; accepted Dec. 22, 1997.
This work was supported by the Department of Veterans Affairs, by the US-Israel
Binational Science Foundation, and by National Institutes of Mental Health Grant
MH-05286. We thank H. Sarofin for assistance.
Correspondence should be addressed to Dr. Aina Puce, Neuropsychology Labo-
ratory 116B1, Veterans Administration Medical Center, West Haven, CT 06516.
Copyright © 1998 Society for Neuroscience 0270-6474/98/182188-12$05.00/0
The Journal of Neuroscience, March 15, 1998, 18(6):2188–2199
by the Human Investigation Committee of Yale University School of
Medicine. Each subject participated in three to five imaging sessions.
Experimental task s.There were six experimental tasks (Fig. 1, top
panel ). Each consisted of two subtasks (A and B) that alternated
throughout each imaging run as described previously (Puce et al., 1995,
1996). The duration of each subtask was 6 sec (Fig. 1, bottom panel ).
Fifteen AB cycles were presented during the 192 sec duration of each
imaging run. Each task was replicated four times; i.e., four imaging runs
were acquired. Two of these runs began with subtask A (ABAB . . .), and
two runs began with subtask B (BABA . . .). The starting order was
counterbalanced across imaging runs.
In the EYES task, one of two possible faces (male or female) was
continuously present during the duration of the imaging run. In this and
all other tasks, the male and female faces were used on alternate runs.
The faces were in color and were superimposed on a radial background
pattern consisting of three concentric black, white, and gray rings (Fig. 1,
bottom panel ). In subtask A, the eyes within the face seemed to move
naturally from the center to the left and then back to center, or from the
center to the right and then back to center. This apparent eye movement
was achieved by presenting 10 successive pictures over the 6 sec duration
of the subtask in which the eyes were either centered, fixated left, or
fixated right, while the head stayed in register. The sequence of apparent
eye movements was random, and there were equal numbers of right and
left movements across runs. In subtask B, the eyes remained fixed at the
Figure 1. The top panel illustrates the six experimental tasks. In EYES, lateral eye movements were contrasted to a static face with the eyes looking
straight ahead. In MOUTH, an open mouth was contrasted to a closed mouth in a static face. Eye movements were contrasted with mouth movements
in the EYES versus MOUTH task. In SIMULATED (SIM ) EYES and SIMULATED MOUTH, colored checkerboard patterns with checks reversing
position in spatially equivalent positions (white arrows) to the real eyes and mouth were contrasted to a static checkerboard. In all of these tasks the radial
background moved continuously in an inward direction (small white arrows) during the entire duration of the imaging run. In RADIAL, the face
remained static, and the radial background either moved in the direction indicated by the white arrows or remained static. The effect of an inwardly
moving radial background was generated by changing the color of the concentric rings on each frame (see bottom panel ). The bottom panel depicts a
schematic of a single cycle in the ABAB alternating design for the EYES versus MOUTH task. The duration of each subtask (A or B) was 6 sec. During
each subtask, a series of 10 images (600 msec duration) was shown. In subtask A, the eyes shifted their position from the center to either left or right
and back to center in a random manner. In subtask B, the mouth closed on alternate frames.
Puce et al. • Temporal Lobe Activation to Moving Eyes and Mouths J. Neurosci., March 15, 1998, 18(6):2188–2199 2189
center. Thus, the subject viewed alternating periods of eye movements
and fixation on an otherwise stationary face. The purpose of this manip-
ulation was to identify brain regions activated by movement of the eyes.
During both subtasks of EYES, the radial background seemed to
continuously move inward. This radial motion was designed to activate
brain regions sensitive to motion per se and to diminish their contribu-
tion to the activation differences between eye movement and eye fixation.
The MOUTH task was similar to the EYES task. In subtask A, the
mouth within the face seemed to open and close. In subtask B, the mouth
remained closed. The radial background moved continuously in both
subtasks, as described above. The purpose of this task was to identify
brain regions activated by mouth movements.
In the EYES versus MOUTH task (Fig. 1, bottom panel ), subtask A
consisted of moving eyes as described above for EYES. Subtask B
consisted of the moving mouth as described above for MOUTH. Thus, in
this task the subject viewed alternating periods of eye and mouth move-
ments. This task was designed to identify activations specific to eye or
mouth movement while de-emphasizing activations common to both
types of movement. The radial background continuously moved inward
as described above.
In the SIMULATED EYES task, the face was replaced by an oval
equal in area to the average area of the two faces used in the previous
tasks. The oval contained a rectangular pattern of checks, the overall
luminance and contrast of which were equal to the average luminance
and contrast of the two individual faces. The check colors were chosen
from the red–green–blue values of the faces and their inner components.
The exposed area of the continuously moving radial background was the
same as in the previous tasks. In subtask A, checks similarly located
within the rectangle as the eyes were located within the face made
discrete left and right movements. These movements had identical timing
to the eye movements as described above. The movements, however,
were not conjugate to avoid the illusion that the flesh-colored pattern was
an abstract face. In subtask B, the checks did not move. This task was
designed to determine whether activations generated by the moving eyes
in the EYES and EYES versus MOUTH tasks were simply because of
movements in a specific part of the visual field.
In the SIMULATED MOUTH task, subtask A consisted of the
movement of checks similarly located within the rectangle as the mouth
was located within the face and equal in area. The movement of the
checks mimicked the opening and closing movements of the mouth. No
movements occurred in subtask B. The radial background moved con-
tinuously during both subtasks A and B.
In the RADIAL task, a stationary face was presented during the entire
imaging run. In subtask A, the radial background moved inward as
described above. However, in subtask B the radial background did not
move. This task was designed to identify brain areas activated by the
radial motion.
Subjects were instructed to attend to the stimulus on the screen and to
focus on a point midway between the eyes of the face for the duration of
each imaging run. Similarly, for the control conditions using the check-
erboards, subjects were instructed to focus on a point in space identical
to that on the real face. The eye movements of subjects were not
monitored while they were in the scanner.
Three separate imaging sessions were required to complete all six
tasks. EYES, MOUTH, and RADIAL were run together in a single
session. EYES versus MOUTH was run in another session, and SIMU-
LATED EYES and SIMULATED MOUTH were run in a third session.
Eleven subjects completed the EYES, MOUTH, and RADIAL tasks.
Nine subjects completed the SIMULATED EYES and SIMULATED
MOUTH tasks, and eight subjects completed EYES versus MOUTH. In
addition to the above, six subjects returned for additional sessions
in which the EYES, MOUTH, and RADIAL tasks were repeated, but in
which images were acquired in oblique axial planes. Experimental timing
and stimulus presentation were controlled by computer. All stimuli were
back-projected onto a translucent screen mounted at the end of the
patient gurney. Subjects viewed stimuli through a mirror mounted on the
head coil. All stimuli subtended a visual angle of 5.4 3 5.4°.
Images were acquired using a 1.5 T General Electric Signa scanner
with a standard quadrature head coil and ANMR echoplanar subsystem
(ANMR Systems, Inc., Wilmington, MA). The subject’s head was posi-
tioned along the canthomeatal line and immobilized using a vacuum
cushion and forehead and chin straps. For the three sessions constituting
the main experiment, T1-weighted sagittal scans were used to select
seven contiguous coronal slices beginning at the posterior edge of the
splenium. Functional images were acquired using a gradient-echo echo-
planar sequence [repetition time (TR), 1500 msec; echo time (TE), 45
msec;
a
5 60°; number of excitations (NEX), 1; voxel size, 3.2 3 3.2 3
7 mm]. Each imaging run consisted of 128 images per slice. Four radio
frequency excitations were performed before image acquisition to
achieve steady-state transverse relaxation. Higher-resolution anatomical
images for these seven slices were acquired using a T1-weighted se-
quence [TR, 500 msec; TE, 11 msec; NEX, 2; field of view (FOV), 24 cm;
slice thickness, 7 mm; skip factor, 0; imaging matrix, 128 3 64]. Whole-
brain axial images were acquired using a spoiled gradient-recalled ac-
quisition in a steady state sequence (TR, 25 msec; TE, 5 msec;
a
5 45°;
NEX, 2; FOV, 24 cm; slice thickness, 2 mm; skip factor, 0; imaging
matrix, 256 3 192).
For the six subjects who repeated the EYES, MOUTH, and RADIAL
tasks, functional images were acquired from seven contiguous oblique
axial slices aligned parallel to, and centered on, the right STS. These
additional imaging runs were included to explore regions of the temporal
lobe anterior to the coronal slices used in the primary experiment.
Data analysis. All functional imaging runs were screened for move-
ment and other artifacts by examining center of mass plots supplemented
by visual inspection of the image series in a cine loop. Activated voxels
were then identified for each subject and task. Three images from each
subtask were used for analysis. These were offset by 4.5 sec from subtask
onset to compensate for the hemodynamic delay; i.e., images occurring at
4.5, 6.0, and 7.5 sec after the onset of each subtask were used for analysis.
Because there were 15 cycles per run and four imaging runs per task, 180
images per subtask were available for comparison. There were two run
pairs per imaging session, each pair consisting of one run performed in
an alternate task order (AB and BA). The alternate task orders were
used to provide experimental replicates that would balance any system-
atic physiological artifacts such as change in breathing pattern, or physical
artifacts associated with the onset of imaging. The AB run for each of the
two run pairs was averaged into a single AB run, and an unpaired t test
was performed voxel by voxel on that average. A similar unpaired t test
was performed on the average of the two BA runs. The t test images from
each replicate were then averaged. A criterion of t . 1.96 was used to
identify positive activations in this resulting t map, i.e., nominally a p ,
0.05 two-tailed test. However, because this criterion was applied to an
average of two t maps, the probability of a voxel with purely random
variation having a mean t value . 1.96 is 0.00125 (or 0.0025 when tested
two-tailed). Activated voxels were then superimposed on higher-
resolution anatomical images for each subject as the initial basis of
analysis. Because the scaling involved with image interpolation can
smooth the shape of the activation, all quantitative analyses were per-
formed on uninterpolated activation images. The Talairach coordinates
(Talairach and Tournoux, 1988) of activated voxels were then deter-
mined. Finally, the anatomical locations of activated voxels were deter-
mined by two investigators working together and were classified using the
atlas of Duvernoy (1991). The activated voxels within each anatomical
structure were then counted and further categorized as described below.
To simplify the initial anatomical analysis, the voxels were sorted into
four anatomical groups based on contiguity and previous functional
findings (Fig. 2). The dorsomedial region included the cingulate, superior
parietal, superior occipital, angular, and supramarginal gyri, the intrapa-
rietal and cingulate sulci, and the precuneus. The lateral region included
the superior temporal, middle temporal, inferior temporal, and middle
occipital gyri, the Sylvian, superior temporal, inferior temporal, and
lateral occipital sulci, and the parieto-temporo-occipital fossa (PTOF)
(Vaina, 1994). The PTOF and nearby cortex is a movement-sensitive
region (Watson et al., 1993; McCarthy et al., 1995; Tootell et al., 1995)
probably homologous to monkey movement-sensitive areas MT/V5 and
MST (Maunsell and Van Essen, 1983; Desimone and Ungerleider, 1986;
Tanaka and Saito, 1989; Lagae et al., 1994). We will use the term PTOF
to refer to an anatomically defined region and the term MT/V5 for
functionally defined movement-sensitive cortex. The ventral region com-
prised the fusiform, inferior occipital and fourth occipital gyri, and the
occipitotemporal and inferior occipital sulci. The ventral region includes
those regions strongly activated by faces in previous functional magnetic
resonance imaging (fMRI) studies (Puce et al., 1995, 1996; Clark et al.,
1996; Kanwisher et al., 1997; McCarthy et al., 1997). The ventromedial
region included the collateral and calcarine sulci, the lingual and cuneate
gyri, and the cuneus and parieto-occipital fissure.
Within subjects, repeated ANOVAs were computed in which the
number of activated voxels was the dependent variable and the task,
hemisphere (left or right), slice (1–7), and anatomical region (lateral,
dorsomedial, ventromedial, and ventral) were independent variables.
2190 J. Neurosci., March 15, 1998, 18(6):2188–2199 Puce et al. • Temporal Lobe Activation to Moving Eyes and Mouths
Four task comparisons were computed: (1) EYES, MOUTH, and RA-
DIAL; (2) EYES, MOUTH, SIMULATED EYES, and SIMULATED
MOUTH; (3) RADIAL, SIMULATED EYES, and SIMULATED
MOUTH; and (4) the moving eyes and moving mouth subtasks from the
EYES versus MOUTH task. Additional analyses were performed to look
for anatomical patterns within the structures constituting the four ana-
tomical regions.
RESULTS
Figure 3 presents results from a single subject for five experimen-
tal tasks. Five contiguous anatomical slices are shown, with the
most anterior slice at the left. Discrete foci of activation (framed
by white squares) in the right STS were observed in anterior slices
1 and 2 for EYES and MOUTH but not for SIMULATED
EYES, SIMULATED MOUTH, or RADIAL. In contrast, all
tasks activated the right PTOF in slice 4 (framed by white circles)
with additional bilateral activation of the PTOF in slice 5. Similar
patterns of activation were observed in the other subjects.
Figure 4 presents results from another individual for EYES
and RADIAL from coronal and axial imaging sessions. Activa-
tion of the right STS to EYES was observed in coronal slices 1–3
(Fig. 4A, white squares) and in the corresponding regions in axial
slices 5 and 7 (Fig. 4B, white squares). Less extensive activation of
the left STS was also observed (Fig. 4, A, slice 2, B, slice 7, white
squares). There was little or no activation to RADIAL in the STS
in these slices. In contrast, activation common to both tasks was
seen in the PTOF and the lateral occipital sulcus (LOS) (Fig. 4,
A, coronal slices 4–7, corresponding regions in B, axial slices
1–4).
Activation was observed in the intraparietal sulcus (IPS) to
EYES (Fig. 4A, slices 1, 2, framed by white circles) and to
RADIAL (Fig. 4A, slices 6, 7, framed by white circles). Activation
was also observed in the calcarine cortex and collateral sulcus to
RADIAL (Fig. 4, A, slices 4–7, B, slice 1).
Activation in the lateral region
Consistent with the illustrative data of Figures 3 and 4, the
greatest number of activated voxels occurred within the lateral
region for all conditions in all subjects. EYES and MOUTH
produced activation mainly in the anterior slices (Fig. 5, top),
whereas RADIAL produced activation mainly in slices 4 and 5 of
the left hemisphere ( p , 0.01 for task; p , 0.05 for slice; p , 0.01
for hemisphere 3 task 3 slice).
When the number of activated voxels in the right lateral region
was examined as a function of anatomical structure, the combined
STS and ITS accounted for 49 and 46% of the total activation for
EYES and MOUTH, respectively (Fig. 6, left panel). The number
of activated voxels for EYES was greater than that for MOUTH,
but this difference did not reach statistical significance ( p 5 0.12).
In contrast to the activation in STS and ITS by EYES and
MOUTH, RADIAL mainly activated the left PTOF and the
LOS (Fig. 6, right panel ), which together accounted for 58% of
the total activation across all slices in left lateral cortex.
As illustrated in Figures 3 and 4, the activation in lateral cortex
formed two discontinuous clusters, an anterior cluster elicited
mainly by EYES and MOUTH and a posterior cluster elicited by
all three tasks. The centroids of these clusters were calculated for
EYES, MOUTH, and RADIAL. The anterior centroids were
calculated in two ways: (1) an unrestricted method that included
all activated voxels from the Sylvian fissure to the inferior tem-
poral gyrus regardless of their proximity to the major activation
cluster; and (2) a restricted method that included only activated
voxels from the STS and ITS, in which the major activation
occurred. A similar approach was used to calculate the posterior
centroids. The unrestricted calculation included voxels from the
PTOF, LOS, and middle occipital gyrus, whereas the restricted
calculation included only voxels from the PTOF and LOS. As
shown in Table 1, the centroids for the unrestricted and restricted
calculations were virtually identical. Thus, the centroids calcu-
lated from the more restricted anatomical structures provide an
accurate representation of the results. A graphical depiction of
these centroids is shown superimposed on a sagittal view of a
representative brain in Figure 7, in which the close spatial corre-
spondence of the anterior centroids for EYES and MOUTH can
be appreciated. The spatial overlap of the posterior centroids for
EYES, MOUTH, and RADIAL is also apparent.
The preferential activation of STS to EYES and MOUTH is
shown in Figure 8. Here, a single cycle of activation was created
by averaging across all cycles for each of the EYES and MOUTH
tasks for 10 subjects (one subject with no activation to any task
was eliminated). The activated voxels in the right STS were
interrogated across the image time series for all experimental
runs. The magnetic resonance activation signal in the right STS
(Fig. 8) increased steadily during eye or mouth movement and
then decayed after movement cessation. The peak signal change
was 0.7%. There was negligible activation in these same voxels by
RADIAL.
Fewer voxels were activated within the lateral region during the
EYES versus MOUTH task. Only 40% of the voxels activated in
EYES were activated by moving eyes within EYES versus
MOUTH. Moving mouths within EYES versus MOUTH pro-
duced 67% of the voxels activated by MOUTH. These results
suggest considerable overlap in the activation by EYES and
MOUTH. The statistical analysis for EYES versus MOUTH
(Fig. 3, slices 1, 2) showed only a significant main effect of slice
( p , 0.01), indicating that activation occurred primarily in ante-
rior slices.
Even fewer voxels were activated in SIMULATED EYES and
SIMULATED MOUTH tasks. Significantly fewer voxels were
activated when both control tasks were compared with EYES and
Figure 2. Four anatomical regions for classification of activated voxels
(lateral, dorsomedial, ventromedial, and ventral) and their borders are
outlined on the lef t side of a coronal anatomical image. Some of the
structures falling within each region are shown on the right. STS, Superior
temporal sulcus; MTG, middle temporal gyrus; ITS, inferior temporal
sulcus; ITG, inferior temporal gyrus; OTS, occipitotemporal sulcus; FG,
fusiform gyrus; CS, collateral sulcus; LG, lingual gyrus; CaS, calcarine
sulcus; POF, parieto-occipital fissure; PrC, precuneus; Ci, cingulate gyrus
and sulcus; SPG, superior parietal gyrus; IPS, intraparietal sulcus; AG/
SuG, angular or supramarginal gyri.
Puce et al. • Temporal Lobe Activation to Moving Eyes and Mouths J. Neurosci., March 15, 1998, 18(6):2188–2199 2191
MOUTH (task p , 0.01) or with RADIAL (task, p , 0.01). No
other significant effects or interactions were noted. The restricted
posterior activation centroids for the SIMULATED EYES and
SIMULATED MOUTH were similar to those of EYES,
MOUTH, and RADIAL (Table 1).
The results of the 11 subjects tested with coronal slices showed
that the most consistent activation to EYES and MOUTH oc-
curred in the most anterior slices. This raised the concern that
our coronal slices may have been posterior to the main locus of
activation. For this reason, the six subjects with the strongest
activation in the lateral region were rescanned in an oblique
axial-imaging study for the EYES, MOUTH, and RADIAL
tasks. The patterns of activation in the axial study were similar to
those seen in the coronal studies (Fig. 4). The restricted activation
centroids in the STS and ITS for EYES and MOUTH in the axial
study were similar to those in the coronal study for both hemi-
spheres (Fig. 7, Table 1), indicating that the coronal study encom-
passed the main locus of activation to EYES and MOUTH. The
posterior activation centroids in the axial study were virtually
unchanged from the coronal study (Fig. 7, Table 1).
Activation in the dorsomedial region
Fewer voxels were activated within the dorsomedial region than
the lateral region. The most prominent activation occurred for
EYES in slices 1 and 2 of the left hemisphere (Figs. 4A, slices 1,
2, white circles,5,second from top) and for RADIAL in slices 5–7
in both hemispheres (Figs. 4B, slices 6, 7, white circles,5,second
from top). These observations were confirmed by ANOVA, which
revealed a significant main effect of task ( p , 0.05) and a
significant interaction effect of hemisphere 3 task 3 slice ( p ,
Figure 3. Individual subject activation data overlaid on T1-weighted coronal anatomical images. Slice 1 is the most anterior. In EYES and MOUTH,
focal activation was observed in the right lateral cortex of the two most anterior slices (framed by white squares). No activation was seen in the same
regions for the other tasks. Activation in all tasks (framed by white circles) was seen in another region of right lateral cortex posterior and inferior to that
seen to EYES and MOUTH. In this and Figure 4, the right hemisphere appears on the lef t side of the image, and the red to yellow color scale indicates
lower to higher t values of activation. In this and Figure 4, activation data have been scaled, translated, and interpolated to fit their anatomical
counterparts.
2192 J. Neurosci., March 15, 1998, 18(6):2188–2199 Puce et al. • Temporal Lobe Activation to Moving Eyes and Mouths
0.01). The IPS contributed 59, 45, and 70% of the activated voxels
in EYES, MOUTH, and RADIAL, respectively. EYES prefer-
entially activated the left anterior IPS, whereas RADIAL acti-
vated the posterior IPS in both hemispheres (Fig. 4, white circles).
Statistical comparison of the EYES versus MOUTH task re-
vealed only a main effect for slice ( p , 0.05), confirming that
more activation occurred in the anterior slices. Greater activation
occurred to EYES and MOUTH than to SIMULATED EYES
and SIMULATED MOUTH in the anterior slices (task, p ,
0.05; slice, p , 0.01, hemisphere 3 task 3 slice, p , 0.05). A
comparison of RADIAL, SIMULATED EYES, and SIMU-
LATED MOUTH revealed greater activation to RADIAL (task,
p , 0.01; hemisphere 3 task 3 slice, p , 0.01).
Activation in the ventromedial region
Strong posterior activation occurred in slices 4–7 for the RA-
DIAL task (slice, p , 0.01; task, p , 0.01), whereas EYES and
MOUTH elicited negligible activation (Fig. 5, second from bot-
tom). The collateral sulcus and the lingual gyrus combined pro-
duced 81% of the activation in this region.
Activation in the ventral region
The ventral region produced the fewest number of activated
voxels of the four regions, with the greatest concentration occur-
ring in slices 3–5 (slice, p , 0.05) but with no significant differ-
ences among RADIAL, EYES, and MOUTH (Fig. 5, bottom).
DISCUSSION
The major results of this study indicate that a region of the
temporal lobe centered in the STS is activated when subjects view
a face in which the eyes or mouth are moving (Figs. 7, 8). The
active region comprises the posterior portion of the straight
segment of the STS (Fig. 7). These activations were not attribut-
able to movement per se. Nonfacial movement in the same part of
Figure 4. Individual subject activation data for EYES (top) and RADIAL (bottom) overlaid on T1-weighted anatomical images. A, Coronal slices 1–7.
Slice 1 is the most anterior. A region of activation in the right lateral cortex is seen in slices 1–3 to EYES but not to RADIAL (white squares). Extensive
activation of lateral cortex bilaterally occurs in slices 4–7 for both EYES and RADIAL. Activation in the IPS (white circles) was also seen to EYES
anteriorly in slices 1 and 2 and posteriorly to RADIAL in slices 6 and 7. B, Oblique axial slices (1–7 ) for the same subject and tasks. Slice 1 is the most
ventral. Activation to EYES (white squares) but not to RADIAL is seen in slices 5 and 7,asinA.
Puce et al. • Temporal Lobe Activation to Moving Eyes and Mouths J. Neurosci., March 15, 1998, 18(6):2188–2199 2193
Figure 5. Voxel counts as a function of hemisphere (R, right; L, left) and slice for each region in 11 subjects. Lateral (top), dorsomedial (second from
top), ventromedial (second from bottom), and ventral (bottom) for EYES ( gray histograms), MOUTH (white histograms) and RADIAL (black
histograms). Slice 1 is the most anterior, and slice 7 is the most posterior. EYES elicited more activation in slices 1–3 than the other two tasks, whereas
RADIAL elicited the most prominent activation in slices 4–7 in the left hemisphere. In the dorsomedial region, the most prominent activation was
elicited to EYES in slices 1 and 2 of the left hemisphere and to RADIAL in slices 5–7 of both hemispheres. In the ventromedial region, RADIAL elicited
the most prominent activation in slices 4–7 of both hemispheres. The least activation was seen in the ventral region and was not different across tasks.
2194 J. Neurosci., March 15, 1998, 18(6):2188–2199 Puce et al. • Temporal Lobe Activation to Moving Eyes and Mouths
Figure 6. Voxel counts as a function of hemisphere and anatomical structure for the lateral region for EYES ( gray histograms), MOUTH (white
histograms), and RADIAL (black histograms) in 11 subjects. In the right hemisphere, EYES produced the most activation in the STS, whereas in the
left hemisphere the most activation occurred in the PTOF and LOS to radial. Syl, Sylvian fissure; STG, superior temporal gyrus; STS, superior temporal
sulcus; MTG, middle temporal gyrus; ITS, inferior temporal sulcus; ITG, inferior temporal gyrus; PTOF, parieto-temporo-occipital fossa; LOS, lateral
occipital sulcus; MOG, middle occipital gyrus.
Table 1. Activation centroids in Talairach coordinates (x, y, z) and SEM
Activation centroids
Right hemisphere Left hemisphere
x SEM y SEM z SEM x SEM y SEM z SEM
Coronal study (n 5 11)
Anterior lateral cortex
Eyes 49 2 248 1 5 2 247 1 252 1 6 2
Mouths 53 3 249 2 5 2 248 1 249 3 5 2
Posterior lateral cortex
Eyes 42 2 270 2 222 240 1 270 1 1 2
Mouths 38 3 265 4 222 230 9 273 2 222
Radial 43 3 272 2 1 2 241 1 272 2 1 2
STS 1 ITS
Eyes 49 2 249 2 3 2 246 1 253 1 5 2
Mouths 50 3 249 2 3 3 247 1 250 3 2 3
PTOF 1 LOS
Eyes 42 2 270 2 222 244 3 268 2 268
Mouth 40 3 270 3 212 239 3 271 4 1 2
Radial 39 2 272 2 212 241 2 271 2 2 2
Simulated eyes (n 5 8) 42 3 265 2 0 2 240 3 267 4 2 2
Simulated mouth (n 5 8) 40 3 271 4 221 240 3 271 4 211
Axial Study (n 5 6)
STS 1 ITS
Eyes 47 3 253 5 7 2 249 1 248 4 3 3
Mouths 45 6 257 6 7 4 248 2 255 2 2 3
PTOF 1 LOS
Eyes 39 6 272 7 213 240 8 264 11 213
Mouth 36 4 271 5 212 237 8 272 15 222
Radial 43 3 269 3 254 233 1 273 6 230
Anterior lateral cortex and posterior lateral cortex refer to unrestricted activation centroids, whereas STS 1 ITS and PTOF 1 LOS refer to restricted activation
centroids.
Puce et al. • Temporal Lobe Activation to Moving Eyes and Mouths J. Neurosci., March 15, 1998, 18(6):2188–2199 2195
the visual field as occupied by the eyes or mouth, or movement of
a radial background, activated an area that was ventral and
posterior to this region (the PTOF and LOS), corresponding to
area MT/V5. As can be seen in Figure 9, the activation centroids
in MT/V5 in the present study correspond closely to those re-
ported in other studies of nonbiological motion.
These results suggest that a discrete region of cortex centered
in the STS is involved in the perception of eye and mouth
movement. That such regions may be lateralized is suggested by
Campbell et al. (1986), who reported that a prosopagnosic patient
with a right occipitotemporal lesion was deficient in determining
direction of gaze but could lip-read normally, whereas a patient
with a left occipitotemporal lesion was alexic and could not
lip-read but could recognize familiar faces and determine direc-
tion of gaze normally. We found that changes in direction of gaze
activated the right STS more than the left. However, this differ-
ence did not reach statistical significance ( p 5 0.10). Calvert et al.
(1997) reported that silent lip-reading of words activated a bilat-
eral region of the superior temporal gyrus (presumably including
cortex within the STS) 2.2–3.0 cm anterior to the bilateral regions
described here (Fig. 9). The STS may also participate in the
perception of biological motion. When subjects viewed point-light
simulations of hand action, body movement, object motion, and
random motion, a region of the STS was activated by hand and
body movement but not by the other movement tasks (Bonda et
al., 1996). Their activations were 0.5–1.5 cm posterior and supe-
rior to the region activated in our study (Fig. 9). In positron
emission tomographic studies, Rizzolatti et al. (1996) found that
the observation of grasping movements activated the left middle
temporal gyrus and STS centered at y 5236 (Rizzolatti et al.,
1996) and at y 5221 (Grafton et al., 1996). This region is
considerably anterior (Fig. 9) to the region activated by hand
Figure 7. Activation centroids to EYES, MOUTH, and RADIAL. Two centroids are shown: anteriorly for the STS/ITS and posteriorly for the
PTOF/LOS for coronal and axial fMRI studies. A, Right hemisphere. B, Left hemisphere. Centroids are superimposed on a sagittal view of a
representative brain, 44 mm from the midline. In this and Figure 9, coordinates in the y-axis (horizontal ) and z-axis (vertical ) are in the system of
Talairach and Tournoux (1988), and the anterior commissure–posterior commissure line (horizontal line) and the anterior commissure at y 5 0(vertical
line) are shown. The SEs around the centers of activation (x, y, z) for the coronal studies were EYES anterior (left,1,1,2;right, 1, 1, 2), MOUTH anterior
(left,1,3,2;right, 3, 2, 2), EYES posterior (left,1,1,2;right, 2, 2, 2), MOUTH posterior (left,9,2,2;right, 3, 4, 2), and RADIAL posterior (left 1, 2,
1; right 2, 2, 2).
Figure 8. Time course of activation of the right STS for a single 12 sec
cycle averaged over all cycles in each task for 10 subjects. Percent signal
change (%DS/S) is shown on the y-axis for EYES, MOUTH, and RA-
DIAL. For the first 6 sec of the cycle the relevant stimulus is in motion,
whereas for the second half of the cycle it is stationary. The right STS is
activated by EYES (solid line) and MOUTH (broken line) but not by
RADIAL (dotted line).
2196 J. Neurosci., March 15, 1998, 18(6):2188–2199 Puce et al. • Temporal Lobe Activation to Moving Eyes and Mouths
action by Bonda et al. (1996) for reasons that are unclear. How-
ever, taken together these studies strongly implicate the human
STS and adjacent cortex in the perception of facial and body
movements of other individuals.
In previous fMRI studies, we reported two regions activated by
faces (Puce et al., 1995, 1996). The major activation occurred in
ventral occipitotemporal cortex, primarily within the fusiform
gyrus. It is notable that this region showed negligible activation in
the present study, presumably because of the continuous presence
of a face during each task. We also reported activation of lateral
cortex by faces, including activation within the PTOF and in and
near the STS (Fig. 9) (Puce et al., 1995, their Fig. 7). The
activation of these same regions in the present study by moving
eyes and mouths suggests a functional dissociation between the
ventral and lateral regions activated by faces.
Further support for a functional dissociation in face processing
is derived from differences we have observed between intracra-
nial and scalp ERP recordings. An intracranial ERP (N200),
recorded primarily from the fusiform gyrus (Allison et al.,
1994a,c), is evoked predominantly by faces and to a lesser extent
by nonface stimuli. N200 is larger to faces than to eyes and other
face parts viewed in isolation (Allison et al., 1994b). A similar
face-specific ERP (N170) can be recorded from the lateral tem-
poral scalp. N170 is larger to eyes viewed in isolation than to
faces, leading Bentin et al. (1996) to conclude that N170 reflects
activity in a different eye-sensitive region of cortex. The neural
generator of the scalp-recorded N170; hence, the location of the
eye-sensitive region is unknown. Bentin et al. (1996) concluded
on the basis of its location and orientation that the fusiform gyrus
was an unlikely generator of N170 and instead proposed the
occipitotemporal sulcus (OTS). The present study shows that
moving eyes primarily activate the STS and not the OTS. The
STS and adjacent surface cortex is favorably located for the
generation of N170, but this issue is unresolved and complicated
by the fact that Bentin et al. (1996) used static views of faces and
isolated eyes. It may be that eye movement is necessary to engage
the STS. However, combined with the present study, these results
suggest that there are two separate systems participating in the
processing of information relating to faces: a ventral region in-
volved with faces and a lateral region concerned with face com-
Figure 9. Centroids of activation (STS/ITS for EYES and MOUTH and PTOF/LOS for RADIAL) in this study compared with centroids of activation
for the perception of hand action or body movement (Bonda et al., 1996), hand grasping (Rizzolatti et al., 1996; Grafton et al., 1996), silent lip-reading
of numbers (Calvert et al., 1997), nonanimate movement (Watson et al., 1993; McCarthy et al., 1995; Tootell et al., 1995), and the perception of static
faces (Puce et al., 1995, 1996). A, Right hemisphere. B, Left hemisphere. Centroids of activation are superimposed on two sagittal views of a
representative brain.
Puce et al. • Temporal Lobe Activation to Moving Eyes and Mouths J. Neurosci., March 15, 1998, 18(6):2188–2199 2197
ponents, or the movement of face components. The former sys-
tem would provide information necessary for the recognition of
facial identity, whereas the latter would provide information
necessary for the successful interpretation of facial gesture.
Direction of gaze is thought to be an important facial gesture.
In monkeys, gaze direction is an important component of facial
expressions, particularly those related to dominance and submis-
sion (Hinde and Rowell, 1962; Mendelson et al., 1982; Perrett et
al., 1990; Perrett and Mistlin, 1990; Brothers and Ring, 1993).
Given the importance of these facial signals, it is not surprising
that some neurons in monkey temporal visual cortex (primarily in
the STS) are sensitive to eye and head direction (Hasselmo et al.,
1989; Perrett et al., 1985, 1992). These neurons may play a role in
what Perrett et al. (1992) call “social attention,” or cells that
signal the direction of another individual’s attention. In the
monkey temporal lobe, cells responsive to direction of gaze tend
to be located within the STS, whereas cells responsive to face
identity tend to be located in adjacent inferior temporal cortex
(Yamane et al., 1988; Hasselmo et al., 1989; Perrett et al., 1990,
1992). In humans and monkeys, direction of gaze provides infor-
mation in social situations, expresses intimacy, and allows infer-
ences about the direction of attention of another individual
(Kleinke 1986; Perrett and Mistlin, 1990). We suggest that the
superior temporal region activated by moving eyes (Fig. 9) is
involved in the perception of direction of gaze.
This same region of superior temporal cortex also responded to
mouth movement (Fig. 9). In monkeys, mouth movements are
also an important component of facial gesture. For example,
mouth opening and teeth baring are components of threat or fear
for many species, whereas “smiling” denotes submission or a
positive affect (Chevalier-Skolnikoff, 1973; Redican, 1982). It is
possible that in humans the STS and surrounding cortex are
involved in the interpretation of facial gestures involving the
mouth. We have interpreted our results to mean that the activated
portion of the STS is preferentially involved in the perception of
dynamic facial movement. Although plausible, this interpretation
remains unproven, because (1) we have not studied activation
evoked by eye and mouth movement compared with static views
of direction of gaze or mouth configuration; (2) we have not
studied the possible activation of this region by complex but
inanimate objects, e.g., a swinging pendulum; and (3) the respon-
siveness of monkey STS cells to moving eyes and mouths has not
yet been reported.
Aside from the activations already discussed, the only other
substantial activation occurred bilaterally in the IPS. The IPS is
a large structure and likely functionally diverse. For example, it is
activated by viewing gratings (Gulya´s and Roland, 1995), by
viewing letter strings and faces (Puce et al., 1996), and by reading
music (Sergent et al., 1992b). The functional significance of IPS
activation in this study is unknown. However, the radial task
primarily activated the posterior portion of the IPS, suggesting
that this region may be a component of the dorsal visual pathway
dealing with movement and spatial location.
Finally, we note that EYES activated area MT/V5 in the right
hemisphere only slightly less than did RADIAL (Fig. 6), although
the radial background moved continuously during the EYES task.
Thus, the continuously moving radial background did not control
movement per se in the EYES task in MT/V5. We consider four
possible explanations. First, EYES may have activated a popula-
tion of MT/V5 cells responsive to more central portions of the
visual field, in addition to the cells responsive to the peripheral
radial background. This explanation does not, however, account
for the relative lack of MT/V5 activation by MOUTH, SIMU-
LATED EYES, and SIMULATED MOUTH, which also in-
cluded movements in the central portions of the visual field.
Second, MT/V5 may be more sensitive to coherent motion, such
as that produced by conjugate eye movements, than by the non-
coherent motion of the other tasks. Third, activation of MT/V5
above that elicited by the moving radial background may repre-
sent attentional modulation (O’Craven et al., 1997). Moving eyes
may be a highly salient stimulus and thus may engage attention
more than the other tasks. Last, MT/V5, or a subregion of it, may
in fact be sensitive to moving eyes. Single-unit recordings
in monkey MT/MST have determined its responsiveness to mov-
ing slits, dots, optical flow, and other kinds of nonbiological
movement (Maunsell and Van Essen, 1983; Desimone and
Ungerleider, 1986; Tanaka and Saito, 1989; Lagae et al., 1994). A
portion of STS receives input from MST (Baizer et al., 1991). If
the human STS has a similar connectivity, the region of STS
described here may receive input from a region of MT/V5 that
itself is responsive to eye movement. Whether a population of
cells preferentially responsive to movements of animate objects is
present in monkey MT/MST, and whether such results could
explain the activation of MT/V5 by eye movements in this study,
remain to be determined.
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