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The Journal of Neuroscience, March 15, 1998, 18(6):2188-2199
Temporal Cortex Activation in Humans Viewing Eye and Mouth
Movements
Aina
Puce1, 2,
Truett
Allison1, 3,
Shlomo
Bentin5,
John C.
Gore4, and
Gregory
McCarthy1, 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
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ABSTRACT |
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 subjects 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 assessed 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 activation by moving eyes and mouths was
distinct from that elicited by the moving radial background, which
primarily activated 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 preferentially 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 movement; temporal lobe; superior temporal sulcus; gaze direction
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INTRODUCTION |
Face recognition and analysis of
facial expression form an important 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). Activation
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 neurons 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 temporal
lobe are sensitive to face parts. For example, some patients with
temporal lobe lesions are deficient in determining gaze direction,
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).
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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 by the Human Investigation Committee of Yale
University School of Medicine. Each subject participated in three to
five imaging sessions.
Experimental tasks.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.
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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.
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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 center. Thus, the
subject viewed alternating periods of eye movements and fixation on an
otherwise stationary face. The purpose of this manipulation 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
contribution 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
movements. 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 continuously 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
checkerboards, 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 SIMULATED 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 × 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 positioned
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
echoplanar sequence [repetition time (TR), 1500 msec; echo time
(TE), 45 msec;  = 60°; number of excitations (NEX), 1; voxel size,
3.2 × 3.2 × 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 sequence [TR, 500 msec; TE, 11 msec; NEX,
2; field of view (FOV), 24 cm; slice thickness, 7 mm; skip factor, 0;
imaging matrix, 128 × 64]. Whole-brain axial images were
acquired using a spoiled gradient-recalled acquisition in a steady
state sequence (TR, 25 msec; TE, 5 msec; = 45°; NEX, 2; FOV, 24 cm; slice thickness, 2 mm; skip factor, 0; imaging matrix, 256 × 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
movement 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 systematic 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 performed on uninterpolated activation
images. The Talairach coordinates (Talairach and Tournoux, 1988) of
activated voxels were then determined. Finally, the anatomical
locations of activated voxels were determined 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 intraparietal 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 comprised 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.
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Figure 2.
Four anatomical regions for classification of
activated voxels (lateral, dorsomedial, ventromedial, and ventral) and
their borders are outlined on the left 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.
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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.
Four task comparisons were computed: (1) EYES, MOUTH, and RADIAL; (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 anatomical regions.
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RESULTS |
Figure 3 presents results from a
single subject for five experimental 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.
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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 left 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.
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Figure 4 presents results from another
individual for EYES and RADIAL from coronal and axial imaging sessions.
Activation 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).
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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, as in A.
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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 × task × slice).
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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.
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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 = 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.
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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.
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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 temporal 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 calculated 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
correspondence 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.
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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 = 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).
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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.
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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 (% S/S) is shown on
the y-axis for EYES, MOUTH, and RADIAL. 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).
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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 produced 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 anterior 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 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 occurred 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 hemispheres
(Fig. 7, Table 1), indicating that the coronal study encompassed 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 × task × slice (p < 0.01). The IPS contributed 59, 45, and 70% of the activated voxels in
EYES, MOUTH, and RADIAL, respectively. EYES preferentially activated
the left anterior IPS, whereas RADIAL activated the posterior IPS in
both hemispheres (Fig. 4, white circles).
Statistical comparison of the EYES versus MOUTH task revealed 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 × task × slice, p < 0.05). A comparison of RADIAL, SIMULATED
EYES, and SIMULATED MOUTH revealed greater activation to RADIAL (task,
p < 0.01; hemisphere × task × slice,
p < 0.01).
Activation in the ventromedial region
Strong posterior activation occurred in slices 4-7 for the RADIAL
task (slice, p < 0.01; task, p < 0.01), whereas EYES and MOUTH elicited negligible activation (Fig. 5,
second from bottom). The collateral sulcus and
the lingual gyrus combined produced 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 occurring in
slices 3-5 (slice, p < 0.05) but with no significant
differences 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 attributable to movement per
se. Nonfacial movement in the same part of 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 reported in other studies
of nonbiological motion.
View larger version (72K):
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|
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.
|
|
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 direction of gaze normally. We found that changes
in direction of gaze activated the right STS more than the left.
However, this difference did not reach statistical significance
(p = 0.10). Calvert et al. (1997) reported that
silent lip-reading of words activated a bilateral 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
superior 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 =  36 (Rizzolatti et al.,
1996) and at y = 21 (Grafton et al., 1996). This
region is considerably anterior (Fig. 9) to the region activated by
hand action by Bonda et al. (1996) for reasons that are unclear.
However, 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 intracranial 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 temporal 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 involved with faces and a lateral
region concerned with face components, or the movement of face
components. The former system 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 submission (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 information in social situations, expresses
intimacy, and allows inferences 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 responsiveness 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 (Gulyás 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 population 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, SIMULATED EYES, and SIMULATED MOUTH, which also included
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 noncoherent motion of the other
tasks. Third, activation of MT/V5 above that elicited by the moving
radial background may represent 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 moving
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.
| |
FOOTNOTES |
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
Laboratory 116B1, Veterans Administration Medical Center, West Haven,
CT 06516.
| |
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M. F. Mason, J. F. Banfield, and C. N. Macrae
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M. Grossman, P. Koenig, G. Glosser, C. DeVita, P. Moore, J. Rhee, J. Detre, D. Alsop, and J. Gee
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Top
Abstract
Introduction
