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Volume 16, Number 16,
Issue of August 15, 1996
pp. 5205-5215
Copyright ©1996 Society for Neuroscience
Differential Sensitivity of Human Visual Cortex to Faces,
Letterstrings, and Textures: A Functional Magnetic Resonance Imaging
Study
Aina Puce1, 2,
Truett Allison1, 3,
Maryam Asgari1,
John C. Gore4, and
Gregory McCarthy1, 2, 3
1 Neuropsychology Laboratory, Veterans Affairs Medical
Center, West Haven, Connecticut 06516, and Departments of
2 Surgery (Neurosurgery), 3 Neurology, and
4 Diagnostic Radiology, Yale University School of Medicine,
New Haven, Connecticut 06510
 ABSTRACT
- INTRODUCTION
- MATERIALS AND METHODS
- RESULTS
- DISCUSSION
- FOOTNOTES
- REFERENCES
ABSTRACT 
Twelve normal subjects viewed alternating sequences of unfamiliar
faces, unpronounceable nonword letterstrings, and textures while
echoplanar functional magnetic resonance images were acquired in seven
slices extending from the posterior margin of the splenium to near the
occipital pole. These stimuli were chosen to elicit initial
category-specific processing in extrastriate cortex while minimizing
semantic processing. Overall, faces evoked more activation than did
letterstrings. Comparing hemispheres, faces evoked greater activation
in the right than the left hemisphere, whereas letterstrings evoked
greater activation in the left than the right hemisphere. Faces
primarily activated the fusiform gyrus bilaterally, and also activated
the right occipitotemporal and inferior occipital sulci and a region of
lateral cortex centered in the middle temporal gyrus. Letterstrings
primarily activated the left occipitotemporal and inferior occipital
sulci. Textures primarily activated portions of the collateral sulcus.
In the left hemisphere, 9 of the 12 subjects showed a characteristic
pattern in which faces activated a discrete region of the lateral
fusiform gyrus, whereas letterstrings activated a nearby region of
cortex within the occipitotemporal and inferior occipital sulci. These
results suggest that different regions of ventral extrastriate cortex
are specialized for processing the perceptual features of faces and
letterstrings, and that these regions are intermediate between earlier
processing in striate and peristriate cortex, and later lexical,
semantic, and associative processing in downstream cortical
regions.
Key words:
extrastriate cortex;
face perception;
functional
MRI;
fusiform gyrus;
ventral visual pathway;
word perception
INTRODUCTION
Physiological studies in Old World monkeys reveal
that particular attributes and categories of visual stimuli are
processed within specialized regions of extrastriate cortex. Regions
engaged in processing of color and form (for review, see Maunsell and
Newsome, 1987 ), faces (Gross, 1992; Perrett et al., 1992), facial
expression (for review, see Rolls, 1992), motion (for review, see
Albright, 1993), and ``biological motion'' (Oram and Perrett, 1994)
have been described. This processing occurs within two separate but
interconnected pathways, a ventral pathway dealing with object
recognition, and a dorsal pathway dealing with motion, spatial
relationships, and visually guided movement (Ungerleider and Mishkin,
1982; Goodale and Milner, 1992; Ungerleider, 1995) (however, see
Merigan and Maunsell, 1993; Zeki, 1993).
Knowledge of human visual processes is limited and has come primarily
from psychophysical studies in normal subjects and from study of
patients with naturally occurring lesions. Additional information has
been obtained from field potentials recorded from chronically implanted
electrodes used to localize epileptogenic foci in human visual cortex
(Allison et al., 1993, 1994a,b; Nobre et al., 1994). These studies
suggest a considerable degree of modularity in the initial processing
of some categories of visual stimuli. For example, Allison et al.
(1994a) found that discrete portions of the fusiform and inferior
temporal gyri were activated by faces but not by equiluminant scrambled
faces or by objects such as cars or butterflies. At these sites, faces
evoked a large field potential with a mean peak latency of 190 msec
(N200). Letterstrings evoked a similar N200 (Nobre et al., 1994), but
letterstring sites were less common than face sites. In some patients,
Arabic numbers also evoked an N200 from the same region (Allison et
al., 1994b). Visual cortex located posterio-medial to the face,
letterstring, and numberstring areas was preferentially activated by
colored checkerboards (Allison et al., 1993). These results suggest
that the human ventral object-recognition system contains localized
subsystems for the perception of colors, faces, and words.
Although many response properties of face and letterstring N200s remain
to be determined, evidence indicates that this activity reflects an
early, automatic stage of category-specific processing. For example,
letterstring N200s were insensitive to word type (e.g., concrete nouns
or unpronounceable nonwords), whereas longer-latency potentials
recorded from anterior regions of the inferior temporal lobe were
highly sensitive to word type (Nobre et al., 1994). Face N200s did not
habituate on repeated presentation of the same face, suggesting that
this activity reflected mandatory processing of face information
(Allison et al., 1995).
The spatial sampling afforded by intracranial electrodes is limited.
Puce et al. (1995a) used functional magnetic resonance imaging (fMRI)
to examine the extent of extrastriate cortex activated by faces.
Although the activated portions of inferior extrastriate cortex in
normal volunteers corresponded well with the regions that generated
face N200s in patients, the extent to which these regions were
activated specifically by faces compared with other objects
or letterstrings was not determined. In the present study, we examined
this issue by comparing fMRI activation evoked by faces to that evoked
by letterstrings. To minimize postperceptual semantic processing,
stimuli consisted of unfamiliar faces and unpronounceable nonword
letterstrings. To maximize the difference in activations
evoked by these stimulus categories, we used an alternation paradigm
(McCarthy et al., 1995; Puce et al., 1995a) in which subjects were
exposed to a repeating pattern of faces and letterstrings. To identify
cortical regions activated by both faces and letterstrings,
a nonobject stimulus category, textures, was alternated in separate
runs with faces and with letterstrings.
MATERIALS AND METHODS
Subjects. Twelve normal right-handed subjects
(Edinburgh Handedness Inventory range 70-100) (Oldfield, 1970) without
a previous neurological or psychiatric history participated in this
study. Age ranged from 19 to 34 years (mean, 26 years), and there were
seven males. The experimental protocol was approved by the Human
Investigation Committee of Yale University School of Medicine, and
informed consent was obtained from each subject.
Activation tasks. Visual stimuli were delivered
under computer control to an active matrix projection panel (Sharp
Instruments, Mahwah, NJ), the images for which were projected onto a
translucent screen mounted at the end of the patient gurney. The
subject viewed stimuli on the screen through a mirror mounted on the
head coil. All stimuli were presented on a dark background and
subtended horizontal and vertical visual angles of 4.3°.
Three stimulus types were viewed as gray-scale images (Fig.
1): (1) Digitally scanned faces from college yearbook
photographs of individuals without eyeglasses or facial hair were
presented. The photographs were full face and consisted of equal
numbers of males and females. (2) Letterstrings consisted of
five black consonants presented on a gray square that was the same size
as faces. (3) Textures were abstract designs. Luminance and
contrast of the stimuli were standardized using image processing
software. The average luminance of all three stimulus categories was
the same, as was the average contrast for the face and texture
stimuli.
Fig. 1.
Examples of stimuli (unfamiliar faces,
unpronounceable nonwords, and textures) used in this study. In
experiment 1, faces were alternated with letterstrings. In experiment
2, textures were alternated with faces or letterstrings in separate
imaging runs. Ten stimuli in each category were presented in each 6.0 sec epoch, followed by 10 stimuli of another category.
[View Larger Version of this Image (77K GIF file)]
Experiment 1. The activation task consisted of the
alternating presentation of sets of faces and letterstrings (F and L,
respectively), each with 10 different stimuli per set as described
previously (Puce et al., 1995a). A single cycle of the activation task
(F-L) had a duration of 12 sec, and each imaging run consisted of 14 cycles. Each run was preceded by a 12 sec prestimulus period and
followed by a 13 sec poststimulus period, during which a white central
fixation cross was presented on a dark screen. The order of
presentation of faces and letterstrings was counterbalanced to yield
three imaging runs starting with faces (FLFL ... ) and three runs
starting with letterstrings (LFLF ... ). Subjects were instructed
to lie as still as possible and to concentrate on viewing the
stimuli.
Experiment 2. The same subjects were run in a second
imaging session in which a nonobject stimulus category, textures (T),
was alternated in separate runs with faces (F-T) and letterstrings
(L-T). Six runs were acquired for the F-T comparison, with three runs
starting with faces (FTFT ... ) and three runs starting with
textures (TFTF ... ). Similarly, six runs were acquired for the
L-T comparison, with three runs starting with letterstrings
(LTLT ... ) and three runs starting with textures (TLTL ...
).
MRI acquisition. A 1.5T MRI scanner (General Electric
Signa, Milwaukee, WI) with a standard quadrature head coil and
echoplanar capability (Instascan, ANMR Systems, Wilmington, MA) was
used. The subject's head was positioned along the canthomeatal line
and then immobilized using a vacuum cushion (Olympic, Seattle, WA) and
a forehead strap. Anatomical sagittal localizer scans were acquired
[T1 weighted: TR
(repetition time) = 500, TE (echo time) = 11, NEX
(excitations) = 1, FOV (field of vision) = 24 cm, slice thickness = 5 mm, skip factor = 2.5 mm; imaging matrix = 256 × 192]. Seven coronal slices beginning at the posterior edge of the
splenium (Fig. 2) were selected, which encompassed all
but the most anterior portion of the region studied
electrophysiologically (Allison et al., 1994b). Anatomical scans for
these seven slices were acquired using a
T1-weighted conventional sequence
(TR = 500, TE = 11, NEX = 2, FOV = 24 cm, slice thickness = 7 mm, skip
factor = 0, imaging matrix = 256 × 256) and echoplanar
sequence (TR = 3000, TE = 80, NEX = 4, FOV = 40 × 20 cm, slice thickness = 7 mm, skip factor = 0, imaging matrix = 128 × 64). At the
conclusion of experiment 1, axial images were acquired for all subjects
using an SPGR sequence (TR = 25, TE = 5,  = 45°, NEX = 2, FOV = 24 cm, slice thickness = 2 mm, skip factor = 0, imaging
matrix = 256 × 192). This whole brain image set was
reformatted to match the slice angles used for functional imaging. In
this way, activated voxels were represented in three dimensions and
transformed into Talairach coordinates (Talairach and Tournoux, 1988).
In addition, coronal magnetic resonance (MR) angiography images were
acquired using a sequence selected to emphasize venous flow
(TR = 45, TE = 7.7, = 40°, NEX = 2, FOV = 24 cm, flow compensation, slice
thickness = 2 mm, imaging matrix = 256 × 128).
Fig. 2.
Midline sagittal T1-weighted image of
the brain showing seven coronal slices. The center of the first slice
was located at the posterior margin of the splenium (indicated by the
first vertical black line). Examples of slices 1, 4, and 7 are shown below the sagittal image. The subject's head was
positioned using the canthomeatal line. In most subjects, this
corresponded to the line between the anterior and posterior commissures
(shown as black Xs). Average anterio-posterior locations of
slices 1-7 in Talairach coordinates were, respectively,
y =  42, 49, 56, 63, 70, 77, and 84. The
temporal lobe anterior to slice 1 could not be imaged reliably because
of susceptibility artifact from the ear canals.
[View Larger Version of this Image (118K GIF file)]
In both experiments, functional images were acquired using a gradient
echo echoplanar sequence (TR = 1500, TE = 45, = 60°, NEX = 1, FOV = 40 × 20 cm, slice thickness = 7 mm, skip factor = 0, imaging matrix = 128 × 64, voxel size = 3.2 × 3.2 × 7 mm). Each imaging run consisted of 128 images per slice
with a duration of 3 min 13 sec. Four additional excitations were
performed before each run to achieve steady-state transverse
magnetization.
The functional imaging runs were screened for movement and other
artifacts using center of mass calculations and by visual inspection of
the image series in an animated loop. Data from one subject in
experiment 2 were excluded because of head movement artifact. Analysis
of functional images was performed using t test mapping and
frequency analysis.
t test analysis. The three runs for each stimulus
alternation order were averaged resulting in two average runs of 128 images per slice for each experiment. For example, for each of the
seven slices of experiment 1, there was one average run for the F-L
alternation order and one average run for the L-F alternation order.
Three consecutive images for each stimulus type (F and L) were selected
from each of the 14 cycles within each average run, resulting in 42 samples for each stimulus type. An unpaired t test then was
performed on a voxel-by-voxel basis for these images. Because of the
lag associated with the functional activation signal, the selected
images were offset from the start and end of each stimulus type within
each cycle. For example, in experiment 1, the three images selected for
faces were those three consecutive images starting at 4.5 sec after the
onset of each face subcycle. Similarly, the three images selected for
letterstrings were those three consecutive images starting at 4.5 sec
after the onset of each letterstring subcycle. The image acquired 3.0 sec after the onset of either stimulus type was not included in the
analysis, because at that point in the cycle, the signal associated
with the current stimulus type was rising while the one associated with
the past stimulus type was declining. (Note that the example above
applies strictly for only the first of the seven slices, because the
acquisition of each was offset from each other within the 1500 msec
TR according to a 1-3-5-7-2-4-6 slice order. A
compensation was introduced in the images chosen for the t
test to account for this acquisition offset.)
The t-maps computed for each stimulus alternation order were
further analyzed using two methods: (1) A ``split-t'' map
(Puce et al., 1995b) was generated for each subject in which only those
voxels whose associated t values exceeded ± 1.5 for
both stimulus alternation orders were retained. These maps
were used as a comparison for the frequency analysis described below.
(2) An across-subjects t-map was computed, which combined
the average t-maps for all 12 subjects. Before averaging,
the t-maps for each subject were translated, stretched, and
rotated (independently in two dimensions) to align gyri and sulci to a
reference image set based on a representative subject. The alignment
factors were calculated using high-resolution anatomical images without
regard to the functional activations. Alignments were performed
separately for each hemisphere of each anatomical slice. To achieve a
good anatomical fit, it sometimes was necessary to offset the slice
order by one image in individual subjects to match the reference images
(e.g., slices 2-6 from one subject might be aligned with reference
slices 1-5). To accommodate these shifts, across-subjects average
t-maps were only created for reference slices 1-5.
Frequency analysis. The frequency analysis has been
described in detail (McCarthy et al., 1995; Puce et al., 1995a). First,
the 128 functional images obtained in each run for each slice were
transformed voxel by voxel into frequency and phase spectra using the
fast Fourier transform. These spectra were averaged across the three
runs, which made up a stimulus alternation order. This resulted in two
average frequency and phase spectra for each voxel in each slice for
each experiment; for example, one for the F-L alternation order, and
one for the L-F alternation order of experiment 1. Voxels were
retained for additional processing if they had a significant spectral
peak at 0.083 Hz, the frequency corresponding to the 12 sec stimulus
alternation period, in both alternation orders. The spectral
peak was considered significant if its power was 1.5 SD higher than the
mean power of the 20 adjacent power estimates.
A decision rule then was imposed in which the phase spectra were
examined for the voxels retained above. Voxels were defined as
activated only if the relative phases of these peaks changed by
180 ± 15° between stimulus alternation orders (e.g., F-L and
L-F). Voxels that survived this two-step procedure then were
superimposed on anatomical images. No other thresholds were used.
Figure 3 illustrates the frequency analysis method for
an individual subject in experiment 1. The activated voxels from both
the split t test (Fig. 3A) and frequency analysis
(Fig. 3B) are shown as overlays on the subject's anatomical
image. The frequency analysis (Fig. 3B) identified voxels
that were typically a subset of those found to be activated by the
t test analysis (Fig. 3A). The time courses for
activation in the left hemisphere (white circle in Fig.
3B) by faces (white) and letterstrings
(black) are shown in Figure 3, C and
D, respectively. Fourteen peaks can be observed in each time
course corresponding to the 14 cycles of stimulus alternation. This
oscillatory time course is reflected in Figure 3, E and
F, which show the frequency spectra for these two regions. A
180° phase shift (Fig. 3C,D) occurred between
the F-L and L-F alternation order. This is shown quantitatively in
Figure 3, G and H, where the power at 0.083 Hz
(corresponding to the 12 sec stimulus period) is plotted as a function
of phase. Two major peaks separated by 180° are evident in each plot.
For this subject, the activation evoked by faces (~2%) was greater
than that evoked by letterstrings (~1%). The time courses show a
clear temporal differentiation between the activation by faces of the
fusiform gyrus and the activation by letterstrings of the
occipitotemporal sulcus. For example, the solid line denoting the F-L
stimulus alternation order reached a peak midway in the 12 sec cycle
(denoted by vertical lines) in the fusiform gyrus,
corresponding to the offset of faces and the onset of letterstrings.
Conversely for the occipitotemporal sulcus, the solid line peaked at
the end of the 12 sec cycle at the offset of letterstrings. This
relationship is seen more easily in Figure 3, G and
H, where the phase of activation for the fusiform gyrus
precedes that of the occipitotemporal sulcus by 160° for the F-L
alternation order (compare solid lines). The reverse
relationship holds for the L-F stimulus alternation order in which the
occipitotemporal sulcus activation precedes that of the fusiform gyrus
by 200° (compare dotted lines).
Fig. 3.
Activation in a subject (slice 4) in experiment 1. A, Activated voxels identified by split-t test
for faces (white) and letterstrings (black) are
shown superimposed on a T1-weighted coronal anatomical
image. In this and subsequent figures, the right side of the brain is
represented on the left side of the image. In the left
hemisphere, a region at the border of the temporal and occipital lobes
(white circle) was activated by faces in the fusiform gyrus
and by letterstrings in the occipitotemporal sulcus. B,
Activated voxels for faces (white) and letterstrings
(black) identified by the frequency analysis are
superimposed on the anatomical image. C, Time course of
signal change for the voxels activated by faces (white
voxels in circle) from B for both task
orders. Percent signal change ( S/S) is
shown on the y-axis. Vertical bars indicate
onsets of the 14 successive stimulus cycles. The F-L and L-F
conditions are represented by the solid and dotted
lines, respectively. D, Time course of signal change
for the voxels activated by letterstrings (black
voxels in circle) from B for both task
orders. E, Power spectra corresponding to the activation
time course shown in C. Note the peak at the stimulus
alternation frequency (0.083 Hz). Power (in arbitrary units) is shown
on the y-axis. F, Power spectra corresponding to
D. G, Power at the stimulus alternation frequency
as a function of phase (in bins of 20°) for the activation time
course shown in C. Note that the change in stimulus order
produces a phase shift of 180°. H, Power at the stimulus
alternation frequency as a function of phase for the activation time
course shown in D.
[View Larger Version of this Image (72K GIF file)]
Anatomical localization. The Talairach coordinates
for each activated voxel were measured, and the anatomical locations
were determined by consensus of three of the authors. The
identification of anatomical landmarks was aided by imaging software
that permitted interactive reformatting of the thin slice,
high-resolution SPGR image series. This was particularly useful in
visualizing the full anterior-posterior courses of the collateral and
occipitotemporal sulci. Parcellation of occipitotemporal cortex was
straightforward with three exceptions: (1) The fusiform gyrus often is
divided by a longitudinal sulcus that can be confused with the
collateral sulcus in isolated coronal slices; (2) The transition
between temporal and occipital cortex is difficult to determine and is
somewhat arbitrary; (3) The location and extent of the transverse
collateral sulcus are difficult to assess. Ventral cortex lateral to
the collateral sulcus, posterior to the transverse collateral sulcus,
and medial to the inferior occipital sulcus will be referred to as
ventral occipital cortex. This region comprises portions of the third
and fourth occipital gyri of Duvernoy (1991) and ventral cortex of the
occipital pole.
RESULTS
To assess the consistency of activation, spatially normalized,
across-subjects t-maps were generated for the
face-letterstring condition (Fig. 4). Faces
(yellow-red) strongly activated the right ventral brain, primarily in
the fusiform gyrus (A-E). A large patch of
activation also was obtained in the right lateral cortex
(A-C). In the left ventral brain, faces
activated a more restricted portion of the fusiform gyrus
(C,D). Letterstrings (pink-purple) produced less
overall activation, which was largely restricted to the left
hemisphere. Activation by letterstrings also was observed in the left
intraparietal sulcus (C). Most prominent was the activation
of the occipitotemporal sulcus and posteriorly contiguous inferior
occipital sulcus (B-D) just lateral and superior
to the activation by faces of the fusiform gyrus. This pattern of
activation also was evident in the individual images of 9 of the 12 subjects. Figure 5 shows data from this region
(white circles) in six individuals. Activation evoked by
letterstrings occurred primarily in the occipitotemporal and inferior
occipital sulci. Letterstring activation of these sulci was restricted
in anterior-posterior extent, and was seen in only one slice in six
subjects and two adjacent slices in three subjects. Activation by faces
in the left hemisphere occurred in the fusiform gyrus and posteriorly
contiguous ventral occipital cortex.
Fig. 4.
Average t test data of 12 subjects in
the F-L condition overlaid on five averaged anatomical images.
A is the most anterior and E the most posterior
slice. Activation by faces is indicated by the
yellow-red color scale, and activation by
letterstrings is indicated by the pink-purple
color scale.
[View Larger Version of this Image (75K GIF file)]
Fig. 5.
Activation data from the ventral left hemisphere
(white circle) in six subjects. In the left
column, activated voxels identified by split-t test analysis
of the F-L condition are superimposed on corresponding anatomical
images. Faces activated a region of the lateral fusiform gyrus
(yellow), whereas letterstrings activated a region of
the occipitotemporal sulcus (pink). The right
column shows the corresponding activation time course
averaged over all alternation cycles for faces (yellow
lines) and letterstrings (pink lines). The
y-axis shows percent signal change with vertical ticks of
0.5%. Time (in sec) is shown on the x-axis.
[View Larger Version of this Image (71K GIF file)]
The time courses of the MR signal change from the encircled voxels
activated by each task are shown to the right of each image (Fig. 5).
To illustrate the timing of activation, each time course has been
averaged across all 14 cycles. The activation evoked by faces was
evident within 1.5-3.0 sec after their onset, and (in five of the six
subjects shown) peak activation occurred within 1.5-3.0 sec after
their offset (i.e., peak activation by faces occurred after the onset
of letterstrings). A complementary time course occurred for
letterstring activation. In these cortical regions, the magnitude of
the activation (signal change divided by mean signal) evoked by
letterstrings was 0.8%, whereas the magnitude of the activation evoked
by faces was 1.3%.
To evaluate the complete activation pattern, each activated voxel
identified by the frequency analysis was localized anatomically and
counted for all slices and subjects. Two percent of these voxels were
located in cerebellum, white matter, ventricles, or sinuses. Comparison
of activated voxels with the angiographic images revealed that few if
any voxels could be attributed to large-vessel activation. Remaining
voxels were located in cerebral cortex and are listed in Table
1. To simplify Table 1, structures for
which little or no activation was found (defined as three or fewer
total voxels for any stimulus category for both hemispheres) are not
listed. These structures are the cingulate gyrus, cuneus, inferior
temporal sulcus, inferior temporal gyrus, parieto-occipital fissure,
precuneus, superior occipital gyrus, superior parietal gyrus, superior
temporal gyrus, and supramarginal gyrus.
Table 1.
Location of activated
voxels
| Location |
Right
hemisphere
|
Left
hemisphere
|
| F(L) |
F(T) |
L(F) |
L(T) |
T(F) |
T(L) |
F(L) |
F(T) |
L(F) |
L(T) |
T(F) |
T(L) |
|
| Calcarine
sulcus |
7 |
0 |
0 |
3 |
0 |
3 |
2 |
2 |
0 |
1 |
0 |
4 |
| Lingual
gyrus |
10 |
2 |
2 |
2 |
1 |
14 |
21 |
0 |
0 |
2 |
0 |
3 |
| Collateral
sulcus |
0 |
2 |
0 |
2 |
14 |
28 |
18 |
2 |
2 |
2 |
12 |
17 |
| Transverse
collateral
sulcus |
2 |
0 |
0 |
0 |
0 |
1 |
2 |
0 |
0 |
0 |
5 |
6 |
| Fusiform
gyrus |
37 |
21 |
3 |
13 |
5 |
24 |
22 |
17 |
4 |
3 |
8 |
14 |
| Ventral
occipital
cortex |
11 |
1 |
0 |
4 |
0 |
3 |
10 |
2 |
4 |
8 |
0 |
2 |
| Occipitotemporal
sulcus |
7 |
12 |
4 |
3 |
0 |
0 |
4 |
5 |
10 |
4 |
3 |
1 |
| Inferior
occipital
sulcus |
7 |
8 |
0 |
4 |
3 |
2 |
0 |
4 |
10 |
9 |
1 |
3 |
| Middle
temporal
gyrus |
7 |
3 |
0 |
1 |
0 |
2 |
2 |
0 |
0 |
0 |
0 |
1 |
| Middle
occipital
gyrus |
9 |
6 |
1 |
0 |
1 |
2 |
8 |
8 |
0 |
1 |
3 |
0 |
| Superior
temporal
sulcus |
7 |
3 |
0 |
0 |
0 |
0 |
2 |
0 |
2 |
0 |
0 |
1 |
| Lateral
occipital
sulcus |
3 |
3 |
0 |
1 |
2 |
5 |
6 |
1 |
2 |
2 |
1 |
2 |
| Angular
gyrus |
0 |
0 |
0 |
0 |
0 |
1 |
0 |
0 |
8 |
0 |
0 |
2 |
| Intraparietal
sulcus |
3 |
0 |
12 |
6 |
1 |
2 |
1 |
1 |
23 |
3 |
4 |
2 |
|
|
Number of voxels activated by faces (F),
letterstrings (L), and textures (T) when compared with
another stimulus category indicated in parenthesis; e.g.,
F(L) indicates activation by faces compared
with letterstrings. Structures are listed in approximate
medial-lateral-superior order. Structures with little or no
activation (see text) are not included.
|
|
Active structures will be described in medial-to-lateral order.
The calcarine sulcus showed little activation to any stimulus category
(Table 1), suggesting that it was more or less equally activated by all
the stimuli and that a steady-state activation was achieved resulting
in no residual periodic signal. The lingual gyrus showed strong
activation by faces when alternated with letterstrings, particularly in
the left hemisphere. However, this activation was reduced to near zero
when faces alternated with textures. The logic of the experimental
design requires that brain regions specifically activated by a stimulus
category must be activated by that category regardless of which control
category was used. [For example, in the left fusiform gyrus, 22 voxels
were activated by faces alternated with letterstrings, whereas 17 voxels were activated by faces alternated with textures (Table 1),
indicating that the region responded specifically to faces. By
contrast, in the left lingual gyrus, 21 voxels were activated by faces
when alternated with letterstrings, whereas none was activated by faces
when alternated with textures, indicating that this structure was
equally responsive to textures and faces and, hence, that the
activation by faces was nonspecific.] These results indicate,
therefore, that the lingual gyrus was activated in common by both faces
and textures. Indeed, the fewest activated voxels were obtained when
these two categories alternated, again suggesting that a steady-state
activation was achieved. This conclusion is supported further by the
fact that textures strongly activated this region when alternated with
letterstrings, particularly in the right hemisphere.
The collateral sulcus was strongly and bilaterally activated by
textures irrespective of the control condition (Table 1), as
illustrated in Figure 6A, indicating that it
was activated specifically by textures. Less but specific activation by
textures of the left transverse collateral sulcus also was seen. Some
nonspecific activation by faces was seen in the collateral sulcus of
the left hemisphere.
Fig. 6.
Histograms of activated voxels (identified by
frequency analysis) in regions of left and right cortices.
A, Collateral sulcus. B, Fusiform gyrus.
C, Combined occipitotemporal and inferior occipital sulci.
D, Combined middle temporal and occipital gyri, and superior
temporal and lateral occipital sulci.
[View Larger Version of this Image (20K GIF file)]
The fusiform gyrus, just lateral to the collateral sulcus, showed a
different pattern of activation (Fig. 6B). It was activated
strongly by faces when alternated with letterstrings, consistent with
both the across-subjects and individual t-maps shown in
Figures 4 and 5. Activation by faces also was obtained when alternated
with textures, indicating that at least part of the activation by faces
was specific. On the other hand, the reduction in the magnitude of the
activation by faces when alternated with textures, and the activation
by textures when alternated with letterstrings, indicates that part of
the fusiform activation was nonspecific and common to faces and
textures. Face activation was bilateral, but greater in the right
hemisphere, consistent with the results of the across-subjects
t-maps (Fig. 4).
Little activation of the fusiform gyrus and more medial structures was
evoked by letterstrings, particularly when alternated with faces.
However, letterstrings strongly activated the left occipitotemporal and
inferior occipital sulci when alternated with either faces or textures,
indicating that this activation was letterstring specific. In contrast,
faces strongly activated the right occipitotemporal and
inferior occipital sulci when alternated with either letterstrings or
textures, again indicating a specific activation. This striking
interaction of stimulus category by hemisphere is illustrated in Figure
6C, in which the activation of these sulci has been combined
and summarized.
Activation of the lateral cortex, a continuous region comprising the
lateral occipital sulcus, middle occipital gyrus, middle temporal
gyrus, and superior temporal sulcus, is summarized in Figure
6D. Strong activation by faces was obtained when alternated
with letterstrings and when alternated with textures, indicating a
degree of face specificity. Like the activation of the occipitotemporal
and inferior occipital sulci, this activation was greater in the right
hemisphere. This result is consistent with the pattern of lateral
activation seen in the across-subjects t-map for the right
hemisphere in Figure 4. Little activation was obtained for either
textures or letterstrings in lateral cortex, but letterstrings showed a
small left dominant asymmetry (Fig. 6D).
Letterstrings also produced strong activation of the fundus of
the intraparietal sulcus and adjacent angular gyrus, primarily in the
left hemisphere (Table 1, Figs. 4, 5), but only when compared with
faces and not with textures, whereas textures also produced little
activation when compared with either faces or letterstrings (Figs.
3, 4, 5, Table 1). This anomalous pattern of activation is difficult to
interpret within the current experimental design.
There was little overlap (5 of 132 voxels) in the activation of ventral
cortex by both faces and letterstrings when alternated with textures.
Although this suggests specificity in activation, it is possible that
even these commonly activated voxels would show a strong preference for
either faces or letterstrings when these categories were alternated
directly. Another way to assess the relative specificity of activation
of a cortical region is to express it as a percentage of the total
activation across regions. Such an analysis for ventral cortex is shown
in Figure 7, and demonstrates that the collateral sulcus
is most strongly activated by textures, the fusiform gyrus by faces,
and the occipitotemporal and inferior occipital sulci by
letterstrings.
Fig. 7.
Activation in ventral extrastriate regions for
each stimulus category, expressed as a percentage of total activation
by that stimulus category. CoS, Collateral sulcus;
FG, fusiform gyrus; LG, lingual gyrus;
OTS/IOS, occipitotemporal and inferior occipital
sulci.
[View Larger Version of this Image (23K GIF file)]
The mean Talairach coordinates for the major regions of activation
described in Figures 4, 5, 6, 7 are given in Table 2. The
centers of activation did not change substantially for faces or
letterstrings across control conditions. However, the center of
activation for textures compared with faces was anterior to the center
of activation when compared with letterstrings, implying (together with
the results of Fig. 6A) that a posterior region of the
collateral sulcus is activated in common by textures and faces.
DISCUSSION
Activation by faces
When alternated with letterstrings, faces activated more cortex
than did letterstrings in both the right (115 vs 26 voxels) and left
(100 vs 67 voxels) hemispheres. A similar result was found for objects
compared with words in the positron emission tomography (PET) study of
Buckner et al. (1995). We have seen a similar difference in recordings
from extrastriate cortex in which face N200 sites are more numerous
than letterstring N200 sites. The reason for this difference is
unclear. It has been argued that faces are an important category of
objects for which rapid recognition requires specialized processing
(Young and Bruce, 1991; Newcombe et al., 1994). However, the same
argument could be asserted for reading. Perhaps in the absence of
competing stimuli, faces activate the general object-recognition system
in addition to face-specific regions. This subsystem may occupy more of
the ventral pathway than does a subsystem specialized for the
perception and grouping of a small set of characters.
Consistent with our previous fMRI study (Puce et al., 1995a), face
activation was concentrated within the fusiform gyrus (Figs. 4,7).
Previous PET studies have consistently shown face activation of this
region (Sergent et al., 1992; Haxby et al., 1994, 1995). Activation was
more extensive in the right hemisphere (Fig. 4), particularly when
faces alternated with letterstrings (Fig. 6B). These results
are consistent with the neuropsychology literature (for review, see
Rhodes, 1993) demonstrating a right hemisphere advantage for face
recognition and with previous PET (Horwitz et al., 1992; Haxby et al.,
1995) and scalp-recorded evoked potential (Bentin et al., 1996)
studies.
Malach et al. (1995) compared the fMRI activation produced by
objects (including faces) with the activation produced by textures.
They found that a region of lateral occipital cortex centered in the
fusiform gyrus was preferentially activated by objects even when the
spatial frequencies and contrast of the object stimuli matched those of
the texture stimuli. We also found that faces activated the fusiform
gyrus compared with textures (Fig. 6B), although the two
categories of stimuli were equated for luminance and contrast. These
results argue that the selective activation of regions of ventral
cortex by faces and other complex objects is not attributable to
between-category differences in luminance, contrast, spatial frequency,
or other elementary stimulus features.
Faces also specifically activated the right occipitotemporal and
inferior occipital sulci (Fig. 6C). This is consistent with
the evoked potential study of Bentin et al. (1996) in which faces and
eyes evoked a right hemisphere dominant N170 hypothesized to be
generated in the occipitotemporal sulcus. Finally, a continuous region
of lateral cortex comprising the middle temporal and occipital gyri,
and superior temporal and lateral occipital sulci, also was activated
specifically by faces (Figs. 4, 5, 6D), again predominantly
in the right hemisphere. The center of activation of this region was
similar to a right lateral region activated by faces (Puce et al.,
1995a), and was anterior and superior to the lateral occipital region
activated by objects (Malach et al., 1995).
Activation by letterstrings
Letterstrings activated more cortex in the left than in the right
hemisphere (67 vs 26 voxels). Activation was largely restricted to a
region of the occipitotemporal and inferior occipital sulci (Figs. 4,
5, 6C), the same region selectively activated by faces in
the right hemisphere (Fig. 6B). Intracranial recordings also
have revealed a left dominant asymmetry (our unpublished observations),
and evoked potential studies have shown that a letterstring N180 is
larger over the left than the right temporal scalp (Nobre and McCarthy,
1994), complementary to the distribution obtained by Bentin et al.
(1996) for faces. These results imply a left hemisphere advantage for
prelexical letterstring processing. However, activation by both faces
and letterstrings was bilateral; the interhemispheric differences were
of degree rather than kind.
This study was designed to engage only the early stages of word
processing; the results suggest that this objective was achieved.
Little activation and no letterstring-specific activation of left
superior and middle temporal cortex was seen, regions previously
activated in PET studies involving phonological processing or word
reading (Petersen et al., 1989; Démonet et al., 1992; Howard et
al., 1992; Price et al., 1994). Semantic processing of auditorily
presented words also activated regions of the temporal lobe distant
from ventral cortex (Petersen et al., 1988; Wise et al., 1991;
Démonet et al., 1992). The region activated by unpronounceable
nonwords here partially overlapped, but was inferior and lateral to a
medial extrastriate region activated by words and pronounceable
pseudowords (but not by false fonts or unpronounceable nonwords) in the
study of Petersen et al. (1990). These considerations indicate that the
unpronounceable nonword stimuli used here activated a prelexical,
presemantic stage of word-form processing in the reading system, and
that the lexical and semantic processes attendant on reading words
activate regions of the temporal lobe anterior and superior to ventral
occipitotemporal cortex. Nevertheless, systematic investigation of the
activation produced by decomposed letterstrings, unpronounceable
nonwords, and different word types will be required to better
differentiate the anatomical substrate of word-processing stages.
We predicted from electrophysiological studies (Allison et al., 1994a;
Nobre et al., 1994) that activation of ventral surface cortex by
letterstrings would be medial to that for faces. This prediction was
not confirmed, and indeed we found little activation of the fusiform
gyrus by letterstrings. There also was little activation of the
inferior temporal gyrus by letterstrings (or, indeed, by faces or
textures). In the study of Puce et al. (1995a), only 14% of the total
volume of activation by faces was in the inferior temporal gyrus. Only
15% of letterstring N200s, and 24% of face N200s, were recorded from
the inferior temporal gyrus (our unpublished observations). These
results indicate that the human inferior temporal gyrus is not a major
site of letterstring or face processing, unlike the inferior temporal
cortex in Old World monkeys, in which it is a major site of
face-specific neurons (Gross and Sergent, 1992; Perrett et al., 1992).
Just as striate cortex in monkeys is located mainly on the lateral
surface but ``migrates'' to ventromedial calcarine cortex in humans,
there may be a parallel migration of lateral face-sensitive regions in
monkeys to ventral cortex in humans.
Activation by textures
Although, textures were used primarily as a nonobject
control condition, some texture-specific activation was seen in the
collateral and transverse collateral sulci (Fig. 6A,
Table 1). The collateral sulcus contains portions of areas V2, ventral
V3 (VP), and V4 (Clarke and Miklossy, 1990; Clarke et al., 1995; Shipp
et al., 1995). It is activated by colors, shapes, and scrambled faces
(Corbetta et al., 1991; Clark et al., 1995; Puce et al., 1995a), but
not specifically by faces (Table 1) (see also Clark et al., 1995; Puce
et al., 1995a). Cortex in the transverse collateral sulcus also is
likely to be a part of the V4 color-form region. These two regions may
perform a stage of pattern recognition intermediate between initial
processing in V1 and V2 and category-specific processing in the
fusiform gyrus and more lateral extrastriate regions.
Specificity of activation by faces and letterstrings
The impetus for this study was our finding that faces and
letterstrings evoke field potentials in different sites on the ventral
brain surface (Allison et al., 1994a,b; Nobre et al., 1994). From
a broader perspective, it is known that different regions of visual
cortex process different visual stimulus attributes. The human ventral
pathway is involved in object perception, but whether there are
category-specific subsystems and if so, how many, is unclear. There are
advocates of a unitary system (Damasio et al., 1982; Critchley, 1986;
Biederman, 1987), two subsystems dealing with faces and words (Farah,
1990), two subsystems dealing with living and nonliving objects
(Sheridan and Humphreys, 1993; Newcombe et al., 1994), three subsystems
dealing with faces, words, and numbers (Allison et al., 1994b), and
nine subsystems dealing with living, nonliving, and symbolic categories
of objects (Konorski, 1967). These classifications are based largely on
case reports of patients with lesions producing specific visual
agnosias. Consistent with the present study, the lesion evidence
suggests that prosopagnosia (for review, see De Renzi et al., 1994) and
pure alexia (for review, see Damasio and Damasio, 1983) are forms of
visual agnosia preferentially involving lesions of the right and left
occipitotemporal regions, respectively. However, it is difficult to
compare lesion and imaging data. First, the deficit experienced by the
patient may be the result of damage in different parts of the pathway
along a perceptual-semantic continuum (Sergent and Signoret, 1992;
Sheridan and Humphreys, 1993). Second, most cases were described before
the advent of high-resolution imaging, making it difficult to identify
the specific location and extent of the lesion.
The PET and fMRI studies cited above, and many others, establish
that regions of extrastriate cortex are activated by objects, faces,
and letterstrings. Because the centers of activation differ, it could
be argued that such differences are evidence of anatomical segregation
of processing of different object categories. But such across-study
analysis is made difficult by differences in task requirements, control
stimuli, and statistical criteria for significant activation. We
attempted to deal with this problem by looking for differences in the
anatomical pattern of activation produced by two important categories
of stimuli, faces and letterstrings. This strategy allows detection of
cortical regions preferentially activated by one or the other stimulus
category, but does not completely answer the question of specificity.
It is possible that different categories of control stimuli would
activate different regions, or that the same region would be activated
equally by untested stimulus categories. Within these limitations,
however, we conclude that portions of extrastriate cortex are activated
specifically by faces and letterstrings. Two strategies might be useful
to further test the anatomical specificity of category-specific
processing: (1) Electrophysiological recordings could provide an
independent data set. In patients in whom face N200s have been
recorded, activation at the same sites should be obtained by fMRI. (2)
Portions of extrastriate cortex may participate to some degree in the
perception of any isolated stimulus. If the system were to
be challenged by concurrent object arrays, then faces or letterstrings
might activate only category-specific processing sites.
Studies to investigate both of these strategies now are underway.
FOOTNOTES
Received Feb. 27, 1996; revised May 28, 1996; accepted May 30, 1996.
This work was supported by the Department of Veterans Affairs and by
National Institutes of Mental Health Grant MH-05286. We thank A. Anderson, H. Sarofin, and S. Thomsen for assistance.
Correspondence should be addressed to Aina Puce, Neuropsychology
Laboratory 116B1, VA Medical Center, West Haven, CT
06516.
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MRI Scans
