fMRI of the Face-Processing Network in the Ventral
Temporal Lobe of Awake and Anesthetized Macaques
Shih-Pi Ku,1Andreas S. Tolias,2,3,4Nikos K. Logothetis,1,5and Jozien Goense1,*
1Max Planck Institute for Biological Cybernetics, Spemannstrasse 38, 72076, Tu ¨bingen, Germany
2Department of Neuroscience, Baylor College of Medicine, Houston, TX 77030, USA
3Michael E. DeBakey Veterans Affairs Medical Center, Houston, TX 77030, USA
4Department of Computational and Applied Mathematics, Rice University, Houston, TX 77005, USA
5Division of Imaging Science and Biomedical Engineering, University of Manchester, Manchester M13 9PT, UK
to processing of faces, which human imaging
studies localized in the superior temporal sulcus
(STS) and ventral temporal cortex. Studies in
macaque monkeys, in contrast, revealed face selec-
tivity predominantly in the STS. While this discrep-
ancy could result from a true species difference, it
may simply be the consequence of technical difficul-
ties in obtaining high-quality MR images from the
ventral temporal lobe. By using an optimized fMRI
protocol we here report face-selective areas in
ventral TE, the parahippocampal cortex, the entorhi-
macaques, in addition to those already known in the
STS. Notably, the face-selective activation of these
memory-related areas was observed although the
animals were passively viewing and it was preserved
even under anesthesia. These results point to simi-
larly extensive cortical networks for face processing
in humans and monkeys and highlight potential
homologs of the human fusiform face area.
Face recognition is a critically important cognitive ability for
primates, who often communicate with facial expressions and
gaze directions and use these cues to determine appropriate
behavioral responses. The importance of face processing for
social function is illustrated by the effects of prosopagnosia in
humans, which can be debilitating (Damasio et al., 1982).
Because of the importance of faces, primates have an extensive
network of brain areas devoted to face processing (Haxby et al.,
Functional magnetic resonance imaging (fMRI), lesion studies,
and electrophysiological studies in humans and monkeys have
discovered numerous face-processing areas. In electrophysio-
logical studies in macaques, neurons responding to facial
expressions and gaze direction were found in the superior
temporal sulcus (STS) (De Souza et al., 2005; Hasselmo et al.,
1989; Perrett et al., 1985), while identity is believed to be
encoded by neurons in the lateral and anterior ventral temporal
cortex (De Souza et al., 2005; Eifuku et al., 2004; Hasselmo
et al., 1989; Leopold et al., 2006). Monkey fMRI studies also
found multiple face-selective patches, although predominantly
in the STS (Bell et al., 2009; Hadj-Bouziane et al., 2008; Logothe-
tis et al., 1999; Pinsk et al., 2005; Tsao et al., 2003, 2008a). In
human fMRI studies, activation in the STS is also found, espe-
cially in response to facial expressions and dynamic aspects of
faces (Haxby et al., 2000), but the fusiform face area (FFA)
responds most strongly and with high specificity to faces and
is involved in detecting faces (Kanwisher and Yovel, 2006).
Comparative fMRI studies (Bell et al., 2009; Hadj-Bouziane
et al., 2008; Pinsk et al., 2005; Tsao et al., 2003, 2008a) show
correspondence between face-selective activation in monkeys
and humans, but substantial differences remain. Differences
are particularly pronounced in ventral temporal areas: for
instance, little face selectivity has been found in the ventral
temporal lobe in macaques and homologs of the FFA or occipital
face area (OFA) have not yet been identified.
To date, the degree of overall similarity in face-processing
areas between humans and macaques is not clear. Although it
is entirely possible that this lack of similarity between humans
and macaques is due to species differences, a factor that
complicates the question is that fMRI of the temporal lobe is
problematic because of the large susceptibility artifacts from
the ear canal. In addition, in humans the anterior temporal lobe
is often not included in the imaging volume, while the use of
surface coils in macaque fMRI can lead to low signal-to-noise
ratios (SNR) in ventral areas that are furthest away from the
coil. Thus, it is likely that the discrepancy arises because face-
selective areas have been missed in humans, macaques, or in
In our earlier work, we showed that by using high-field spin-
echo echo-planar imaging (SE-EPI), blood oxygen level-depen-
dent (BOLD) signals can be obtained with high sensitivity in
ventral temporal areas despite the presence of susceptibility
gradients from the ear canal and that SE-based fMRI out-
performs gradient echo (GE) fMRI in these regions (Goense
et al., 2008). Here, our goal was to map the face-selective
network in macaques, particularly in the ventral temporal
lobe. As stimuli we used monkey faces with different views,
352 Neuron 70, 352–362, April 28, 2011 ª2011 Elsevier Inc.
expressions, and gaze directions to activate areas that respond
to identity as well as areas that respond to social cues like
facial expression. Faces were contrasted against fruit, houses,
and fractals. In addition, we repeated the experiment in anes-
thetized monkeys to eliminate possible confounding effects
of motion and to identify those areas that depend on awake
We found face-selective patches in STS, prefrontal cortex,
and amygdala in agreement with earlier fMRI studies in the
macaque (Logothetis et al., 1999; Pinsk et al., 2005; Rajimehr
et al., 2009; Tsao et al., 2003, 2008b). But we also found
face selectivity in several additional locations: ventral V4,
anterior TE, and the parahippocampal cortex in the ventral
temporal lobe and the hippocampus and entorhinal cortex
(EC) in the medial temporal lobe (MTL). The face-selective pat-
tern was largely similar in awake and anesthetized monkeys,
suggesting that most of this network is not dependent on the
awake state of the animal. Our results show that the face-pro-
cessing network in the macaque brain is more extensive than
reported previously and includes several additional areas in
MTL and the ventral temporal cortex, including potential FFA
Visual Responses in the Temporal Lobe
acquired while the animals were shown visual stimuli belonging
to different categories (faces, fruit, fractals, and houses for
awake animals and faces and fruit for anesthetized animals).
Data were acquired at 7T by using a vertical primate scanner
(see Goense et al., 2008 for technical details). Figure 1 shows
examples of the stimuli (Figure 1A) and the timing of the behav-
ioral paradigm used for awake monkeys (Figures 1Band 1C). We
used an SE-based functional imaging protocol that was opti-
mized to perform fMRI in the ventral temporal lobe and was
previously shown not to suffer from signal loss near the ear canal
(Goense et al., 2008). Figures 1D–1G show that by using this
protocol we were able to reliably record functional activation in
the ventral temporal lobe. Figures 1E–1G show visually induced
functional activation in an awake animal in response to static
images. Visual responses were found in the early visual cortex
(V1–V4) and in a large portion of the temporal cortex, including
the STS and inferior temporal gyrus (ITG). In addition, the ventral
temporal cortex was also clearly activated (Figure 1G), including
reward & inter trial time (sec)
Example Stimuli for Each Object Category
(A) Example images for faces, fruit, houses, and
fractals. All images have the same mean intensity
and contrast and similar power spectrum.
(B) Images were randomly selected from a cate-
(isoluminant gray) in between.
(C) Behavioral paradigm for experiments with
awake animals. The monkey initiated a trial by
ceasing body and jaw movement and was
required to remain motionless throughout the trial.
Four seconds after the start of the trial a fixation
spot was shown, upon which the monkey was
required to fixate in a 3?window. After 4 s of
fixation the stimulus was presented. The monkey
maintained fixation during stimulus presentation
and for an additional second afterwards. After this
the monkey was allowed to break fixation but
needed to remain immobile for 9 more s. The
monkey received a juice reward after successfully
completing the trial.
(D–G) Visually responsive areas in an awake
monkey (B04, all categories versus blank). In
awake fMRI-experiments the entire temporal lobe
and part of the parietal lobe were covered (D).
(E–G) Visually responsive voxels are shown on
a rendered brain (p < 0.001 uncorrected, cluster-
level R 5). Visual activation can be seen in the
entire temporal lobe. The ventral view in (G) shows
extensive activation in the temporal lobe without
loss of BOLD signal near the ear canal. Because
the extent of the stimuli was 5?, V1 activation
(E and F) was restricted to the foveal 5?.
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ventral TE and the parahippocampal region (area TF). The
pattern of visually elicited activation agrees well with the known
visual areas based on electrophysiological and anatomical data
(Gattass et al., 2005).
Face and Object Selectivity in the STS
We examined face-selective areas in the STS and ITG of awake
monkeys (Figure 2) with the purpose of comparing the functional
activation measured with the high-field SE-BOLD method to
data reported in the literature with the more common GE-
BOLD method (Pinsk et al., 2005) and the contrast agent-based
cerebral blood volume (CBV) method (Tsao et al., 2003, 2008a).
The comparison of faces versus the other three object cate-
gories yielded significant bilateral face-selective BOLD activa-
tion in the anterior, middle, and posterior parts of the STS
(Figure 2 and Figure S1, available online). All animals showed
strong and extensive face-selective activation in the STS
(Table 1) in agreement with previous studies in macaques
(Logothetis et al., 1999; Pinsk et al., 2005; Rajimehr et al.,
2009; Tsao et al., 2003, 2008a). Although in cases of strong
activation the STS middle patch appeared to be contiguous,
single-subject analysis showed that in several animals it actually
consisted of two separate patches. Figures 2E and 2F show the
time courses of the signals in the anterior and middle face
patches in the STS of monkey B04. The face patches showed
significantly higher responses to faces than to the other cate-
% signal change
Figure 2. Brain Areas in the STS and ITG that
Showed Significantly Higher Responses to Faces
Than to the Other Categories in Two Awake
(A–D) Face-selective areas shown on 3D reconstructed
brains. The right hemispheres are shown in (A) and (C) and
the left hemispheres in (B) and (D). Face-selective activity
is seen in the STS, fundus, upper and lower bank, and the
lip. The most extensive face-selective activation was
found bilaterally in the middle and the anterior STS.
Contrast: face > fruit, house, and fractals; p < 0.001
uncorrected, cluster-level R 5 voxels.
(E and F) Average time courses of the face patches in the
middle (mSTS) (E) and anterior STS (aSTS) (F) of monkey
B04 in response to the different categories. The time
courses show that the face patches in the STS also
responded to the other categories. The time courses
represent the average responses over the significantly
activated voxels in the middle and anterior STS. The gray
area indicates the stimulus duration. Error bars show the
SEM. See Figure S1 for coronal views of the face-selective
areas in STS. Abbreviations: AMTS, anterior medial
temporal sulcus; AS, arcuate sulcus; CS, central sulcus;
IOS, inferior occipital sulcus; IPS, intraparietal sulcus; LS,
lateral fissure; LUS, lunate sulcus; PS, principal sulcus.
gories, but they showed nonzero responses to
the other object categories. These results indi-
cate that the face areas in the STS do not exclu-
sively respond to faces, consistent with pre-
vious literature in humans and monkeys (Bell
et al., 2009; Haxby et al., 2001; Ishai et al.,
1999; Pinsk et al., 2005; Tsao et al., 2003).
Because STS neurons respond selectively to different cate-
gories, including faces and other objects (Logothetis and Shein-
berg,1996; Zangenehpour andChaudhuri, 2005), wealsoexam-
ined the object selectivity in the STS by comparing the response
to each of the nonface categories to the other three categories.
that fruit evoked higher BOLD responses than the other cate-
gories in several brain regions across all subjects (Figure 3 and
Table S1). Fruit-selective activation was found in V3, the poste-
rior STS (TEO), and anterior STS (IPa). Fruit-selective activation
rior to the face-selective patches. The distribution of house- and
fractal-selective voxels was not consistent across animals,
which suggests that only biologically relevant objects such as
faces and fruit evoke sufficiently strong and clustered functional
activation in the monkey temporal cortex.
Face Selectivity in the Ventral Temporal Cortex
Although many electrophysiological studies have shown face-
and object-selective cells in the anterior temporal pole in
macaques (i.e., area TGa, the area around the anterior medial
temporal sulcus [AMTS], and the perirhinal and entorhinal
cortices; Nakamura and Kubota, 1996) and fMRI activation has
been shown in monkeys (Logothetis et al., 1999; Tsao et al.,
2003) and humans (Kriegeskorte et al., 2007; Rotshtein et al.,
2005), face-selective BOLD signals are not always strong or
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354 Neuron 70, 352–362, April 28, 2011 ª2011 Elsevier Inc.
canal can potentially obscure face-selective areas in the ventral
temporallobeinbothhumansandmonkeys.Hence, a goal of the
present study was to examine whether there are possibly addi-
tional face-selective areas in this region. By using our SE fMRI
protocol, we found multiple face-selective areas in the ventral
temporal cortex and MTL in both awake monkeys (Figure 4 and
Figure S2). We considered an area face selective if it was signifi-
cantly activated in four or all five animals (see Table 1); although
for inclusion. We found face-selective areas around the AMTS
(labeled AMTS) at AP 17–21 (Figure 4B), which for four animals
was localized in TEav, and for one at the border of TEav and
TEad. Furthermore, a face-selective area was found in anterior
ventral TE (AP 13–21) corresponding to TEad and another patch
was found in the most anterior part of the temporal cortex, area
tion in ventral V4 near TF (Figure 4C, Figures S2C and S5, and
Table 1), and a face-selective area located in the parahippocam-
pal cortex (area TF) at AP 2–10 (Figure 4D, Figures S2D and S5,
cortex contains multiple additional face-selective patches.
Although the monkeys were only required to fixate, we found
face-selective activation in the medial temporal lobe in the ento-
rhinal cortex (Figure 4E and Figure S2E) and two patches in the
hippocampus (anterior and posterior) (Figure 4G and Fig-
ure S2G), areas usually associated with memory (Squire et al.,
2004). Face-selective activation was also identified in the amyg-
dalae in both awake monkeys (Figure 4F and Figure S2F) in
agreement with previous fMRI and neurophysiology studies
(Hadj-Bouziane et al., 2008; Hoffman et al., 2007; Leonard
et al., 1985). Outside the temporal lobe, face-selective patches
were found in the anterior insula (Figure 4H and Figure S2H)
and posterior cingulate cortex (Figure 4I and Figure S2I).
Face Selectivity in Awake and Anesthetized Monkeys
Three monkeys were scanned anesthetized, with the goal of
identifying whether activation of these face-selective areas
depends on processes that require the animal to be awake,
like processes involving attention or memory. Because even
minor animal motion can potentially lead to artifactual activation
(Goense et al., 2010), anesthetized experiments have an addi-
tional advantage in that they provide a control, which allowed
B04 G03N08C06 L04
Figure 3. Brain Areas Selective to Fruit
Fruit-selective areasare located in theSTS,the ITG, and the IOS. See also Table S1. Contrast: fruit > face, house, and fractals inthe awake animals B04 and G03,
and fruit > face in anesthetized animals; p < 0.001 uncorrected, cluster-level R 5 voxels.
Table 1. Face-Selective Areas in Awake and Anesthetized
Known Face Areas
BABABA BA BA
Amygdala BAL BA––
OF**L BA BA
PF** BABA BA
Unknown Face Areas
aInsula (or LS)a
pCingulate (area 23/24)a
aCingulate (area 32)b
vaTE (TEad)L–R BA–
Included in the table are all areas that showed significantly higher
responses to faces than to the other categories in at least three monkeys
(p < 0.001 uncorrected; cluster-level R 5 voxels). Most areas showed
bilateral activation (BA), although several areas showed lateralized
responses (indicated L for the left and R for the right hemisphere). *Brain
areas that were not included in the imaging protocol (prefrontal areas and
anterior cingulate) or for which the resolution was insufficient to accu-
rately delineate them (claustrum).
aAreas where face-selective activity was found in all animals.
bAn area was activated in four out of five monkeys.
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inated by motion artifacts.
Figure 5 shows that face-selective responses in most areas
were retained under anesthesia and the pattern of activity was
largely similar for awake and anesthetized animals. Figure S3
shows the other two anesthetized animals and Table 1 provides
a summary of the areas thatwere activated in the two awake and
three anesthetized monkeys. Face-selective functional activity
was preserved under anesthesia in the STS (Figure S4), in the
ventral temporal lobe, around the AMTS, and in ventral V4,
area TF, the entorhinal cortex, the insula, and cingulate cortex
(Figure 5, Table 1, and Figures S3 and S5).
In contrast to the awake animals, where we focused on the
temporal lobe, in anesthetized animals the entire brain was
scanned. Thus, we also found two face-selective areas in the
prefrontal cortex (Table 1): one in the lower limb of the arcuate
sulcus (area 44/45, Figure S4) and one in the orbital frontal
(OF) cortex (area 13 m). Prefrontal face-selective activation
othetis et al., 1999) and awake macaques (Tsao et al., 2008b).
The notable differences between awake and anesthetized
monkeys occurred in the hippocampus and amygdalae.
Responsiveness to faces was detected in the amygdalae of
both awake monkeys but only in the amygdala of one anesthe-
tized monkey (Table 1). Hippocampal activation, which was
bilateral in both awake monkeys, was absent in two of the anes-
thetized monkeys and unilaterally preserved in one animal. The
functional activation in the amygdalae and hippocampus is
Figure 4. Face-Selective Areas in Awake Monkey B04
(A) Locations of the slices shown in panels (B–I).
(B–I) Face-selective areas were found around AMTS (B), ventral V4 (C), area TF (D), the entorhinal cortex (EC; E), the amygdala (F), the anterior hippocampus (G),
the anterior insula (aInsula; H), and posterior cingulate cortex (pCingulate; I). Also visible are the face-selective patches in the entorhinal cortex (B), the STS (C, D,
and G–I), around the AMTS (E and H), the hippocampus (F), and area TF (I). The activated areas showed significantly higher responses to faces than to the control
categories (face > fruit, houses, and fractals; p < 0.001, cluster-level R 5 voxels). See Figure S2 for the other awake monkey.
E F Cingulate
Figure 5. Face-Selective Areas in a Representative Anesthetized Monkey
The AMTS area (A), ventral V4 (B), area TF (C), the entorhinal cortex (D), the insula (E), and the posterior cingulate cortex (F) are also activated in anesthetized
monkeys (face > fruit; p < 0.001 uncorrected, cluster-level R 5 voxels). Also visible are the hippocampus and the orbital frontal cortex (B), the STS and insula (C),
the amygdala (D), and the STS (E). See Figure S3 for the other two anesthetized animals.
fMRI of Face Processing in Macaque Ventral IT
356 Neuron 70, 352–362, April 28, 2011 ª2011 Elsevier Inc.
suppressed under anesthesia or at the least severely reduced.
That these areas are activated only in awake animals suggests
they are involved in awake processing of faces or their
Figure 6 shows the mean responses of the face-selective
areas to faces and to the other categories in awake and anesthe-
tized animals. Overall response amplitudes were lower in anes-
thetized than awake monkeys. The reduction of the amplitude
of the BOLD signal was expected given the effects of anesthesia
on the vascular system. While the face-selective areas in the
middle STS showed significant responses to the other object
categories (t test, p < 0.05), the ventral areas, for instance
near the AMTS, were more selective to faces, given that the
responses to objects were often not significantly different from
zero in these areas. These results suggest that the ventral
pathway is more selective for faces than the STS patches.
In this study, we took advantage of the increased sensitivity
of high-field (7T) SE fMRI to study face processing in the
temporal lobe of awake and in the entire brain of anesthetized
vV4paraH AMTSEC Amyg Hippo CinmSTSaSTSInsula
vV4paraH AMTS ECmSTSaSTS Cin Insula
% signal change
% signal change
Figure 6. Percentage BOLD Signal Change of the
Face-Selective Areas in Response to the Different
(A and B) Mean responses to the different categories for
awake monkeys (A, two monkeys) and anesthetized
monkeys (B, three monkeys).
(A) For awake monkeys the mean response amplitude was
determined by calculating the percentage change at the
peak response (6–10 s after stimulus onset) over all
significantly activated voxels of a given patch and aver-
aged across animals and experiments. Only the middle
STS showed significant responses to all control cate-
gories. The responses to fruit, houses, and fractals in the
face-selective areas in awake monkeys were not signifi-
cantly different from each other and thus only fruit was
used as a control in the anesthetized experiments.
(B) The response amplitudes were lower than in awake
monkeys but selectivity patterns were similar. Only the
middle STS showed a significant response to fruit. Error
bars indicate the SEM. Abbreviations: paraH, para-
hippocampal cortex; Amyg, amygdala; Hippo, hippo-
campus; Cin, cingulate; PF, prefrontal cortex.
monkeys. First, we confirmed the face-selective
activation found in earlier monkey fMRI studies,
but in addition, we found and report a number of
face-selective areas in the ventral and medial
temporal lobe that have not been described
before, such as ventral V4, ventral TE, TG,
hippocampus, entorhinal cortex, and parahip-
pocampal cortex (area TF). Some of the more
occipitotemporal face areas. We also scanned
awake and anesthetized animals by using the
same protocol and observed that MTL activa-
tion that was present under passive viewing
was mostly preserved under anesthesia (except
in the hippocampus), suggesting that processes related to
memory, like familiarity or recollection, are not necessarily
required for functional activation in the MTL.
Face-Selective Activation in the Temporal Lobe
Inagreement with previous studiesof face-selective activationin
macaques we found extensive face-selective activation in STS,
with the largest and most reproducible face-selective patches
located in the middle STS, which responded to other categories
as well (Pinsk et al., 2005; Tsao et al., 2003). Activation in or near
faces. Selectivity of AMTS areas for faces was also identified in
earlier fMRI studies (Logothetis et al., 1999; Tsao et al., 2003)
although not in all, most likely because of signal loss in the
temporal lobe. Additional face-selective areas were found in
area TG and ventral TE but these results were less reproducible
across animals. Figure 7 summarizes our results and compares
using macaque fMRI (Bell et al., 2009; Logothetis et al., 1999;
Pinsk et al., 2005; Tsao et al., 2008a, 2008b). The figure high-
lights the overall agreement across studies and illustrates the
interindividual variability. Note that in our study faces with
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different gaze directions and expressions were used, while other
investigators used neutral faces, which may account for some of
the observed variability, especially in STS. Electrophysiological
data in monkeys show that STS neurons encode facial expres-
sions and gaze directions, and face-selective neurons in the
anterior ventral temporal cortex are thought to be involved in
the encoding of identity (De Souza et al., 2005; Eifuku et al.,
2004; Hasselmo et al., 1989; Leopold et al., 2006). Human
fMRI data show a similar division, with the STS being involved
in the encoding of changeable aspects of faces, while ventral
and anterior areas are involved in detecting faces and encoding
identity (Haxby et al., 2000; Kriegeskorte et al., 2007; Rotshtein
et al., 2005; Sergent et al., 1992).
Because the SE signal is not degraded by susceptibility arti-
facts from the ear canal and because we used volume coils
that provided uniform SNR in the entire ventral visual pathway,
it allowed us to map several additional face-selective patches
in ventral areas (Figure 7B). We found face-selective patches in
the posterior part of the ventral temporal cortex, of which the
most posterior patch was located in the anterior part of ventral
V4. Face selectivity in this area has not been reported before,
but most electrophysiological studies in this region used simple
features such as gratings, edges and textures, and selectivity to
+300 +12+18 +24+6-6
Tsao 2008a,b Ku et al.
+300 +12+18+24 +6-6
Ku et al.
Figure 7. Comparison of Face-Selective
Activation Found in the Current Study with
Face-Selective Activation Described in the
Literature Superimposed on a Side and
Ventral View of the Brain
(A) Side view of the brain. The locations of face-
selective patches found in the literature (Bell et al.,
2009; Logothetis et al., 1999; Pinsk et al., 2005;
Tsao et al., 2008a, 2008b) are marked by closed
symbols and locations found in the current study
are indicated by the open circles. For the activated
areas described by Tsao et al. (2008a, 2008b),
naming conventions used by the authors were re-
otherwise positions were estimated by comparing
the coronal slices to the atlas by Saleem and
where activation extended over multiple slices the
average position was taken. The locations shown
are after normalization to the macaque template
(McLaren et al., 2009). Note that not all studies
(including ours) make a distinction between STS
patches located on the lip and the fundus.
(B) Ventral view of face-selective activation in this
study (open circles) and the literature (closed
symbols). The coordinates of the ventral activation
are given in Table S2. Abbreviations: LOS: lateral
orbital sulcus; MOS: medial orbital sulcus; OTS:
occipitotemporal sulcus; PMTS: posterior middle
temporal sulcus; RS: rhinal sulcus.
complex objects such as faces was not
explicitly tested (Gattass et al., 1988).
We assigned the activation in this area
to ventral V4 based on the histological
atlas by Saleem and Logothetis (Saleem
with electrophysiology and the border of ventral V4 also shows
substantial interanimal variation (Boussaoud et al., 1991; Gat-
tass et al., 1988). Furthermore, different atlases show variation
in the areal borders in this region (Paxinos et al., 2000; Saleem
and Logothetis, 2006). Because activation was often located
near the border of V4 it also cannot be excluded that activation
was located adjacent to ventral V4. Thus, to be able to defini-
tively assign this activation to ventral V4, the location would
have to be verified histologically in the same animal. So although
this face-selective area might be a tentative homolog of the OFA
in humans, which is located adjacent to human V4 (Brewer et al.,
2005; Hasson et al., 2003), it requires further study. Face-selec-
tive activation was also found in all animals in area TF, which lies
anterior to ventral V4 and is part of the parahippocampal cortex.
According to anatomical and retinotopic criteria, Halgren et al.
(Halgren et al., 1999) predicted that a macaque homolog to the
human FFA would be located in this area. Responses to objects
have been reported with electrophysiology in area TF (Bous-
saoud et al., 1991; Riches et al., 1991; Rolls et al., 2005) and
neurons that exhibited some response to faces were seen in
the parahippocampal cortex (Sato and Nakamura, 2003),
although the parahippocampal cortex is usually associated
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358 Neuron 70, 352–362, April 28, 2011 ª2011 Elsevier Inc.
with spatial processing (Alvarado and Bachevalier, 2005; Bach-
evalier and Nemanic, 2008). However, this region is still relatively
unexplored with electrophysiology and except for the current
study no fMRI study has yet shown face-selective activation in
macaque parahippocampal cortex.
of the OFA and FFA in humans. Further study is needed to deter-
are actual homologs of human face areas. Similar activation and
functionality for anterior ventral areas between macaques and
humans has been suggested (Tsao et al., 2008a), but a macaque
equivalent of FFA has not been conclusively identified. Face-
selective activation in the fusiform gyrus was also shown in chim-
panzees (Parr etal., 2009).Because themiddleSTS patchshows
vation is most robust in humans (while STS activation is often
weak), the middle STS patch was suggested to be the macaque
the brain maps of macaques and humans (Orban et al., 2004;
Rajimehr et al., 2009; Tsao et al., 2003, 2008a). However, STS in
as well (Puce et al., 1998; Winston et al., 2004), suggesting func-
tional similarity between humans and monkeys. The intensity
difference may reflect different specialization and different
on detection and identification in humans and a stronger
emphasis on expression in monkeys. Thus, the homology ques-
tion requires further study. Comparative studies between
macaques and humans are likely to benefit from performing SE
fMRI of the more anterior ventral temporal areas in humans.
Although Schmidt et al. (Schmidt et al., 2005) found that SE
fMRI revealed no additional face-selective areas, their study
was performed at 3T, and because functional changes are lower
for SE-BOLD than for GE-BOLD methods, the BOLD signal may
face-selective areas are easily missed if the spatial resolution is
insufficient (Op de Beeck et al., 2008). The higher BOLD signal
and the higher spatial resolution achievable at high field (7T)
may negate some of these drawbacks and may reveal additional
face-selective areas in humans as well.
Effects of Anesthesia
There was a large degree of similarity in the areas that were
activated in awake and anesthetized monkeys. Most visual
areas also showed face selectivity under anesthesia, including
prefrontal areas. The difference in stimulus size between awake
and anesthetized animals did not lead to any differences
between awake and anesthetized animals, most likely because
faces were contrasted against other categories and because
many of the reported areas are size invariant. The areas that
showed no consistent activation under anesthesia were the
amygdala and the hippocampus. Both awake animals showed
bilateral activation in the amygdala, in agreement with earlier
studies (Hadj-Bouziane et al., 2008; Hoffman et al., 2007). Only
one animal showed activation in the amygdala under anesthesia.
icance in the anesthetized monkeys, because faces were con-
trasted against fruit and the amygdala also showed significant
responses to fruit in awake monkeys (p < 0.05). The amygdala
has a high m-opioid receptor density (Mansour et al., 1988) and
it is also possible that binding of remifentanil may have reduced
its neural responses.
There are two caveats concerning the results from anesthe-
tized monkeys. One is that the results may depend on the type
of anesthesia and results may not generalize to other anesthesia
regimens because different anesthetics affect cognitive pro-
cessing differently. The other concerns the interpretation of the
represents the input to an area and its local processing than its
output and that functional activation can occur in the absence
of spiking (Goense and Logothetis, 2008; Logothetis et al.,
2001). The conservative interpretation of preserved BOLD signal
in a brain area would be that this means the activated area
receives synaptic input. What types of further neural processes
take place, whether these differ between awake and anesthe-
tized animals, and how they relate to single- or multiunit electro-
physiological data (neural output) remains subject to further
investigation. Conversely, a lack of BOLD signal could signify
a lack of input from an earlier area. The issue of interpretation
of the BOLD signal is independent of anesthesia, however, and
is also relevant for awake subjects.
Face-Selective Activation in the MTL
The importance of the MTL in learning and memory function is
well established. Area TE, the perirhinal (Brodmann areas 35
and 36) and parahippocampal cortices, the entorhinal cortex,
and the hippocampus have all been shown to be involved in
learning and memory (Osada et al., 2008; Squire et al., 2004)
with different structures mediating different (and possibly over-
lapping) functions, i.e., forming associations between objects,
forming associations between objects and locations, or forming
memories of scenes or locations. Although face selectivity is
were shown in the human MTL in the context of memory and
familiarity (Eichenbaum et al., 2007; Gonsalves et al., 2005; Quir-
campus, entorhinal cortex, and parahippocampal cortex, even
though the monkeys were passively viewing. Activation in the
parahippocampal and entorhinal cortex and areas TE and TG
also remained under anesthesia.
Two intensely debated questions are: (1) whether the MTL
serves only a memory function or whether it also has a role in
visual perception (this concerns in particular the perirhinal
cortex; Baxter, 2009; Gaffan, 2002; Graham et al., 2010; Levy
et al., 2005; Suzuki, 2009) and (2) whether familiarity and recol-
lection are mediated by different MTL structures (this question
focuses on whether the hippocampus is also involved in famil-
iarity; Eichenbaum et al., 2007; Squire et al., 2007). Because
our animals were not engaged in a memory task we cannot
directly address such questions, albeit the activation of MTL
structures under passive viewing and anesthesia may provide
important hints on them. There are several possible interpreta-
tions of the activation of the MTL under passive viewing and
anesthesia: (1) the BOLD signal in these areas reflects visual
input, but cannot be directly associated to the function or the
fMRI of Face Processing in Macaque Ventral IT
Neuron 70, 352–362, April 28, 2011 ª2011 Elsevier Inc. 359
output of the area; (2) MTL neurons respond to the visual prop-
erties of the stimuli (this would argue for a perceptual involve-
ment of the MTL); (3) activation is due to familiarity or memory,
with faces as a preferred stimulus, although this would imply
that these processes take place under anesthesia.
Although the stimuli were familiar to the awake animals, two of
face-selective responses in the entorhinal and parahippocampal
cortex in these animals cannot represent prior memory or famil-
iarity of the stimuli. Although the assumption that familiarity or
memory processes play absolutely no role under anesthesia is
anterior temporal lobe, the entorhinal cortex, and the parahippo-
neurons to visual properties of the stimulus or due to input from
earlier areas. Functional activation of the hippocampus was
reduced under anesthesia (activation was unilaterally preserved
in only one animal), suggesting that the hippocampus may
need processes like storage and retrieval to be activated.
The MTL may show face-selective activation given the biolog-
ical relevance to macaques. Identification of conspecifics and
their association to certain events is important for monkeys’
social functioning and the MTL may play an important role in
encoding and retrieval of information associated with specific
individuals. Although the MTL activation found in this study
raises many interesting questions, further study with memory
tasks is needed to address these questions.
In conclusion, by using high-field SE fMRI, we were able to
show functional activation in an extensive network within the
ventral temporal lobe and MTL and identified several additional
face-selective areas, some of which may be homologous to
human face areas. Most activated areas were also activated
under anesthesia, suggesting the network is to a large extent
independent of conscious processes.
Awake monkey fMRI experiments were performed on two healthy male
monkeys (Macaca mulatta), weighing 14 (G03) and 16 kg (B04). We needed
three experimental sessions for animal B04 and five sessions for animal
G03. In each session, the monkey successfully performed the task for an
average duration of 2 hr. All experiments were approved by the local authori-
ties (Regierungspra ¨sidium) and were in full compliance with the guidelines of
the European Community (EUVD 86/609/EEC) for the care and use of labora-
tory animals. The primate setup and hardware for the awake monkey experi-
ments were described in detail previously (see Goense et al., 2008 and
Logothetis et al., 1999). Briefly, the monkeys were implanted with a custom-
made MR-compatible headpost and extensively trained in a mock environ-
ment to acclimatize them to the scanner environment and noise. During
scanning the monkeys were seated in a custom-made primate chair with their
head fixed to a predetermined location on the chair to ensure reproducible
positioning in each session. The animal’s jaw and body motions were
monitored by custom-designed sensors. Eye movements were monitored by
using an infrared camera or implanted eye coil and data were analyzed with
iView software (iView, Sensomotoric Instruments GmbH, Teltow, Germany).
Anesthetized experiments were performed on three adult macaques weighing
7–12 kg (two males, C06 and L04, and one female, N08). The experimental
setup and anesthesia protocol were similar to the procedures described
in Logothetis et al., 1999. Anesthesia was maintained with remifentanil
(0.5–2 mg/kg/min) and mivacurium chloride (3–6 mg/kg/hr). Physiological
parameters were monitored and maintained within the normal physiological
range as described previously (Logothetis et al., 1999).
In awake experiments visual stimuli were presented binocularly by using
an SVGA fiber optic system (AVOTEC, Silent Vision) with a resolution of
800 3 600 pixels and frame rate of 60 Hz. The stimuli were 24 exemplars of
faces, fruit, houses, and fractals (Figure 1A) and occupied 5?3 5?of visual
angle. The smaller stimuli made it easier for the monkeys to maintain fixation.
Images were black and white, normalized to the same mean intensity and
contrast, and overlaid on a gray background with the same intensity as the
mean intensity of the stimuli. All stimuli had similar power spectra. Fractals
were used instead of scrambled images because the power spectra of fractals
more closely match that of natural objects (Falconer, 2003). The face stimuli
were monkey faces of different individuals and although the individuals
pictured were unknown to the monkeys they were trained on these exemplars.
Themonkey faces had different views, gaze directions,andfacialexpressions.
Figure 1C shows the trial-based behavioral paradigm that was used to obtain
artifact-free MR images. Trials were initiated by the monkey by ceasing body
and jaw motion. After sitting quietly and fixating on a central fixation spot for
4s, six images were presented (Figure 1C). The animals wererequired to fixate
within a 3?window before and during the stimulus. To receive the reward, the
monkeys had to remain motionless for an additional 9 s. Trials were aborted
when the animal moved or broke fixation.
In anesthetized experiments, the stimuli were presented by using a custom-
made MR-compatible display system, similar to the AVOTEC system, with a
resolution of 800 3 600 pixels. Animals were wearing lenses (Wo ¨hlk-
Contact-Linsen, Scho ¨nkirchen, Germany) to focus the eyes on the stimulus
plane and the eyepieces of the stimulus presentation system were positioned
by using a modified fundus camera (Zeiss RC250; see Logothetis et al., 1999).
The same stimuli were used as in the awake experiments except that a block-
design paradigmwas used and stimuli spanned 10?3 10?.Onlyfacesand fruit
selective areas to the control categories were not significantly different in the
awake experiments. In anesthetized monkeys larger stimuli were used to
decrease possible errors because of minor variations in the alignment of the
displays to the center of the fovea. Given that the face stimuli are contrasted
against fruit and size differences affect both categories, stimulus size is not
expected to affect the results. In each block, 48 images were presented in
random order (24 exemplars of the same category, each presented twice),
yielding a 48 s visual stimulation time. During the blank period a mid-gray
square was presented for 48 s.
Images were acquired by using a 7T vertical Bruker BioSpec scanner with
a bore diameter of 60 cm (Bruker BioSpin, Ettlingen, Germany). The imaging
procedure for awake monkeys was described in detail elsewhere (Goense
et al., 2008); a summarized description follows. The RF coil was a custom-
made 16 cm saddle coil that covered the entire brain and was optimized for
imaging of the temporal lobe. A two segment SE-EPI was used for image
acquisition. The field of view (FOV) was 12.8 3 9.6 cm2and the matrix size
was 84 3 64 for B04 and 96 3 64 for G03. Slices were 2 mm thick and were
acquired at ?20?from the Frankfurt zero plane (Figure 1D) to reduce suscep-
tibility artifacts. Seventeen slices per volume were used to cover the entire
visual cortex. TE was 40 ms and TR 1 s, yielding a final temporal resolution
of 2 s per volume. A total of 3440 volumes were used in the analysis for B04
and 4563 volumes for G03. For anatomical reference a high-resolution
(0.5 mm isotropic) T1-weighted three-dimensional (3D) MDEFT image was
acquired under general anesthesia at 4.7 T (see Logothetis et al., 1999). In
each session, SE-EPI and GE anatomical reference images were acquired
withthesameslice orientationasthefunctional images. FortheGEanatomical
reference, which was used for quick visualization during experiments, FOV
was 12.8 3 9.6 cm2, matrix size 256 3 256, slice thickness 1 mm, TE 10 ms,
and TR 750 ms. For the SE-EPI anatomical reference, which was used as an
intermediate to accurately coregister the statistical map with the MDEFT
image, a 16 segment SE-EPI was acquired (see Goense et al., 2008). The
fMRI of Face Processing in Macaque Ventral IT
360 Neuron 70, 352–362, April 28, 2011 ª2011 Elsevier Inc.
matrix was 256 3 192, bandwidth 60–159 kHz, spatial resolution 0.5 3
0.5 mm2, slice thickness 1 mm, TE 62 ms, and TR 4 s. For field mapping,
two 3D FLASH images were acquired with FOV 12.8 3 9.6 3 9.6 cm3and
matrix 128 3 128 3 64, resulting in a resolution of 1 3 0.75 3 1.5 mm3. TEs
were 4.9 and 5.9 ms, TR was 50 ms, and flip angle was 15?. Data were field-
map corrected as described previously (Goense et al., 2008).
For anesthetized experiments a 12 cm custom-made quadrature RF coil
was used that covered the entire brain. Images were acquired by using
a four segment SE-EPI. The FOV was 8.0 3 7.2 cm2, with a matrix size of
80 3 72, yielding a final resolution of 1.0 3 1.0 mm2. The slices were acquired
along the temporal lobe, and 22–25 slices with a thickness of 2 mm were typi-
cally needed to cover the entire brain. TE was 40 ms and TR was 2 s per
segment, yielding a final temporal resolution of 8 s per volume. Data were
acquired inasingle session(experiment day)foreachanimal, whichamounted
anatomical reference a 16 segment SE-EPI was acquired in each scanning
session. The matrix was 192 3 176 and the FOV was 8.0 3 7.2 cm2with
1 mm slice thickness. TE was 62 ms and TR was 3 s. Reference anatomical
scans and the 3D FLASH for field mapping were acquired by using the same
parameters as in awake experiments.
EPI images were reconstructed by using Bruker ParaVision 4.0 software. Data
were analyzed by using custom-written software in MATLAB (The MathWorks,
Natick, MA, USA), SPM 2 and SPM 5 (Wellcome Department of Cognitive
Neurology, London, UK [Friston et al., 1995]), and Caret 5.9 (Washington
University, St. Louis, USA [Van Essen et al., 2001]). Data from awake monkeys
were processed following the methods described in Goense et al., 2008.
Images were realigned, field-map corrected, and coregistered with the
anatomical image by using SPM 2. For anesthetized animals similar proce-
dures were used. Images were smoothed by using a 3 mm (awake) or 2 mm
(anesthetized) full width at half maximum Gaussian kernel. Statistical analysis
was done in SPM 2 by using general linear model analysis with the default
level of p < 0.001 uncorrected for multiple comparisons) and clustered in three
dimensions by using a minimal cluster size of 5 contiguous voxels.
The high-resolution MDEFT anatomical image of each monkey was skull
stripped by using MRIcro 1.39 (Chris Rorden, ª 1999–2005) and imported
into Caret 5.9. The segmentation, reconstruction, and inflation of cortex
were done automatically with minimum manual correction (http://brainvis.
wustl.edu/wiki/index.php/Main_Page). Functionally activated areas were as-
signed based on the atlas by Saleem and Logothetis (Saleem and Logothetis,
2006). For comparison with functional activation reported in the literature,
images were referenced to the aforementioned atlas after normalization
to the rhesus macaque template by McLaren et al. (McLaren et al., 2009)
(http://www.brainmap.wisc.edu/monkey.html) by using the normalization
routines in SPM5. All images are displayed referenced to the Frankfurt zero
plane. AP positions refer to the AP positions for individual monkeys after
normalization to the template. Locations of functional activation in the litera-
ture were estimated based on AP positions of individual animals when AP
positions were given (typically not normalized to the macaque template);
otherwise positions were estimated by comparing coronal slices shown in
the figures to the atlas by Saleem and Logothetis (Saleem and Logothetis,
2006). In cases where activation extended over multiple slices, the average
position was taken. Data from the left and right hemispheres were merged in
the schematic figure (Figure 7).
Supplemental Information includes six figures and two tables and can be
found with this article online at doi:10.1016/j.neuron.2011.02.048.
We are grateful to Thomas Steudel for the excellent technical support and to
Hellmut Merkle for designing and building the RF coils. Andreas Bartels and
Christoph Kayser provided usefulinformation on data analysis;Natasha Sigala
and Kevin Whittingstall provided helpful discussions and comments on the
manuscript. This work was supported by the Max Planck Society.
Accepted: February 9, 2011
Published: April 27, 2011
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