DOI: 10.1093/brain/awg241

Advanced Access publication July 22, 2003

Brain (2003), 126, 2381±2395

A network of occipito-temporal face-sensitive areas
besides the right middle fusiform gyrus isnecessary for normal face processing
Bruno Rossion,4 Roberto Caldara,1 Mohamed Seghier,2 Anne-Marie Schuller,4 Francois Lazeyras2 andEugene Mayer3
1Faculte
Â de Psychologie et des Sciences de l`Education,
2DeÂ partement de Radiologie, Hopital Universitaire deGeneÁve and 3UniteÂ de Neuropsychologie, Hopital
Universitaire de GeneÁve, Geneva, Switzerland, and 4UniteÂ
de Neurosciences Cognitive et Laboratoire deNeurophysiologie, UniversiteÂ Catholique de Louvain,
Louvain-la-Neuve, Belgium

Summary

Neuroimaging studies have identi®ed at least two bilateral areas of the visual extrastriate cortex that respond
more to pictures of faces than objects in normal humansubjects in the middle fusiform gyrus [the `fusiform
face area' (FFA)] and, more posteriorly, in the inferior
occipital cortex [`occipital face area' (OFA)], with aright hemisphere dominance. However, it is not yet
clear how these regions interact which each other andwhether they are all necessary for normal face perception. It has been proposed that the right hemisphere
FFA acts as an isolated (`modular') processing system
for faces or that this region receives its face-sensitive
inputs from the OFA in a feedforward hierarchicalmodel of face processing. To test these proposals, wereport a detailed neuropsychological investigation combined with a neuroimaging study of a patient presenting
a de®cit restricted to face perception, consecutive to

Correspondence to: Bruno Rossion, UniteÂ de
Neurosciences Cognitives (NESC), UniversiteÂ Catholiquede Louvain, 10 Place du Cardinal Mercier, 1348 Louvainla-Neuve, Belgium
E-mail: bruno.rossion@psp.ucl.ac.bebilateral occipito-temporal lesions. Due to the asymmetry of the lesions, the left middle fusiform gyrus and theright inferior occipital cortex were damaged but theright middle fusiform gyrus was structurally intact.
Using functional MRI, we disclosed a normal activationof the right FFA in response to faces in the patient
despite the absence of any feedforward inputs from theright OFA, located in a damaged area of cortex.
Together, these ®ndings show that the integrity of theright OFA is necessary for normal face perception andsuggest that the face-sensitive responses observed at thislevel in normal subjects may arise from feedback connections from the right FFA. In agreement with thecurrent literature on the anatomical basis of prosopagnosia, it is suggested that the FFA and OFA in the righthemisphere and their re-entrant integration are necessary for normal face processing.

Keywords: prosopagnosia; face recognition; visual cortex; fusiform gyrus; FFA; feedback
Abbreviations: BORB = Birmingham Object Recognition Battery; FFA = fusiform face area; fMRI = functional MRI;OFA = occipital face area; rFFA = right fusiform face area; rOFA = right occipital face area

Introduction

Understanding how the human brain perceives and recognizes faces is one of the most exciting and debated areas ofresearch in cognitive neuroscience (e.g. Haxby et al., 2000;
Tarr and Gauthier, 2000). Pursuing this general goal,
neuroimaging studies (mostly PET and functional MRI)
have identi®ed a number of relatively small functional areas
lying outside the retinotopic cortex that respond more to
pictures of faces than other objects in the normal humanbrain. The most robust difference in activity between faces
Brain 126 ã Guarantors of Brain 2003; all rights reserved

and objects has been described in the lateral middle fusiform
gyrus, bilaterally, but often stronger in the right hemisphere(e.g. Halgren et al., 1999; Haxby et al., 1999; Kanwisher
et al., 1997; McCarthy et al., 1997; Rossion et al., 2000). Thisis the region that has been named the `fusiform face area'(FFA) and de®ned as a module for face perception(Kanwisher et al., 1997). Posterior to the FFA, a region of
the inferior occipital gyrus (termed OFA for occipital facearea, Gauthier et al., 2000) also responds more to faces than

2382

B. Rossion et al.

objects, with a larger differential response in the righthemisphere as well (Sergent et al., 1992; Halgren et al., 1999;
Haxby et al., 1999; Gauthier et al., 2000; Rossion et al.,2000). A smaller number of studies have also disclosed larger
activation for faces than objects in the posterior part of thesuperior temporal sulcus, but these observations are muchless consistent (e.g. Puce et al., 1998; Haxby et al., 1999).
Although their relative functions in face processing remain
unclear, these regions are considered to form a common
neural network for face perception, providing outputs tofurther areas and processes related for instance to facial
expression processing, or retrieval of semantic knowledge
about persons (see Haxby et al., 2000).
Besides the precise function of these regions, there areseveral important questions regarding the neuro-functional
basis of face processing which cannot be addressed byneuroimaging alone. First, neuroimaging cannot indicate
whether these functional brain regions are necessary for the
successful perception and recognition of faces. It may well bethat some of these regions are activated in response to thepresentation of faces in normal humans and yet do not play a
crucial role in any important aspects of face recognition. As amatter of fact, selective lesions of the regions where thelargest proportion of face-selective cells (~20%, see Gross,1992) are usually found in the monkey brain (namely in the
superior temporal sulcus) do not appear to prevent monkeys
from recognizing faces (Heywood and Cowey, 1992). A
second, related, question that is dif®cult to resolve by
neuroimaging experiments alone is the nature of the interactions between the different functional brain areas involvedin face processing. For instance, in a recent neuro-functionalmodel of face processing, Haxby and colleagues (see also
Halgren et al., 1999) proposed that the most anterior facesensitive regions of the visual cortex, such as the FFA, receive
their input from the OFA, which would be involved in a basic
analysis of facial features (Haxby et al., 2000). However, thishypothesis has not yet been veri®ed by neuroimaging studies
of normal subjects.
Neuroimaging studies of brain-damaged patients may help
resolve these questions (Price and Friston, 2001). One of themost spectacular de®cits observed following brain damage is
prosopagnosia, a de®cit classically de®ned as the inability torecognize faces of conspeci®cs, despite normal intellectual
abilities and apparently normal recognition of other object
categories. Although a few cases had been reported at the endof the 19th century, the term `prosopagnosia' was coined by
Bodamer in 1947 (Bodamer, 1947). Since then, despite its
rarity, a certain number of cases with a major de®cit of facerecognition have been described (see Farah, 1990; for more
recent cases, e.g. Sergent and Signoret, 1992; Clarke et al.,
1997; Gauthier et al., 1999; Laeng and Caviness, 2001).
Prosopagnosic patients are usually able to distinguishbetween a face and another object category (`face detection'),but are unable to identify familiar facesÐincluding famous
faces, friends and relatives or even their own faceÐand arealso unable to learn new faces (Damasio, 1985). Different

types of prosopagnosia have been described in the literature(e.g. Damasio et al., 1990), but it is generally acknowledgedthat every patient is unique and most studies focus on thedetailed analysis of single cases in order to clarify current
theoretical debates regarding normal face processing (seeFarah, 1990).
The lesions that cause prosopagnosia are usually found inventral occipito-temporal cortex, involving the lingual andfusiform gyri, and are bilateral in most of the cases (Damasio
et al., 1982; Sergent and Signoret, 1992) although right
unilateral lesions can be the cause of the syndrome (e.g.
Landis et al., 1988; Wada and Yamamoto, 2001; Uttner et al.,2002). However, establishing relationships between structures and function based on clinical studies alone has always
been problematic; the lesions of prosopagnosic patients are
not always clearly identi®able, can be highly variable fromcase to case, and are usually very large and not limited to thestructures subtending face processing. Relative to the study ofpatients with naturally occurring brain lesions, neuroimaging
thus affords far greater anatomical precision and avoids theconfounding factors associated with patient studies, such as
any compensatory functional reorganization of the brain(Sergent et al., 1992).
In the present paper, we combine a detailed neuropsychological testing with a neuroimaging investigation of a
prosopagnosic patient (P.S.) in order to: (i) test whether astructurally and functionally normal FFA is suf®cient fornormal face processing or if other high-level visual areas
besides the right FFA are necessary for normal faceperception; and (ii) test the hypothesis that the FFA activation
is dependent on face-sensitive feedforward inputs from the
OFA.

Methods
Subjects
Patient P.S.

P.S. is a 52-year-old woman (born in 1950; right-handed) who
sustained a closed head injury (hit at the back of the head by abus) in 1992. CT scans ®rst indicated contusions in theoccipital and parieto-occipital regions, and the left cerebellum. A recent MRI scan revealed lesions to the lateral part ofthe occipital and temporal lobes, bilaterally, as well as in theanterior part of the left cerebellum. The right hemispherelesion extends from the posterior part of the inferior occipitalgyrus to the posterior fusiform gyrus. The left hemisphere
region is more anterior and covers a large part of the fusiform
gyrus, extending into the lower part of the temporal lobe
(Fig. 1).
Following months of neuropsychological rehabilitationand spontaneous recovery, P.S. was normal at all the nonvisual functions that were slightly impaired following the
injury (motor aspects of language, calculation, imagery andmemory), yet she was slow at all visual tasks requiring a ®negrained discrimination (September 1993: overlapping ®gures,

FFA activation with OFA damage in acquired prosopagnosia

Fig. 1 P.S.'s lesions are bilateral but asymmetrical, covering theoccipital inferior gyrus and posterior fusiform gyrus in the righthemisphere and the middle and anterior fusiform gyrus in the left
hemisphere. As shown on the three slices, the most robust faces±
objects activation (in red) is at the level of the right middle
fusiform gyrus, anterior to the lesion. The homologous region in
the left hemisphere has been damaged by the lesion, as illustrated
on the transverse and coronal slices. The reverse comparison(objects±faces) led to a large signi®cant difference in the
parahippocampal gyrus (in blue, transversal slice), as shown
previously (e.g. Epstein and Kanwisher, 1998).

dots counting tasks), presented a de®cit in contrast sensitivity
and a massive prosopagnosia. Helped by a neuropsychological rehabilitation programme, P.S. returned to her work asa kindergarten teacher, and she has to be trained regularly at aneuropsychological rehabilitation centre to use external cues
to distinguish among children of her new class (see Mayer
et al., 1999). P.S. complains of a profound dif®culty inrecognizing faces, including those of her own family, and her
own face. To determine a person's identity, P.S. is reliant oncues such as haircut, hat, moustache or earrings, but also on
the person's voice, his/her posture and clothes. We presented
P.S. with 60 faces of famous people, whose faces were wellknown by her before her accident (selected on the basis of aquestionnaire that she had to ®ll up months before testing),
and 60 unfamiliar faces. Each face was presented for 3000 ms
and P.S. had 5000 ms to press one of two keys according to
the familiarity/unfamiliarity of the face. Whereas she correctly classi®ed all the unfamiliar faces, P.S. pressed the key`familiar' for 14 out of the 60 famous faces only. After theexperiment, she was shown the famous faces she classi®edcorrectly (14) and asked to name them or give some
information about them; she was correct only for four
faces. P.S. does not complain of any dif®culty at object
recognition, but she reads more slowly than she used to.
The performance of P.S. on standard clinical tests of visual
perception and recognition is given in Table 1. P.S.'s visualacuity is good, but not perfect and she is slightly slower thannormal controls at detecting letters and numbers in her right2383

visual ®eld. She is also slower than normal controls at a
simple reaction time task, detecting a cross in the centre of thescreen, as typically observed in brain damaged patients (e.g.
Benton, 1986). Her contrast sensitivity is in the normal range
except at higher frequencies (>22 c/degree). She is perfect at
all tests of low level visual processing as tested by the
Birmingham Object Recognition Battery (BORB) (Riddochand Humphreys, 1993; tests 1 to 6), including matching
objects under different viewpoints (tests 7 and 8), and she has
no dif®culty in perceiving and identifying objects, including
semantic associations and naming (Table 1 Object recognition). She was also tested in an object decision task on acomputer (line drawing objects taken from Snodgrass andVanderwart, 1980; non-objects taken from Kroll and Potter,1984), which she performed perfectly. Her short-term andlong-term visual memory are in the normal range (Table 1), as
well as reading (slower than normal controls but perfectly
accurate) and visual imagery (BORB, test 9). She waspresented with the full set of colorized Snodgrass andVanderwart's objects (Rossion and Pourtois, 2001) to name,each object being presented for 3000 ms or until response on acomputer screen. She was perfect at this task, always giving
the most common object label or a close label also given bynormal young subjects (see Rossion and Pourtois, 2001)
without any hesitation.
These observations contrast with her face perception andrecognition performance. She achieved a score of 27 out of 54
in the Benton face perception test, which rank her as highly
impaired (<39). Her score at the Warrington face recognition
test was 18 out of 25, being also signi®cantly less accurate
than controls.

Normal controls

In addition to P.S., six age- and sex-matched normal subjects
performed all the behavioural tasks described in the sections
below. Eleven normal controls (®ve females, mean age
29.8 years, all right-handed) were used in the neuroimaging
study. Young normal controls of both genders were used in
the neuroimaging study mainly for practical reasons, but there
is no evidence of gender differences in face-sensitive
responses, which also appear to remain stable until theninth decade of age (Brodtmann et al., 2002). Both P.S. andthe normal controls in the neuroimaging study gave informed
consent to the experiments, which were approved by the
Ethics Committee of the University of Geneva (Hopital
Universitaire).

Materials and procedure
Behavioural tests

Computer tests of face processing. P.S.'s face processing
abilities were tested extensively using a variety of computertasks with well-face stimuli (see Fig. 2). Sex decision on faces
was tested with 50 face stimuli (25 males) presented on the2384

B. Rossion et al.
Table 1 Summary of visual functions of patient P.S.
Basic perceptual processes
Visual ®eld
AcuityContrast
Colour perception (Ishihara)
Low-level visual processing
Benton line orientation
Birmingham Object Recognition Battery (BORB)
Object copying test 1
Line length (test 2)
Size (test 3)
Orientation (test 4)
Gap position (test 5)
Overlapping shapes (test 6)
Minimal feature match (test 7)
Foreshortened views (test 8)
Object recognition
BORB (test 10) Object decision task
Object decision task on computer

Slower than normals on left superior ®eld
0.7 bilaterally
Nicolet contrast sensitivity test: OK
12/17, lower range
Normal (57/60)
OK
OK
OK
OK
OK
OK, slowed down for three subtests
OK
OK

BORB (test 11) Item match (class recognition)
BORB (test 12) Semantic association
Object naming (Colorized Snodgrass and Vanderwart)
Short-term visual memory
Test de la ruche (French)
Long-term visual memory
Doors test
Rey complex drawing
Face processing
Benton face recognition test
Warrington face recognition battery
Reading
Visual imagery
Object Drawings (test 9: BORB)
Reaction Time (phasic alert)

centre of the screen for 10 s maximum (next trial as soon as
key press). P.S. and control subjects had to indicate the sex of
the person by pressing one of two keys as accurately and as
quickly as possible. Facial expression analysis was tested in
two blocks. In the ®rst block, three kinds of facial expression
were presented: joy; fear; and anger (each face for 10 s
maximum; next trial on key press), and subjects had to press
one of three keys according to the kind of expression
presented (second block: choice among disgust; sadness; andsurprise). Age judgement was also a three-forced choice task:
subjects were presented with 40 successive faces (10 smaximum) of different age and had to categorize them inthree age classes: child (10 trials); adult (17 trials); and old
person (13). Face matching, as indicated in Table 2, wastested using a same/different task with two faces presented
simultaneously (a full front face and a three-quarters face) for
10 s maximum (two blocks of 35 trials).
Discrimination of non-face objects from visually homogenous categories. P.S. was presented with a matching taskwith a set of homogeneous objects: cars (Fig. 2). Seventy-twopairs of three-quarter pro®le cars were presented successively
in the centre of the screen for 7000 ms each maximum or untilOK
OK (98%)
Objects: 946 ms; non-objects: 1626 ms
OK
OK
OK
OK
OK
OK
27/54 (strongly impaired); 32 s
18/25 (impaired, percentile 3)
Slow but accurate
OK
Slower than normals, percentile 5

the subject's response (a blank screen of 1000 ms separated
two trials). Subjects simply had to press a key if the two cars
were the same (half of the trials) as accurately and quickly as
possible. P.S. was also tested with a matching task using
different sets of multi-parts novel objects (Fig. 2). In the ®rst
twoblocks, objects were presented simultaneously in the same
viewpoint. For each block, there were 60 trials (7000 ms
maximum, 1000 ms inter-stimulus interval).
Analysis. The Z-score is the ratio of the difference between
P.S.'s score and the normal controls average score by the SDof the normals. A Z-score >2 means that P.S.'s performance isabove or below 2SDs of the normals. A¢ is a nonparametricmeasure of sensitivity used in previous investigations of
prosopagnosic patients (Gauthier et al., 1999). Chance
performance yields a score of 0.5 and positive values indicate
better than chance sensitivity.

MRI acquisition

Stimuli. Twenty full front photographs of unknown faces(http://faces.kyb.tuebingen.mpg.de/) and 20 pictures of com-

FFA activation with OFA damage in acquired prosopagnosia

2385(TR = 3000 ms; TE = 40 ms; ¯ip = 80°; FOV = 250 mm;
matrix = 128 3 128; 30 contiguous 5 mm axial slices).
Epochs of face and object presentations (18 s, 6 3 TR) werecounterbalanced and separated by baseline epochs (®xation
cross, 9 s; 3 TR). Two runs were performed, with six epochsof each experimental condition (faces or objects) in each run.
In each face/object epoch, 24 stimuli were presented for
750 ms, without any offset, but a small shift of position(20 pixels) between consecutive images. Twenty different
images were used in each epoch, with four images repeated
twice consecutively, and subjects were required to detect therepetitions (one-back task) by pressing a response key. In
addition, patient P.S. was scanned twice, with the same
paradigms, in two different sessions at a 5 month interval inorder to ensure reproducibility of our ®ndings.

Fig. 2 Examples of stimuli used in testing P.S.'s face and object
perception. (A) Two pictures of faces presented simultaneously
under different viewpoint. (B) Two pictures of cars used in the
study. (C) Two novel (`scott' objects, http://www.cog.brown.edu/~tarr/stimuli.html).

mon objects (object databank at http://www.cog.brown.edu/~tarr/stimuli.html) were used. Stimuli were presented to thesubjects via a video projector, a front-projection screen and asystem of mirrors fastened to the head coil. The visual ®eld
spanned by this set-up was approximately 15° 3 11°.
Scanning procedures. For anatomical scans, experiments
were performed on a 1.5 T whole-body ECLIPSE system(Marconi Medical Systems, Cleveland, OH, USA) using thestandard head coil con®guration (body coil for excitation,
head coil for detection). Acquired multi-slice volume waspositioned on sagittal scout images. A ®rst GRE (gradientrecalled-echo) T1-weighted sequence [TR (repetitiontime) = 162 ms; TE (echo time) = 4.47 ms; ¯ip = 80°; FOV(®eld of view) = 250 mm; matrix = 256 3 256; slice
thickness = 5 mm] was performed to acquire the same volume
as in the functional session. Anatomical reference images
consisted of a 3D GRE T1-weighted sequence (TE = 15 ms;
FOV = 250 mm; matrix = 256 3 256; slice
thickness = 1.25 mm).
For the fMRI localizer experiment, functional imaging
consisted of an echo planar imaging (EPI) GRE sequence

Data analysis. Collected data was processed with crosscorrelation analysis (Bandettini et al., 1993) after motion
correction (Woods et al., 1992) using MEDX software(Sensor Systems, Sterling, VA, USA) (Gold et al., 1998).
Data were smoothed spatially by convolution with a Gaussian[full width half maximum (FWHM) = 6 3 6 3 6] kernel. The
cross-correlation, expressed in terms of Z-values (Le Bihanet al., 1993) was calculated pixelwise between a delayed boxcar function and the set of measurements, without temporalauto-correlation correction (Friston et al., 1995).
Individual maps were then normalized to the Talairach
space (Talairach and Tournoux, 1988). Afterwards, thestatistical distribution of the Z-values for each subject wascalculated and a probability value for each Z-value wasattributed. Clusters size of >0.08 cm3 (>10 voxels; voxel size
after normalization was 2 3 2 3 2 mm3) showing statisticallysigni®cant Z-score (typically Z-threshold = 3.0, at P < 0.002,
uncorrected) in the faces±objects comparison were considered (Forman et al., 1995). In addition, clusters with signal
intensity <50% of the mean intensity of the functional images
were ruled out, in particular in the vicinity of P.S. lesions.

Results
Neuropsychological investigations
Computer tests of face processing

The results of the face processing tests in P.S. and normal
controls are given in Table 2. P.S. was impaired at a sex
decision task, both in accuracy and sensitivity (percentage:
Z = 7.94, P < 0.001; A¢: Z = 8.30; P < 0.001) and response
times (Z = 7.77, P < 0.001). Although she could discriminate
faces of different expressions, P.S. was not as good as normal
subjects at these tasks (®rst block: percentage: Z = 21,
P < 0.001; reaction times: Z = 9.66, P < 0.001; second block:percentage: Z = 0.79, NS; reaction times: Z = 3.96, P < 0.001).
As for judging the age of faces, P.S. had a normal
performance at this task (accuracy: 90%; Z = 1.282,
P = 0.10), but was signi®cantly slower than control subjects(Z = 8.84, P < 0.001). Finally, P.S. was strongly impaired at a

2386

B. Rossion et al.

Table 2 Summary of P.S.'s performance during the computer tests on face processing

Gender decision
Facial expression
Block 1 (joy, fear, anger)
Block 2 (disgust, sadness, surprise)
Age assessment
Face matching

Control subjects (mean age: 51 years)

P.S. (age 50 years)

Accuracy (%)

Reaction times (ms)Accuracy (%)

Reaction times (ms)

96

1162

79

3316

98
89
96
90

1318
1468
1218
2721

77
88
92
62

2265
2348
2315
5105

Table 3 Summary of P.S.'s performance during the computer tests on object processing
Control subjects

Cars
Novel objectsÐsame viewpoint (set A)
Novel objectsÐsame viewpoint (set B)
Novel objectsÐdifferent viewpoint

Accuracy (%)

Reaction times (ms)Accuracy (%)

Reaction times (ms)

90
97
79
77

2437
1798
4071
5158

83
95
82
72

3218
3202
4412
6571

face matching task, both in accuracy and sensitivity (percentage: Z = 7.74, P < 0.001; A¢: Z = 11; P < 0.001) and she
was also much longer than control subjects (reaction times:
Z = 4.23, P < 0.001).

Discrimination of non-face objects from visuallyhomogenous categories

As indicated in Table 3, P.S.'s performance was good,
although slightly lower than the age-matched controls(sensitivity: Z = 2.23; P < 0.05) due to her higher rate offalse alarms, but she was not signi®cantly slower thencontrols (Z = 1.67, not signi®cant). In the ®rst two blocks,
objects were presented simultaneously in the same viewpoint.
For set A, P.S.'s sensitivity was very good; she made only
three mistakes but she was slower than the controls (Z = 4.19,
P < 0.001). A similar pattern was found for set B, which wasmore dif®cult overall, objects being more similar to eachother. P.S.'s sensitivity was in the normal range (see Table 3),
but she was also slower than the controls (Z = 4.48, P < 0.001).
Finally, we ran a block of trials with the different and same
trials presenting objects under different viewpoints. Again,
P.S.'s performance was within the normal range, but she wasslightly slower than normal controls (Z = 2.45, P < 0.01) andhits (Z = 2.19, P < 0.05).

Neuroimaging study

P.S.

A signi®cant activation for the comparison between faces andobjects was found in the right middle fusiform gyrus for all
the normal subjects (P < 0.002 uncorrected, 10 voxels

minimum, see Table 4 and Figs 3 and 5). This is the region
that has been termed the FFA (Kanwisher et al., 1997) andwill be referred to in this paper as the right fusiform face area(rFFA). The mean coordinates of activation for this region(Table 4) in the Talairach coordinates correspond to thecoordinates found in previous neuroimaging studies (e.g.
Kanwisher et al., 1997; Gauthier et al., 2000; Rossion et al.,2000). Compared with the Talairach-transformed individual
brain of our prosopagnosic patient P.S., this average
activation corresponds to an area of cortex completely sparedby the lesions (Figs 1 and 6). Most importantly, when P.S.
was tested in the same experiment, the rFFA presents asigni®cant differential response between faces and objects
just like normal subjects (Figs 1, 4 and 6; Table 5).
Furthermore, the extent and height of the rFFA activationin P.S. do not differ from normal controls (see Figs 3±6;
Table 5). Structurally and functionally, her rFFA thus appears
to be perfectly normal, and these observations were replicatedafter an interval of several months (Tables 5 and 6, Fig. 4).
These observations were made despite the fact that, as
expected, P.S. performed quite well in the one-back object
discrimination task (37 out of 48 correctly responded<750 ms; mean reaction times for correct trials: 499 ms),
but her performance was very low for the face stimuli (12 outof 48; 526 ms).
In most normal subjects (n = 9 out of 11), there was also asigni®cantly larger activation for faces compared with objects
in the right inferior occipital cortex [Table 4; Fig. 5; `rightoccipital face area' (rOFA)]. The coordinates of the maxima

FFA activation with OFA damage in acquired prosopagnosia

2387

Table 4 Mean coordinates, level of activation and size of the functional regions observed in all the normal control
subjects
Right FFA Talairach

S1
S2
S3
S4
S5
S6
S7
S8
S9
S10
S11
Mean 6 SE

Left FFA Talairach

x

y

z

Z-scoren voxelsxyz

Z-scoren voxels

38
45
38
46
42
41
32
31
48
47
47
41 62

±62
±62
±46
±50
±44
±48
±53
±54
±41
±40
±54
±50 62

±15
±17
±16
±15
±9
±14
±21
±25
±18
±15
±13
±16 61

4.66
4.03
3.74
3.9
5.23
3.46
3.38
2.92
2.80
3.16
4.23
11/11 subjects

108
219
69
314
90
45
27
5
5
33
417

±33
±28
±37
±35
±41
±40

±46
±61
±50
±49
±44
±48

±19
±13
±12
±17
±14
±13

4.62
3.24
3.63
4.66
5.08
3.41

16
14
5
191
25
16

±33

±67

±22

4.46

60

±38
±36 62±58±53 63±11±15 61

4.49
8/11 subjects

161

Right OFA Talairach

S1
S2
S3
S4
S5
S6
S7
S8
S9
S10
S11
Mean 6 SE

Left OFA Talairach

x

y

z

Z-scoren voxels

37

±87

±3

4.74

55

27
38
34
48
38
44
31
42
38 6 2

±83
±69
±80
±76
±73
±80
±93
±83
±80 6 2

0
±11
±10
3
±19
±11
±12
±3
±7 6 2

3.62
5.00
3.30
3.40
2.97
3.4
3.26
4.41
9/11 subjects

46
50
30
25
10
49
11
97

x

y

z

Z-scoren voxels

±33
±35
±29

±80
±83
±83

±11
±14
±11

3.02
3.90
3.99

5
44
50

±37

±78

±18

3.36

17

±34

±81

±18

3.45

19

±34 6 1

±81 6 1

±14 6 2

5/11 subjects

A signi®cant faces±objects difference was clearly observed in 11 subjects in the right middle fusiform gyrus, albeit slightly lower for two
subjects (5 voxels, in italics). Eight subjects presented signi®cant differences in the left fusiform gyrus and in the right inferior occipitalcortex (rOFA), and it was slightly below threshold for subject S8. In the left hemisphere, a small subset of subjects (®ve out of 11) but not
P.S., presented a larger faces±objects difference in the inferior occipital cortex.

of activation in the group analysis correspond to a region thathas been damaged by the lesion in P.S.'s brain (Figs 1 and 6).
Furthermore, the individual Talairach coordinates for the
maximum of activation in the rOFA of each subject also
correspond spatially to a structurally damaged area of cortex
in P.S.'s brain (Fig. 6).
In the left hemisphere, a number of subjects (n = 8 out of
11; see Table 4) showed a signi®cant increase in the left
middle fusiform gyrus for faces (±objects). Strikingly, theseareas of activation were all localized in a region that iscompletely damaged in P.S.'s brain (Fig. 6). Few (®ve out of11) subjects also showed a signi®cant differential response to
faces in an area of the left inferior occipital cortex (Fig. 6).
For P.S., there was a small but signi®cant extent of activationin the left inferior occipital cortex only in the ®rst session,
which was posterior to the damaged area. However, the mean
signal intensity of this activation was reduced by 60%
compared with the mean intensity of the functional images,
such that this activation in the vicinity of the lesion may

re¯ect an artefactual combination of partial volume and headmotion effects.
Finally, as described previously (e.g. Epstein and
Kanwisher, 1998), there was a signi®cant increase ofactivation for the opposite contrast (objects±faces) in amore medial and anterior region of the temporal lobe, in the
parahippocampal gyrus, for both P.S. (P < 0.002; size
>10 voxels; see Table 6; Fig. 3) and the normal controls (11out of 11 subjects at the same threshold).

Discussion
A selective de®cit at recognizing faces

On the basis of the patient's complaints and her results atclassical object recognition tests (Table 1), P.S.'s case canarguably be de®ned as one of the most selective de®cits forface recognition that has been described in the neuropsychological literature. She is perfect at object recognition andnaming. In this respect, she represents a clearer case of

2388

B. Rossion et al.

Fig. 3 Localization of the fusiform and occipital `face areas' and the parahippocampal place area in a few normal subjects (with a similarlevel of activation as P.S.; see Table 5).

prosopagnosia than most previously well-described cases ofacquired prosopagnosia, who presented evident de®cits andcomplaints at object recognition, such as patients L.H. (e.g.
Levine and Calvanio, 1989; Farah et al., 1995), S.M. and C.R.
(Gauthier et al., 1999), or E.L.M. (Dixon et al., 1998) for
instance. Although the distinction between apperceptive andassociative (prosop)agnosia is certainly not clear-cut (seeFarah, 1990), P.S. is de®nitely of the former type, as shownby her impairment at simultaneous face matching tasks.
P.S. is also slightly impaired at other face processing tasks
such as sex categorization and facial expression analysis,
whereas a number of previous cases of apperceptive
prosospagnosia have been reported to be intact at thesefunctions (e.g. Tranel et al., 1988). Evidence from functional
imaging in humans (e.g. Sergent et al., 1992; Morris et al.,1998) and neurophysiological recordings in monkeys (e.g.

Hasselmo et al., 1989) indicates that facial expression
processing and face recognition depend on separate brain
substrates, but that they probably share several primitive
perceptual mechanisms that could be impaired in P.S.'s casedue to the posterior localization of her lesions. The fact that
there was no activation of her amygdala (faces compared with
objects P > 0.05, uncorrected), a region that is involved inemotional aspects of face processing (Haxby et al., 2000) is
inconclusive because there was not any activation in thisregion for any of the control subjects for the face±object
comparison.
P.S. has no problem with object perception, matching,recognition and naming. She also performed at a normal leveland she was not signi®cantly slower than normal controls(one control was actually slower than P.S.) at a within
category discrimination task of control objects, namely cars.

FFA activation with OFA damage in acquired prosopagnosia

Fig. 4 (A) Percentage signal change (faces±objects) in the right
FFA of P.S. across the two different sessions (two runs in eachsession). (B) Average time course of the magnetic signal in the
FFA during all the runs for P.S.

When tested with novel objects sharing identical surface
properties but differing slightly by their overall shape and theshape of their parts (not their organization), P.S.'s performance was again in the normal range. She was slightly slowed
down overall, which should not be surprising given her
general slowing down typical of brain-damaged subjects (e.g.
Benton, 1986) and the fact that even normal control subjects
were also particularly slow at this task (>2000 ms on
average). Most importantly, however, increasing the visualhomogeneity of the distractors or presenting the objects under
different viewpoints caused a slight drop of performance andan increase of response times that was similar for P.S. and fornormal subjects (Table 3). Other evidence reported elsewhere(Rossion et al., 2002) also indicates that she is not moresensitive than controls to manipulations of the level ofcategorization in object discrimination tasks as used previously in other patients (Gauthier et al., 1999).
How can P.S.'s object recognition performance be soremarkably preserved despite presenting such extensive
lesions of the extrastriate visual cortex (Figs 1 and 6)? One
possibility may be that non-face objects are recognized using
a single well-localized system, different than that for faces
and located in the medial ventral temporal cortex where thelarger activation for objects was found to be normal for P.S.
(see Figs 1 and 6). However, recent evidence suggests that thediscrimination of object categories, including faces, can be
carried out through a distinct pattern of response across a

2389

wide expanse of cortex in the occipital and ventral part of thetemporal lobe (Ishai et al., 1999; Haxby et al., 2001). Because
large but also small amplitude responses in the ventral
temporal cortex carry information about the object appearance, only very large bilateral lesions of the ventral lateraland medial visual pathway would lead to impairments ofbasic level object recognition according to this view. The factthat P.S., despite extensive lesions of the ventral temporal
cortex, is still able to easily perform such basic level
discriminations, can be taken as supporting the view that
object recognition (including faces) at the basic level iswidely distributed (Ishai et al., 1999; Haxby et al., 2001):
there is still enough information carried out in the visualcortex to perform basic level object recognition ef®ciently.
Yet, contrary to most objects, faces pose a special challenge
to the visual system because they belong to a highly visuallyhomogeneous category (Damasio et al., 1982) and need to berecognized at the individual level for ef®cient social interactions (Tarr and Gauthier, 2000; Tanaka, 2001). The
development of a visual expertize at recognizing faces at
the individual level appears to require the fast extraction ofcon®gural relationships (Maurer et al., 2002), a mechanismthat may extend to the discrimination of non-face categories
from visually homogeneous categories following expertize
training (Gauthier and Tarr, 1997) and seems to be impairedin P.S.'s case (Rossion et al., 2002).

The necessary integrity of the right hemisphereface-sensitive areas in face processing

The lesions of prosopagnosic patients usually concern theventral part of the occipital and temporal cortex, bilaterally(e.g. Damasio et al., 1982; Sergent and Signoret, 1992; Clarke
et al., 1997), with an area of maximum overlap between
lesions including the right posterior and middle fusiform
gyrus (Barton et al., 2002). Three recent case descriptions of
prosopagnosia with unilateral damage have also identi®ed theright middle fusiform gyrus as a critical area for normal faceperception. In one case, the lesion concerned both the rightfusiform gyrus and the lateral occipital cortex (Wada andYamamoto, 2001), whereas in two other cases the lesion also
extends posteriorly but possibly spares the right lateral
occipital cortex, at least structurally (Uttner et al., 2002).
These observations are in agreement with the proposal thatthe right middle fusiform gyrus or rFFA is a dedicated areathat is critical for face perception, or a `face module'(Kanwisher et al., 1997; McCarthy et al., 1997). However, inthe present study, we observed a prosopagnosic patientpresenting a structurally intact right middle fusiform gyrus orrFFA and, most importantly, a signi®cantly larger response to
faces±objects at this level (Figs 1 and 6). This result suggeststhat this region was also intact functionally, at least as far as
basic level face categorization is concerned. These neuroimaging ®ndings are in agreement with a recent fMRI study that
disclosed a rFFA activation in a prosopagnosic patient (S.M.;

2390

B. Rossion et al.
Table 5 Comparison of the right FFA response observed in P.S. (scanned twice) and thenormal subjects
Subjects

S5
S1
S11
S2
S4
S3
S6
P.S.(1)
P.S.(2)
S7
S10
S8
S9

Talairach coordinates
x

y

z

42
38
47
45
46
38
41
42
41
32
47
31
48

±44
±62
±54
±62
±50
±46
±48
±59
±59
±53
±40
±54
±41

±14
±15
±13
±17
±15
±16
±14
±18
±18
±21
±15
±25
±18

Z-meanSize (cm3)

5.23
4.66
4.23
4.03
3.90
3.74
3.46
3.43
3.22
3.38
3.16
2.92
2.80

0.72
0.86
3.33
1.75
2.51
0.55
0.36
0.17
0.24
0.22
0.26
0.04
0.04

Subjects are ranked by order of magnitude in the height of activation for the difference between faces andobjects.

Table 6 Signi®cant activations (Z > 3.0) observed for P.S. during the two scanning sessions
Contrast

Faces±objects 1

Objects±faces 1

Faces±objects 2

Objects±faces 2

RegionFusiform gyrus RH
Other regions:Middle/inferior temporal gyrus RH
Inferior/middle frontal gyrus Bil
Cingular gyrus
Parahippocampal gyrus RH
Parahippocampal gyrus LH
Other regions:Middle temporal gyrus LH
Superior parietal lobule LH
Fusiform gyrus RH
Other regions:
Inferior/middle frontal gyrus Bil
Inferior parietal lobule RH
Parahippocampal gyrus RH
Parahippocampal gyrus LH
Other regions:Middle temporal gyrus LH
Superior parietal lobule LH
Middle occiptal gyrus RH

Talairach coordinates

Z-meann voxels

x

y

z

42

±59

±18

3.43

21

30
-23

±42
±43

±15
±12

4.43
3.73

106
36

41

±59

±18

3.22

30

31
±24

±42
±45

±16
±11

4.44
4.12

136
55

RH = right hemisphere; LH = left hemisphere. The bilateral activation of the parahippocampal gyrus for the comparison between objects
and faces corresponds to the locus of activation de®ned as the `parahippocampal place area', which usually responds less to faces than toother object categories.

Marotta et al., 2001), although this patient also presented
large de®cits at recognizing common objects (Gauthier et al.,1999) and his lesions were mostly anterior (temporal lobe),
sparing the entire occipital lobe and the fusiform gyrus
bilaterally. Together, these ®ndings contradict the view thatthe rFFA represents a module for face perception andsupports a critical role of other high-level visual regions fornormal face processing (ToveÂe, 1998; Haxby et al., 2000,
2001).
What is the localization of these high-level visual regionsthat appear to be critical for normal face processing?
Although the region of the left FFA is damaged in P.S., it isunlikely that the areas of the left occipital and temporal cortex
that respond more to faces in normal subjects are also critical.

FFA activation with OFA damage in acquired prosopagnosia

2391

Fig. 5 Average time courses of activation in the right fusiform `face area' and the occipital `face area' forfour control subjects illustrated in Fig. 3 (except for Subject 3, who was replaced here by Subject 1, whoin turn showed signi®cant activation in both regions).

Indeed, several cases of prosopagnosia have been observed
previously with unilateral right hemisphere lesions (Landis
et al., 1988; Wada and Yamamoto, 2001; Uttler et al., 2002).
The functional integrity of the left face-sensitive areas was
unknown in these cases, although there was no evidence for adecrease of blood ¯ow in the left hemisphere in the casedescribed by Wada and Yamamoto (2001). There are also a
number of cases with extensive lesions of the ventral occipitaland temporal left hemisphere without prosopagnosia thathave been reported in the literature (see Farah, 1990). Yet, it
has also been shown that a lesion to the left hemisphere, evenin right-handed humans, may be necessary at least in somecases (Ettlin et al., 1992) to produce a prosopagnosic de®cit,
or even suf®cient (Mattson et al., 2000), thus pointing to theindividual-speci®c degrees of hemispheric dominance forface processing.
If the necessary role of the left hemispheric regions
remains unclear, what our study indicates, however, is thatthe rOFA is not only involved during face processing innormals, but that it is a necessary component for suchnormally functioning face processes to take place.
The face-sensitive response in the inferior occipital cortex(rOFA), within the lateral occipital (LO) complex involved inshape perception (Malach et al., 1995), is observed in manyneuroimaging studies (e.g. Halgren et al., 1999; Haxby et al.,
1999; Gauthier et al., 2000; Ishai et al., 2000; Rossion et al.,2000). Yet, despite the robust co-occurrence of this region
with the FFA, authors have been quick to reject the possibility
that the OFA presents a particular sensitivity to faces(Kanwisher et al., 1997), probably because of its relatively
early localization in the ventral pathway, and its somewhat
weaker face-sensitive response compared with the FFA(Gauthier et al., 2000). On the other hand, Haxby et al.
(2000) included this OFA in their neuro-functional architecture of face processing, suggesting that the rFFA receives
most of its input information for face processing directly from

2392

B. Rossion et al.

Fig. 6 Schematic representation on a Talairach slice (z = ±14) of
P.S.'s lesions and the areas of activation in the ventral extrastriate
cortex for both P.S. and normal subjects. The lesions cover mostof the functional network involved during the perception of faces,
but spare completely the right middle fusiform gyrus, where the`fusiform face area' is found in normal subjects.

this region (see also Halgren et al., 1999). Although our datasuggest rather a role of feedback connections in leading to theface-sensitive response of the OFA (see below), theyde®nitely support a critical role of the rOFA for normal
face processing, and thus a distributed processing model inthe ventral visual pathway for this function rather than asparse coding (Young and Yamane, 1992).

What is the neuro-functional relationshipbetween the OFA and FFA?

In their neuro-functional model of face processing, Haxby
et al. (2000) proposed that the rFFA receives most of its input
information for face processing directly from the posteriorrOFA, albeit suggesting the presence of feedback mechanisms between the two areas (see also Ishai et al., 2000).
According to this view, the rOFA is involved in the extractionof individual facial features and project in turn to the rFFA,
which would respond more to the whole face con®guration.
This hypothesis is consistent with a classical hierarchical andfeedforward view of the visual system (Hubel and Wiesel,1977), according to which the ¯ow of visual information goesfrom more posterior visual areas to more anterior areas, withan increase of the receptive ®eld and the complexity of thevisual information represented. At ®rst glance, this proposal
is also consistent with the observation that the rFFA, but not
the rOFA, is more activated when the subject's attention is
focused on the whole face versus single face features(Rossion et al., 2000). The less robust differential activation
between faces and objects usually found at the level of therOFA is also considered as supporting the view of aprogressively increasing face-selectivity along the ventral

visual pathway (Grill-Spector et al., 1999; Halgren et al.,1999).
However, the data reported here do not support thishypothesis of a main feedforward processing of information
related to faces from the rOFA to the rFFA since there was anormal activation of the FFA in the right hemisphere of P.S.,
despite a structurally and functionally damaged rOFA. In
addition, to our knowledge, there has not been any empiricalevidence in normal subjects supporting such a feedforwardand dependent processing of information from the OFA to the
FFA, whose differential function in face processing remain
largely unclear. Moreover, behavioural evidence clearlysuggests that the processing of faces as integrated wholes
has precedence over the processing of single face features(Tanaka and Farah, 1993)Ðan observation that does not ®twith a feedforward hierarchical model of face processing thatwould go from processing features to whole faces.
Electrophysiological recordings in humans also show thatthe peak latency of the N170 face-sensitive potential isdelayed for isolated face features, compared with the
response to whole face stimuli (e.g. Bentin et al., 1996).
For these reasons and given the data reported here, we suggestthat the larger response observed for faces compared with
objects as early as in the inferior occipital cortex (OFA) rather
arise from feedback connections from the rFFAÐan hypothesis perfectly compatible with the concurrent and distributed
processing of information (Felleman and Van Essen, 1991;
De Yoe et al., 1994) as well as the presence of feedback(Lamme and Roelfsema, 2000; Bullier, 2001) and re-entrant
phasic signalling (Edelman, 1993) in the visual cortex.
Recent studies using cooling techniques in monkeys indicatethat such feedback signals from higher order visual areas may
contribute to the emergence of functional responses in earlyvisual areas (Galuske et al., 2002; see also Bullier, 2001). If
such mechanisms were in place within the ventral visualstream, the response to faces observed at the level of theinferior occipital cortex could arise as a consequence of
higher-level face-sensitivity processes in the FFA, possibly to
guide the ®ne-grained visual analysis of faces for individual
discrimination (Gauthier et al., 2000) and old/new recognition (Rossion et al., 2003).
Although the ®ndings reported here suggest strongly thatthe two right-sided face-sensitive regions and their possible
re-entrant interactions are critical for normal within-category
discrimination and recognition of human faces, the limited
temporal resolution of fMRI does not allow us to clarify thenature of the dynamic interactions between these twofunctional areas at this stage. Future neuroimaging investigations of P.S. and other brain-damaged prosopagnosic
patients may be directed towards this goal of understanding
functional connectivity between visual areas (Friston, 2002).
As far as this prosopagnosic patient is concerned, future
neuroimaging studies will also have to clarify the exact
localization of the lesions with respect to the retinotopic
visual cortex and other extrastriate visual areas involved in
object recognition in the ventral temporal and occipital

FFA activation with OFA damage in acquired prosopagnosia
cortices (Ishai et al., 1999; Haxby et al., 2001), as well as totest the sensitivity of the rFFA to within category discrimination and recognition of faces.

Conclusions

Combining a neuropsychological and neuroimaging investigation on a case of prosopagnosia, we showed that besides theright middle fusiform gyrus (FFA), the right inferior occipitalcortex (OFA) is critical for normal face perception and thatthe face-sensitive responses observed at the level of theoccipital cortex in normal subjects may arise from feedback
connections from the right FFA rather than from afeedforward mode of processing. We suggest that a re-entrant
mechanism between these two regions in the right hemisphere subtends within category discrimination and recognition of faces.

Acknowledgements

We are immensely indebted to P.S. for her patience andmotivation during the experiments carried out in this study.
We also wish to thank Isabel Gauthier and Christine Schiltz
for their comments on a previous version of this manuscript
and Michael J. Tarr for his support and for making available
the novel stimuli used to test P.S. behaviourally. B.R. is
supported by the Belgian National Fund of Scienti®cResearch. This study was supported by a grant ARC 01/06±
267 (CommunauteÂ FrancËaise de Belgique ± Actions deRecherche ConcerteÂes).

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Received November 11, 2002. Revised February 26, 2003.
Second revision May 1, 2003. Accepted May 19, 2003