NeuroImage 15, 454–461 (2002)doi:10.1006/nimg.2001.0979, available online at http://www.idealibrary.com on

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Neural Correlates of Woman Face Processing by 2-Month-Old InfantsNathalie Tzourio-Mazoyer,* Scania De Schonen,†,1 Fabrice Crivello,* Bryan Reutter,‡

Yannick Aujard,§ and Bernard Mazoyer*,2

*Groupe d’Imagerie Neurofonctionnelle, UMR 6095 CNRS, CEA, Universite de Caen and Universite Paris V, GIP Cyceron, BP 5229,14074 Caen Cedex, France; †Developmental Neurocognition Group, Center for Research in Cognitive Neurosciences,

CNRS, 31 Chemin Joseph Aiguier, 13402 Marseille Cedex, France; ‡Center for Functional Imaging,Lawrence Berkeley National Laboratory, 1 Cyclotron Road, Mail Stop 55-121, Berkeley, California 94720;

and §Neonatalogy Unit, Hopital Robert Debre, 47, Boulevard Serrurier, 75019 Paris, France

Received April 24, 2001

The age of 2 months marks a turn in the develop-ment of face processing in humans with the emergenceof recognition based on internal feature configuration.We studied the neural bases of this early cognitiveexpertise, critical for adaptive behavior in the socialworld, by mapping with positron emission tomogra-phy the brain activity of 2-month-old alert infantswhile looking at unknown woman faces. We observedthe activation of a distributed network of cortical ar-eas that largely overlapped the adult face-processingnetwork, including the so-called fusiform face area.We also evidenced the activation of left superior tem-poral and inferior frontal gyri, regions associated, inadults, with language processing. These findings dem-onstrates that cognitive development proceeds earlyin functionally active interconnected cortical areasdespite the fact they have not all yet reached full met-abolic maturation. © 2002 Elsevier Science

INTRODUCTION

Infants show attraction for face pattern within thefirst minutes of life, a feature followed around the ageof 2 months by the ability to recognize their mother’sface among others (Morton and Johnson, 1991). Thismakes faces the primary visual stimulus category forwhich humans are expert at making discrimination. Asa matter of fact, young infants first recognize theirmother’s face on the basis of information coming fromboth the outer contour of the head and hair line and the

1 Present address: Laboratory of Cognition and Development,CNRS-Paris 5, 71 ave Edouard Vaillant, Boulogne-Billancourt92774, and INSERM E9935, Hopital Robert Debre, 48 BoulevardSerurier, 75019, Paris, France.

2 To whom correspondence and reprint requests should be ad-dressed. Fax: 33-2-31470222. E-mail: mazoyer@cyceron.fr.

4541053-8119/02 $35.00© 2002 Elsevier ScienceAll rights reserved.

internal configuration of the face (Bushnell et al.,1989). It is around the sixth week of postterm life thatthey become able to recognize their mother’s face onthe basis of the sole face internal configuration. Theneural bases of such an early developmental compe-tence are not known, although some authors proposedthat subcortical regions support face attraction atbirth, while visual cortical areas maturation is neces-sary for the emergence of larger looking fixation timefor faces stimuli (Morton and Johnson, 1991). Consis-tent with this hypothesis is the time course of regionalbrain metabolism that is highest at birth in subcorticaland primary motor regions, progressively increasingoverall the cortex, reaching relatively high values inposterior areas during the second month of posttermlife (Chugani et al., 1987).

Investigations of brain areas involved in face pro-cessing in alert infants have been up to now limited byboth ethical and technical issues. Here, we took advan-tage of the opportunity to perform positron emissiontomography (PET) scans in six 2-months-infants aspart of the clinical follow-up of the major brain stressthey had suffered from at birth, adapting to alert in-fants the classical PET activation paradigm used tomap cognitive functions in adults. Permission wasgiven by the Atomic Energy Commission Ethics Com-mittee to acquire a PET scan in each of two differentconditions during which visual stimuli were used tocapture the infant gaze for the 2 min necessary forlabeled water injection and blood flow map acquisition.

METHODS

Subjects

Six neonates were recruited during their first weekafter birth from a neonatalogy intensive care unit aftertheir parents had given their written informed con-

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sent. All infants, who were full term, had suffered froma neonatal syndrome known as hypoxic–ischemic en-cephalopathy (HIE), due to various causes (see Table1). Permission was given in 1990 by the Atomic EnergyCommission Ethics Committee to acquire blood flowmaps in these infants at the age of 2 months based onthe rationale that early detection of potential regionalblood flow deficits would help in defining the optimalneurospychological follow-up for these infants. Permis-sion was given for two oxygen-15-labeled water injec-tions with the constraint that the total injected dosewould stay below published recommendation for a sin-gle blood flow map in infant, e.g., 0.5 mCi/kg body wt(Powers et al., 1988).

All experiments were carried out between April 1991and July 1992. At the date of the PET scanning theinfants mean age was 10 weeks 3 days (ranging from 8weeks 2 days up to 11 weeks 5 days). They presentedmild neurological signs and were free from neurologi-cal medication (see Table 1). A clinical follow up wasconducted for at least 3 years that demonstrated anormal developmental age (Bayley, 1969) in four of thechildren evaluated with developmental tests (Brunetand Lezine, 1951; Sparrow and Cicchetti, 1989). Onechild was tested at the age of 6 months only, showing anormal development; it was not possible to follow-upone child.

Evaluation of Infant Visual Ability

Before PET scanning, each infant was tested forseveral visual abilities. All infants showed a goodsmooth horizontal visual tracking of a moving object.When presented with the mother and a stranger theyall looked at their mother and smiled within 40 s beforelooking at the stranger, looking thereafter back andforth at the stranger and the mother. They all fixated

TAB

Clinic

Child ID SexAge

(at PET study)N

syndrom

LEF M 2 months 3 weeks HIE; meconium inhhypoxemia with efor blood oxygena

CHE M 2 months 3 weeks HIENeonatal convulsio

BEL M 2 months HIE due to umbilicApparent death

KEB F 2 months 3 weeks HIEStatus epilepticus

PUJ M 2 months 3 weeks HIEStatus epilepticus

RED M 2 months 2 weeks HIE

Note. HIE, hypoxic–ischemic encephalopathy.

and tracked visually their silent mother’s face when

she was moving from right to left and conversely at adistance of 80 cm and when she was moving away fromthem up to a distance of 2 m. They all showed signs ofvisual habituation to a stationary visual patternwithin 10-s presentations followed by visual preferencefor a novel stimulus. They all turned their head andeyes to fixate their mother’s face when she was callingthem from the side. They all made eye to eye contactand smiled to their mother when she talked to them.

Stimuli

Our first constraint in stimulus design was to selecttasks that would capture the infant attention for atleast 2 min in order to obtain head immobility requiredby PET scanning. The second constraint came from thefact that a relatively low level cognitive task was to beincluded in the protocol so that regional blood flow mapacquired in this condition could serve for clinical pur-poses. Finally, the third constraint was that only twoinjections were to be performed. Accordingly, infantswere presented with two different kind of visual stim-uli. One consisted of colored slides of frontal view ofwoman faces wearing a black scarf on a black back-ground and showing a gentle but neutral expression(see example in Fig. 1). The scarf masked the outercontour of the hair so that only the face was visible.Face expressions were neutral in order to avoid asmuch as possible emotional and social reactions. Eachslide showed a different woman but for one that waspresented repeatedly at irregular intervals varyingfrom one to four. The reason for this experimentaldesign was to give the infant the opportunity to learnand recognize a stimulus and to notice differences be-tween at least a face and the other ones while main-taining the infant’s attention by changing stimuli (themother face was not used in order to avoid any social or

1

Data

atalsymptoms Neurological signs (at 2 months of age)

tion, majoracorporeal circulationn for 60 h

Mild peripheral hypertonia

Peripheral hypertonia, left dominanceNormal axial tonus

hord prolapse. Axial hypotoniaPeripheral hypertoniaAxial hypotoniaMild peripheral hypertoniaMild peripheral hypertonia

Normal

LE

al

eone/

alaxtrtio

nsal c

emotional behavior). The faces were projected onto a

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translucent 19-cm-high 3 24-cm-wide rectangularscreen mounted on a transparent arm, placed at 35 cmfrom and making a 50° angle with the infant’s faceplane. The size of the projected faces was 12 3 7.8 cm(subtending a visual angle of 12° 40 in. in width).Eighty slides were charged in the projector carousel,slides being presented at a rate of one every 4 s, eachslide being presented for 4 s.

The other visual stimulus consisted in an assemblyof diodes inserted at 2 cm from the upper edge of thescreen vertical axis (see Fig. 1). Four red diodes werearranged in square within a 18-mm diameter circle of12 green diodes, the diode circle center being at 35 cmfrom the infant’s eyes and subtended a 3° visual angle.Pairs of diametrically opposed diodes were successivelylit up at a frequency that was varied by the experi-menter every 4 s (ranging from 100 to 0.2 Hz) so thatchanges in visual stimulation were equally frequent inthe two situations. The luminances of the face stimuliand of the diode stimuli were measured by means of alux meter at the distance of the infant’s eyes. A uniformluminance filtering slide was used during the diodecondition to match the screen luminance of the twoconditions.

Image Acquisition

A tiny catheter was introduced in the infant’s rightfoot at least 1 h before they were comfortably placed inthe PET camera. When the infant was quiet and atten-tive, according to classical criteria of eyes opening anddirection of gaze, stimulus presentation was started,the fixation of which maintained the infant’s head im-mobile.

About 30 s after stimulus presentation started, 15O-labeled water was injected (0.25 mCi/kg). A 2-min-longseries of 10-s-duration scans was acquired in each con-dition, using an ECAT-953B PET camera (Siemens,Erlangen, Germany). During image acquisition an ex-perimenter could watch the infant head and eyes with-out being seen by the infant. No visible eye and headmovement were observed, due to the small size of thestimuli and to the fact that only the stimuli were vis-ible for the infant.

Upon completion, a single 80-s-duration image wasreconstructed for each stimulus condition, startingfrom the radioactive tracer arrival in the brain.

Right after PET scanning, anatomical images wereacquired on a Signa 0.5-T magnet (MRMAX, GeneralElectric, Buc, France) as series of 3- or 10-mm-thickT1-weighted contiguous axial slices after the childrenwere orally given a preparation of chloral.

Image Analysis

Since infants were alert and unable to stay immobilefor 10 min during the PET session, we could not mea-

sure the attenuation correction factors (ACF) required

for emission scan correction, except for two infants whofell asleep. Consequently, attenuation correction wasperformed using a manufacturer-designed algorithmbased on predefined ACF values and the outline of theinfant brain as assessed on emission scan. Because ofdifferences in bone density between 2-month-old in-fants and adults, ACF to be applied to infant PETimages were estimated thanks to the transmissionscans acquired from the two children who fell asleep(ACF 5 0.095 cm21 for both the brain tissue and thesoft cartilaginous skull layer). Head outer edge wasdefined using the individual PET emission sinogramderived brain outer edge, to which was added an aver-age skull thickness of 5.1 mm as measured from theinfant MR images.

The two attenuation corrected PET scans of eachsubject were then coregistered, initializing the processwith the multiparametric imaging tool (Pietrzyk et al.,1990) (MPI tool) interactive software, pursuing withthe automatic AIR procedure (Automated Images Reg-istration (Woods et al., 1997)). The transformation ma-trices of both algorithms were combined in order tobring the first PET image within the same coordinatesas the second one. AIR was also used to calculate aPET-to-MRI coregistration matrix for each infant.

PET image stereotaxic normalization, required forintersubject averaging, was then performed. The high-est quality MRI of the infants, reoriented in the Ta-lairach space, served as a template. Each child’s MRIwas registered and warped onto this template usingAIR, the same transformations being applied to hisPET images after coregistration to his MRI volume.Each PET raw count volume was further normalizedby global scaling.

Finally, faces minus diodes difference volumes wereaveraged over the six children. This averaged differ-ence image was filtered (final image smoothness 11mm) and scaled by its standard deviation (SD). A 3Dregion growing algorithm helped to segregate 3D clus-ters showing normalized regional cerebral blood flow(NRCBF) increases larger than 2 SD (P , 0.05, uncor-rected). Center of mass coordinates, volume, and aver-age NRCBF variation were computed for each cluster,retaining only those having volumes larger than 144mm3 (10 voxels). The selected clusters were then su-perimposed onto the infant MRI template for anatom-ical labeling.

RESULTS

Comparison of brain activity maps during face per-ception and diodes fixation revealed that 2-month-oldinfants activated a network of areas (see Table 2, Fig.1), including in particular an area located within theinferior temporal gyrus nearby the occipitotemporalsulcus. This activation was predominant in the right

hemisphere (activation was detected at the left hemi-

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sphere at a similar location, but its volume did notreach the threshold for significance). Besides this rightinferior temporal gyrus focus, this network includedbilateral inferior occipital and parietal areas. More-over, one should note that the left inferior frontal andsuperior temporal gyri were activated during face pro-cessing.

DISCUSSION

The main finding of the present study is that2-month-old infants activated a network of areas be-longing to the core system for face perception identifiedin adults (Haxby et al., 2000). In particular, the acti-vated area located within the inferior temporal gyrusnearby the occipitotemporal sulcus is very likely to bethe homologue of the adult fusiform face area (FFA)defined by Kanwisher (Kanwisher et al., 1997; Gau-thier et al., 2000a). As a matter of fact, despite existingdifferences between 2-months-old infant and adultbrain anatomy, the anatomical location of the inferiortemporooccipital activation focus in infants was veryclose to that of the FFA as reported in Kanwisherseminal paper (Kanwisher et al., 1996). Interestingly,the adult FFA, more active during processing of facesthan of any other object (for review see Table 3 and Fig.2), is at the center of a debate. Some authors considerthat it is specialized for faces (Kanwisher, 2000) while

TAB

Brain Areas Activated on Average iduring Face Processing C

Anatomical localizationDiodes condition

NRCBF (SD)

FrontalL inf frontal gyrus 67.0 (16)L inf frontal gyrus, orbital part 64.9 (10)R mid frontal gyrus, orbital part 77.6 (21)R medial superior frontal 56.5 (16)R median cingulate 103.4 (8)R ant cingulate, orbital part 83.4 (16)

Occipital and temporalL sup occipital 105.0 (14)R sup occipital 112.5 (16)L inf occipital/middle temporal 61.7 (22)R inf occipital/middle temporal 106.2 (10)L sup temporal 100.9 (8)R sup temporal 107.5 (12)L inf temporal 55.4 (17)R inf temporal gyrus/fusiforma 87.2 (12)

ParietalPrecuneus 110.7 (14)R inf parietal 105.1 (17)

Note. For each activated area, the table gives its anatomical locatioMRI that was used as a template), the normalized regional cerebraland the average NRCBF variation amplitude during face processing

a The activated area homologue to the adult fusiform face area.

others think that it is domain general and related to

the acquisition of expertise in object discrimination(Gauthier et al., 1999, 2000a,b; Tarr and Gauthier,2000). Within this debate, one could argue that evi-dence of FFA activation in infants, as early as 2months of age, provides a developmental argument forthe domain specificity of this region, since faces is thefirst perceptual category of complex objects with whichan infant becomes an expert at. However, since facesconstitute the dominant visual stimulus to which in-fants are exposed during their first 2 months of life,FFA activation at 2 months could as well reflect theinfants general expertise in object discrimination. Nev-ertheless, it can be assumed that it is related to indi-vidual face processing rather than facedness recogni-tion inasmuch as it has been shown that in 12-weekinfants facedness can be categorized by either hemi-sphere despite a lack of interhemispheric coordination(de Schonen and Bry, 1987). In addition, a recent studyin adult has shown that while the right FFA supportsindividual face matching based on internal configura-tion, its left hemisphere homologue is involved inmatching face parts (Rossion et al., 2000). This is con-sistent with behavioral data in 4- to 10-month-old in-fants showing a right-hemisphere advantage in facerecognition (de Schonen and Mathivet, 1990; Deruelleand de Schonen, 1998). As previously proposed (deSchonen and Mathivet, 1989), the right hemisphere

2

Group of Six 2-Month-Old Infantspared to Diode Fixation

Faces–diodes NRCBFincrease (%)

Activatedvolume (mm3)

12.8 79213.7 67213.5 60213.1 165613.3 80612.1 182

12.5 41815.2 67712.4 18213.1 15414.4 240413.2 48914.8 30812.6 224

12.4 25912.4 201

ased on the identification of major sulci and gyri on one of the infantd flow (NRCBF) in the area during the diodes condition, its volume,, left; R, right; inf, inferior; sup, superior; mid, middle.

LE

n aom

n (bbloo. L

advantage of the face area in adults (Gauthier et al.,

e bo

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1999) might then well be related to its earlier func-tional maturation.

We know from anatomical (Brody et al., 1987) andmetabolic studies (Chugani and Phelps, 1986; Chuganiet al., 1987) on human cerebral maturation that at theage of 2 months the most myelinated and highest met-abolic areas are located within subcortical structuresand primary cortices, while the temporal cortex as awhole shows a low metabolic activity. In such a region,poorly mature at the age of 2 months, the synaptic

FIG. 1. Network of areas active during face processing as compaareas (orange) are superimposed on a series of transaxial structuralselected anatomical landmarks: anterior limit of the occipital lobeidentification of these anatomical landmarks was obtained on the tdrawing in any incidence. These and other landmarks were used tocorresponding in the left hemisphere to Broca’s area in adults (pinkwere used for activation anatomical labeling. The graph gives for eacduring the diode and face conditions in the cluster enclosed in the blu

density is far below the adult level and far from its

peak (Huttenlocher and Dabholkar, 1997). UsingNRCBF during the diode condition as an index, wecompared the cerebral blood flow values of the rightFFA cluster with that of the right precentral region.This region is known to have high glucose metabolism(Chugani et al., 1987) and myelination (Brody et al.,1987) at this age and can thus be considered as rela-tively mature. In order to do so, we identified the pre-central and postcentral sulci and manually defined onthe MRI template the precentral region. Normalized

to fixation of diodes in a group of six 2-month-old infants. Activatedes taken from an infant MRI brain template. Colored ticks indicateck), rolando sulcus (red), and occipitotemporal sulcus (green). The

plate brain with a software allowing a 3D reconstruction and sulciw structural volumes of interest, such as the inferior frontal gyrusiddle frontal gyrus (yellow), and superior frontal gyrus (white) thatfant the variation of normalized regional cerebral blood flow valuesxes that corresponds to the adult fusiform face area. L, left; R, right.

redslic(blaemdra

), mh in

cerebral blood flow of the right FFA was found 30%

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lower than that of the precentral gyrus (right FFA,87 6 12; right precentral gyrus, 123 6 8, P 5 0.003;paired t test, 5 df ). This result can be taken as anindication that the metabolic maturation of this regionlevel was lower that that of the precentral gyrus. Oneshould note that the comparison of these blood flowvalues was undertaken in the diode condition. Thesame comparison during the face condition showed asimilar trend, the activated right fusiform area stillhaving lower NRCBF values than the precentral gyrus(right FFA, 104 6 13; right precentral gyrus, 119 6 6,P 5 0.07; paired t test, 5 df ).

Therefore, a major finding of the present study isthat, despite a low level of metabolic activity, thisvisual associative cortex shows some relatively special-ized functional activity. This demonstrates that func-tional maturation does not require metabolic and ana-tomical maturation completion in the involved cortical

FIG. 2. Comparison of FFA locations reported in the literaturelocations described in the stereotaxic space are displayed on the axiaMNI template, corresponding to the mean coordinates of the FFA actlocation defined in a single subject on one of his axial brain MRI slicthe present study superimposed on the template MRI of a single 2-moactivation during face matching defined in a single subject and diActivated fusiform gyrus area detected in the present study in the s

areas. It indicates the anteriority of functional matu-

ration which might proceed simultaneously in severalconnected and active cortical regions. This hypothesisis consistent with the idea that synaptic stabilization isa crucial aspect of neural specialization (Changeux,1983).

Besides FFA, face perception by 2-month old infantsactivated a bilateral inferior occipital area correspond-ing to the occipital face area previously identified inadults as involved in early perception of facial features.Both this region and the FFA belong in adults to thevisual analysis of faces core system, as defined byHaxby, which also includes the superior temporal sul-cus (STS) that is consistently activated in adults (Ser-gent et al., 1992; Puce et al., 1996; Kanwisher et al.,1997; Chao et al., 1999a,b; Hoffman and Haxby, 2000;Haxby et al., 2000). Interestingly, the latter region wasnot activated in 2-month-old infants, consistent withits putative functional role in the adult brain, namely

th in stereotaxic space and in single subjects. Metanalysis of FFA40 mm, a) and sagittal (253 mm, d) slices on the SPM single subjecttions; white dots correspond to the extrema listed in Table 3. (b) FFAanwisher et al., 1996). (c) Activated fusiform gyrus area detected in-old infant, in the same incidence as b. (e) Location of the right FFAyed on one of his brain MRI sagittal slice (Clark et al., 1996). (f)e incidence as e.

, bol (1ivae (Knth

splaam

to respond to changeable aspects of faces, perception of

460 RAPID COMMUNICATION

gaze, and lip expression (Haxby et al., 2000). In thepresent study, the use of static and neutral faces mayhave led to the absence of recruitment of this region.Alternately, STS is an integrative multimodal areathat will develop later on and thus was not to be ex-pected to be involved at such an early stage of cognitivedevelopment.

We also observed a right inferior parietal activation,nearby the intraparietal sulcus (Fig. 1). In reference towhat is known in adults, this region belongs to theextended face processing system (Haxby et al., 2000)that, within this system, supports spatially directedattention.

Finally, as opposed to adults, face processing in2-month-old infants appears to recruit what will be-come later their language network, namely the leftinferior frontal and superior temporal gyrus. We pro-pose that coactivation of the face and this future lan-guage networks sustains the facilitative effects of so-cial interactions, such as looking at the mother’s face,on language development (Locke, 1997).

ACKNOWLEDGMENTS

The authors express their gratitude to Anne Bore, Marie Arnaud(Hopital Robert Debre), Monique Crouzel, Bernadette Bruck, and theCyclotron staff of the Service Hospitalier Frederic Joliot (CEA, Or-say) where the PET experiments were carried out; to Uwe Pietryzk(Research Center of Juelich, Germany) and Olivier Quinton (GIN,Caen) for their help in data analysis; and to Petros Tzourio for hisassistance in preparing the manuscript. This work has been sup-ported in part by a grant from the Ministere de la Recherche, “Sci-

TAB

Review of the Fusiform Face Area Extremum in the ClustePapers Giving Their Results in the Stereotaxic Reference Spay 5 253 6 10, z 5 220 6 7 (mm))

Publications Task

Puce et al., 1996 Faces perception Lette

Dolan et al., 1996 Faces mental imagery FixaDolan et al., 1997 Faces specific learning effectChao et al., 1999a Faces perception Hous

Hoffman and Haxby, 2000 Faces perceptionScraPictu

Chao et al., 1999b Faces perception AnimMcCarthy et al., 1997 Faces among objects perceptionNakamura et al., 2000 Faces perception Fixa

Rossion et al., 2000 Faces perception Obje

Kanwisher et al., 1997 Faces perception ObjeIshai et al., 1999 Faces perception HousGauthier et al., 2000b Faces perception BirdGauthier et al., 1999 Faces perception GreeKim et al., 1999 Recognize novel faces Reco

ences de la Cognition.”

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