Sciencee

How Learning to ReadChanges the CorticalNetworks for Visionand Language

Stanislas Dehaene, Felipe Pegado,Lucia W. Braga, Paulo Ventura,Gilberto Nunes Filho, Antoinette Jobert,Ghislaine Dehaene-Lambertz, Regine Kolinsky,Jose Morais, Laurent Cohen

3 December 2010

Volume 330, PP.1359-1364

How Learning to Read Changesthe Cortical Networks for Vision.and Language5tanislas Dehaene/,2,3,4* Felipe Pegado/,2,3 Lucia W. Braga,S Paulo Ventura,6Gilberto Nunes Filho, S Antoinette lobert,l,2,3 Ghislaine Dehaene-Lambertz,l,2,3Regine Kolinsky/'s lose Morais/ Laurent (ohen9,10,l1

Does literacy improve brain function? Does it also entail losses? Using functional magneticresonance imaging, we measured brain responses to spoken and written language, visual faces, houses,tools, and checkers in adults of variable literacy (10 were illiterate, 22 became literate as adults, and31 were literate in childhood). As literacy enhanced the left fusiform activation evoked by writing,it induced a small competition with faces at this location, but also broadly enhanced visual responsesin fusiform and occipital cortex, extending to area VI. Literacy also enhanced phonological activationto speech in the planum temporale and afforded a top-down activation of orthography fromspoken inputs. Most changes occurred even when literacy was acquired in adulthood, emphasizingthat both childhood and adult education can profoundly refine cortical organization.

Practically all adult neuroimaging experi-ments are performed in highly educatedcollege students. The observed brain archi-

tecture therefore reflects the influence of cultureand education over and above spontaneous braindevelopment (1, 2). Indeed, the acquisition ofreading, a major event in children's lives, is nowrecogrlized as capable of changing both brainanatomy (3, 4) and brain activation (5-9). In theauditory modality, literacy leads to phonemicawareness, the ability to manipulate the smallestunits of spoken language [i.e., phonemes (10)],and alters online speech processing (Il-14). Atthe visual level, developmental neuroimagingstudies in normal and dyslexic children showthat, with reading acquisition, a specific brain sitein left occipito-temporal cortex, which has beentermed "visual word form area" (VWFA), startsto respond to orthographic stimuli in the learnedscript (15-19).

These observations leave many importantquestions unanswered. First, does literacy primar-ily lead to cooperative or to competitive effects

'INSERM, Cognitive Neuroimaging Unit, Gif sur Yvette 91191,France. 'Commissariat a l'Energie Atomique, Direction desSciences du Vivant, 12BM, Neurospin center, Gif sur Yvette91191, France. 3University Paris-Sud 11, 9140S Orsay, France.'College de France, 11 Place Marcelin Berthelot, 7S00S Paris,France. 'SARAH Network-International Center for Neurosciencesand Rehabilitation, OL 13, Lago Norte, 71.535-005 Brasilia, DFBraziL6Facultyof Psychology, Universityof Lisbon, 1600-214 Lisbon,PortugaL 'Faculty of Psychology, Universite Libre de Bruxelles(ULB),1050 Brussels, Belgium. BFondsde la Recherche Scientifique(FNRS), 1000 Brussels, Belgium. 9Unive~ite Pierre et Marie Curie-Paris 6, Facutte de Medecine Pitie -Salpetriere, 75013 Paris, France.lOAssistance Publique-+i6pitaux de Paris, Groupe hospitalier Pitie-Salpiitriere, Department of Neurology, 75651 Paris, France. "INSERM,Centre de Recherches de l'lnstitut du ceM'au et de Ia moelleepiniere, UMRS975, Paris, France.

'To whom correspondence should be addressed. E-mail:sta nislas. de ha ene@gmail.com

on cortical processing? Two theoretical positionscan be contrasted. The first view, derived fromanimal studies of environmental enrichment andsensory plasticity, emphasizes that perceptuallearning entails beneficial modifications of cor-tical maps, including sharpened receptive fieldsand neuronal tuning curves correlated with be-havioral improvements (20-22). Without denyingthese positive effects, the second view empha-sizes that reading is a cultural invention too re-cent to involve dedicated genetic or developmentalmechanisms. Thus, during education, reading pro-cesses must invade and "recycle" cortical spacedevoted to evolutionary older functions, openingthe possibility that these functions suffer as read-ing expertise sets in (2, 23). Much like expertisefor nonface stimuli induces a reduction in face re-sponses (24-26), reading, which recruits an iden-tical cortical site in all cultures (27), might entaila reorganization of nearby responses to faces,

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houses, and objects. We thus sought to under-stand which of these stimuli are processed in theVWF A area before reading and how their corticalrepresentation, which gets refined during theschool years (28), is affected by literacy.

A second issue is that, at present, most func-tional imaging studies of illiteracy only contrastedschooled versus unschooled adults. Because thesestudies did not include "ex-illiterate" adults whodid not attend school but learned to read duringadulthood, they confounded the effects of school-ing and literacy. The only important exception (4)focused solely on how brain anatomy is changedby literacy. In this study, we separated the func-tional effects of schooling and literacy by compar-ing illiterates, ex-illiterates, and adults schooledin childhood.

Populations studied and verification of literacylevel. We scanned a total of 63 Portuguese andBrazilian participants. Our sample included 32 un-schooled adults (10 illiterates and 22 ex -illiterateswith variable reading skills), and 3 I schooled andliterate adults. The latter group included I) lit-erate subjects matched to the illiterates in socio-economic status (SES) (29). Reading skills wereverified through behavioral tasks of letter identi-fication, word and pseudo-word reading (with orwithout speed pressure), and sentence reading(Fig. I, fig. S I, and table S I). All tests revealedthe same ordering of literacy, from Brazilian il-literates (ILB) to Portuguese ex-illiterates (EXP),Brazilian ex-illiterates (EXB), low-SES Brazilianliterates (LB2), Portuguese literates (LP), and Bra-zilian literates (LB I). We therefore relied on whole-brain linear regressions with reading performance(number of stimuli read per minute) across allgroups to identifY the brain regions influenced byliteracy. Once identified, each brain site was sub-mitted to restricted comparisons of subgroups toevaluate the effects of schooling and literacy withmaximal sensitivity (29).

We used three types of whole-brain functionalmagnetic resonance (fJ\1RI) runs: a "localizer" withhorizontal and vertical checkerboards, written and

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- Literates (LB1) -1_ Literates (LP)

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Fig. 1. The six groups of participants and their reading skills. Box plots show (A) the speed and(8) accuracy in reading a list of pseudowords (central horizontal line, median; box, 25th and 75th per-centiles; whiskers, minimum and maximum), Additional data on word and sentence reading are providedin fig, 51.

spoken sentences, motor commands, and calcu-lation problems (fig. S2); three visual runs eval-uating cortical responses to faces, houses, tools,letter strings, false fonts, and moving checker-boards, while the participant focused on detectinga target star (fig. S3); and four auditory lexical-decision runs with spoken stimuli. To verifYcom-pliance, dwing the localizer, participants eitherheard or saw short verbal instructions to performsimple calculations or to click the left or rightbutton. With spoken instructions, we observedclassical regions for calculation and hand move-ments, without modulation by literacy, indicat-ing similar comprehension and compliance in allgroups. With written instructions, however, acti-vation at the same locations was strongly modu-lated by reading performance, varying from zeroactivation in illiterates to a level equivalent tospoken instructions in literates (see fig. S4). Whileunsurprising, these results validate our group def-initions and literacy measure and establish that,with spoken materials, all groups followed instruc-tions quite well. Thus, any subsequent differencescannot be attributed to lower attention or compre-hension in illiterates.

Responses to written sentences enhanced byliteracy. We first examined, in the localizer run,which regions were modulated by reading per-formance during the viewing of simple sentencesconsisting of serially presented written words (Fig.2 and fig. S7). A massive effect was seen in theleft ventral occipito-temporal cortex, at classicalVWFA coordinates (-40, -50, -14, Z score = 6.86);with posterior subpeaks (-46, -70, -18, Z = 5.39;-32, -80, -8, Z = 3.96); and at a right occipitalsite (22, -86, -10, Z= 5.17). These regions werestrictly visual, as attested by their lack ofactivation to spoken sentences. Modulation byreading performance was also seen in a vast left-hemisphere language network, which was alsoactivated by spoken language in all groups: leftposterior, middle, and anterior superior temporalsulcus (STS; -50, -44, 6, Z= 7.10; -54, -12, -12,Z = 5.42); left temporal pole (-50, 12, -24, Z =4.13); left and right pr=otor cortex (-46, -2, 52,Z = 8.50; 46, 4, 40, Z = 5.48); left inferior frontalgyrus (-54, 26, -6, Z = 5.76); and left supple-mentary motor area (-4, 2, 62, Z = 6.33). A sig-nificant left-hemispheric asymmetry of this effectwas observed in all areas except temporal poleand occipital cortex. Direct comparison of spokenversus written stimuli showed that, in the literateparticipants, frontal regions became equallyactivated by spoken versus written language,whereas temporal areas overlapped but still showeda significant difference favoring spoken language(fig. S8).

This analysis thus uncovered three simple ef-fects: with the acquisition of literacy, written ma-terials (i) activate right occipital cortex at thesame level as checkerboards; (ii) induce a strongactivation in left ventral visual cortex, at the clas-sical site of the visual word form area (VWFA);(iii) gain access to left perisylvian temporal andfrontal language areas.

Left superior temporal sulcusResponse at [-50, -44, 6] Response at [-50,12, -24]

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The visual word form area: A major correlateof literacy. Our next analyses focused on visualresponses in the VWFA. The effect of readingperformance on occipito-temporal cortex dwingsentence reading was replicated when passiveviewing of letter strings was contrasted to rest[main peak = -46, -80, 4, Z = 5.75; subpeaks at-40, -70, -12, Z= 4.50; and the VWFA proper,-46, -58, -10, Z = 4.11; right occipital region,24, -86, -10, Z = 5.25, corrected P < 0.05 byfalse detection rate (FDR) analysis (29)]. In thispart of the experiment, which involved viewingmeaningless pseudowords during an easy target-detection task, only these visual regions weremodulated by literacy, confirming their role inautomatic orthographic coding (J 6). Notably, theimpact of schooling on the VWFA was replicatedwhen the illiterates were compared with thematched low-SES literates (ILB < LB2), both forwritten sentences versus rest (-40, -50, -14, Z=6.77) and strings versus rest (-48, -60, -10, Z =

3.54). The VWFA was also identified when wesearched for activation positively correlated withreading performance within the unschooled par-ticipants only (illiterates and ex-illiterates; sen-tences versus rest: -42, -54, -6, Z = 6.25; strings

VWFAResponse at [-44, -50, -14]

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OccipitalResponse at [22, -86, -10]

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versus rest: -48, -56, -6, Z = 3.53). This findingindicates that adult literacy suffices to establish anincreased VWFA response to orthographic pattems.

Literacy not only amplified letter string re-sponses, but also increased the cortical selectivityfor this category relative to others. When we testedthe impact of reading performance on the differ-ence between letter strings and other visual cate-gories, only the VWFA appeared (peak at -44,-56, -14, Z= 5.00; subpeak -44, -68, -12, Z=3.85). This effect showed a highly significant hemi-spheric asymmetry, peaking at the classical VWFAcoordinates (-44, -56, -12, Z = 5.07). Thus,literacy results in the emergence of a cortical siteincreasingly more responsive to writing than toother visual categories (J 7, 30).

Group analyses left open the possibility of aselective but spatially variable response to writtenstrings in every subject. Literacy would then merelydisplace this response to a reproducible site, with-out changing its amplitude. This possibility wasrefuted, however, through an individual analysisin which the voxel most responsive to writtensentences versus checkerboards was first identi-fied in each participant, within 10 mm of thegroup peak (similar results were obtained with 20

Left frontal

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Fig. 2. Effects of literacy on brain responses to written sentences during the localizer. Axial andsagittal slices show voxels where activation was modulated by literacy during exposure to writtensentences relative to rest (voxel P < 0.001, cluster P < 0.05 corrected). Colored labels refer toparticipant groups and are ordered according to reading performance (see Fig. 1). Plots reportactivation to visual checkers, spoken and written language relative to rest in the localizer run, inarbitrary units (mean ± 1 SE). To avoid circularity, we generated plots solely from the spoken andwritten commands data, which were independent from the voxel-selection criterion.

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Fig. 3. Effectsof literacy on visual responses todifferentcategoriesofstimuli.(A)Visualresponsesin theWJFA.(Inset)Statisticalparameter map (SPM)map ofmodulationby literacyof activationto writtensentencesin the localizerI,p < O.DOLclustercorrectedP < 0.05).Plotshowingactivationin the independentvisualrunsatthe isolatedpeak (mean± 1 5E).Activationincreasedinresponseto letterstringsI,p = 0.005) and decreasedforcheckerboardsI,p = 0.013) and, to a lesserextent,forfaces(overallP = 0.09, ILL> LB2,P = 0.003).(8 and C)SPMmaps(voxelP < 0.D01uncorrected)and peakplotsshowing increases with reading performanceof faceresponsesin right anterior fusifonn,and of house re-sponsesin bilateralparahippocampalregions.(D)SPMmap of enhancement by literacyof the response towrittensentencesin lateral ocdpital cortex(inset,P <0.D01,clustercorrectedP < 0.05), and plotshowingitsreplicationin response to other visual categories.(E)Modulationby literacyof the greater responseto hor-izontalthan to verticalcheckerboardsin primaryvisualcortex(inset,voxelP < 0.001 uncorrected).In (B), (0,and (El,plotsare providedfor illustration,becausetheydo not arise from independent data; plots !..IV and (D)are from independentdata.

or 40 nun), and then analyzed for its responses tostrings and false fonts in the independent visualruns. We observed a significant lateral~to-mesialshift of the word~responsive peak (from x = -48in illiterates to -46 in ex-illiterates and -44 in lit-erates, p= 0.006), but its activation to strings alsoincreased strongly with reading performance (linearregression, ,J- = 46.5%, P < 0.0001), as did theselectivity index for strings relative to false fonts(P= 0.001). Thus, literacy genuinely increases boththe strength and specificity of cortical responsesto the learned script in the VWFA.

We also searched for nonrnonotonic effectsacross our six groups, which might arise if the ex-illiterates had to mobilize a broader network thaneither literates or illiterates in order to read. Indeed,during sentence reading, Brazilian ex-illiteratesshowed greater activity than Brazilian literates inbilateral mesial fusiform areas (-34, -60, 0, Z =

5.34; 38, -50, -2, Z = 4.54) and right posteriorparietal cortex (24, -62, 38, Z = 4.70; 12, -58,60, Z = 4.16) (fig. S5). Thus, to achieve theirmodest reading performance, ex-illiterates enga-ge a broader and more bilateral ventral networkthan literates and recruit additional posteriorparietal regions associated with serial effortfulreading (31). This observation is similar to thedevelopmental finding that reading in youngchildren initially involves a broad bilateral visualnetwork (18) that progressively restricts to theVWFA as greater expertise sets in (19).

Competition with other visual categories inocopito-temporal cortex. At the peak coordi-nates of the VWFA (-44, -50, -14, identified bythe localizer), analysis of the independent visualruns showed a strong response to strings but alsoto other visual categories, particularly faces andtools (Fig. 3). This fmding confirms that this areaplays a broad role in visual shape analysis. Read-ing being a recent invention, we expected thatwritten words would not activate a fully dedi-cated cortical site but would only partially "re-cycle" existing cortical mechanisms for visualrecognition (2, 23), inducing a cortical competi-tion that would increase with reading expertise.We tested the predicted cortical competition bysearching for a decreasing response to visual stimu-li with increasing reading performance. At the in-dependently defined VWFA peak, the responsesto checkerboards slightly diminished with read-ing performance, both across all groups (linearregression, P= 0.013), for illiterates compared toall other groups (P = 0.025), and for illiteratescompared to SES-matched literates (ILB > LB2comparison, P = 0.039). For houses and tools,only marginal decreasing trends were found (samethree tests, P = 0.08, 0.025, 0.09 for houses and0.13, 0.025, 0.06 for tools). For faces, the de-creasing tendency was stronger: The regressionwith reading performance across all participantswas marginal (P = 0.09), but the more focusedcomparisons were significant (ILB > other groups,P = 0.025; ILB > LB2, P = 0.003). Comparingilliterates with SES-matched literates indeed argu-ably provides a purer test, controlling for the pos-

RESEARCH ARTICLE Isibility that frequency of exposure to faces mightincrease with socioeconomic status and influencefusiform responses (32). When studied at the whole-brain level, the ILB > LB2 contrast indicated ahighly significant reduction offace response withliteracy (P < 0.00 I, cluster P < 0.05 corrected) intwo bilateral posterior fusiform clusters (right 40,-80, 0, Z = 5.93, with an anterior subpeak, 38,-50, -12, Z = 4.70; left, -44, -70, -12, Z =4.58, with a subpeak precisely at the VWFA, -42,-54, -14, Z= 3.91).The same contrastdid not reachcorrected-level significance for houses or tools.

In summary, at the VWFA site, learning toread competes primarily with the cortical repre-sentation of checkers and faces. Further analysesshowed that this competition was spatially re-stricted. We implemented analyses inspired byGolarai et al. (28), who showed that cortical peakswith adult-like selectivity to faces and places al-ready exist in 7 to II year olds and, with increas-ing age, progressively expand into the surroundingcortex. For each subject, we fIrst searched forthe peak response to faces versus houses within10 nun of the group coordinates of the VWFA.We then examined an orthogonal regression test-ing how the activation to faces varied with liter-acy, at the peak and in increasingly larger annuliof 2, 4, 6, or 8 voxels surrounding it (fig. S6).There was no change in peak face responses withreading performance (P = 0.47), nor in annuli ofradius 2 or 4, but in the more distant annuli ofradius 6 or 8, face activation decreased with read-ing performance (regression across all groups, re~spectively P = 0.037 and P = 0.015). Similarfindings were obtained for the individual peak ofresponsitivity to houses versus faces: no changein peak activation (P = 0.20), but a decrease inhouse-driven activation in the larger annulus ofradius 8 (P = 0.045). For tools, a category forwhich no selective region exists in ventral visualcortex (33), we did not fmd an annular reduction,but a more diffuse reduction in activation withreading performance, significant over both a largesphere of 16 mm (P= 0.039) and in the 50 voxelsbest responsive to tools versus houses (P= 0.019),but again not at the peak itself (P = 0.27).

Overall, our results indicate that the develop-mental competition induced by the expansion oforthographic representations in the ventral visualsystem is modest, does not directly affect thepeak responses to faces and houses, but interfereswith their expansion into the surrounding cortex.These conclusions fit with previous studies of visualdevelopment (28), expertise (24, 25), and plasticityof sensory maps (20), which reveal a displacementof map boundaries due to cortical competition.

Positiveeffectsof literacyon visual organization.Competition could also have a positive effect oncortical responses to non-reading-related visualcategories: By reducing the dispersion of theirneural responses, it might force them to a moreconsistent cortical site. Indeed, a whole-brainsearch revealed positive correlations of readingperformance with face and house responses inventral occipito-temporal cortex (Fig. 3). Reading

performance modulated positively the face-versus-rest contrast in the right anterior fusiform gyrus(38, -42, -20, Z = 4.84, FDR) and induced asignificant right-hemispheric shift offace responsesin occipito-temporal cortex (24, -88, -10, Z =8.02; 36, -62, -12, Z = 6.72; and 38, -40, -22,Z = 4.77, FDR). Similarly, reading performancemodulated the house-versus-rest contrast in bi-lateralmesial fusiform and parahippocampal regions(peaks at 34, -58, -12, Z= 5.19; 24, -36, -16, Z=4.83), with a right-hemispheric asymmetry (36,-60, -12, Z = 5.53). Altogether, these inflnenceson word, face, and place responses resulted in abetter differentiated mosaic of category-specificregions in ventral visual cortex in literates (Fig.4). Notably, however, face and house increaseswere found neither when we compared illiterateswith their SES-matched literate group (lLB <LB2 comparison), nor when we tested for theeffect ofliteracy in nonschooled participants only(table S2). Plots showed that these effects differ-entiated the participants living primarily in urbanareas (LB I, LP, and to a lesser extent, EXP) ver-sus those living in rural areas (ll.B, EXB, andLB2), regardless of their schooling and readingscores (Fig. 3). Although these observations sug-gest an influence of familiarity rather than literacyor schooling per se, they are nevertheless impor-tant in showing how ventral fusiform organizationcan be affected by cultural variables (1).

Literacy led to another effect: a general en-hancement of occipital responses. We probed theright occipital location identified as being modu-lated by reading performance during written sen-tences versus rest in the localizer run (coordinates22, -86, -10). During the independent visualruns, the activation of this region to every visualcategory correlated positively with reading scores,with the lowest correlation achieved with thecheckerboards (? = 0.08, P = 0.02; all other cat-egories, ? ranging from 0.17 to 0.22, P < 0.0007).Furthermore, these effects were genuinely relatedto literacy, not just schooling (table S2). Whenextended to a whole-brain search, with a maincontrast for increasing activation to all visual cate-gories, this effect was significant not only in rightoccipital (24, -84, -10, Z = 14.6) but also in leftoccipital cortex (-48, -80, -4, Z = 9.35) and aright occipito-parietal cluster (24, -76, 36, Z =6.75), always with significant right-hemisphericasymmetry. Thus, literacy enhanced occipital re-sponses to essentially all the contrasted black-and-white visual stimuli used in our study.

We also examined whether early retinotopicresponses were affected. The localizer comprisedhorizontal and vertical checkerboards, designedto isolate the meridians of early visual maps. Inthe Roman alphabet, words appear as horizontallyextended strings, and expert readers show en-hanced behavioral processing of letter stringspresented at the familiar foveal and horizontallocation (31, 34). We therefore predicted thatliteracy might increase the responses to horizon-tal relative to vertical checkerboards. Indeed, thiseffect was observed at two symmetrical occipital

sites corresponding to primary visual cortex (16,-88, 2, Z = 5.10; and -12, -88, 2, Z = 4.75,FDR). These sites exhibited a strong response tohorizontal, but not vertical checkerboards, andthe modulation by reading performance was seenonly with horizontal checkerboards (Fig. 3). Thiseffect was significantly stronger in left than inright VI (asymmetry effect for horizontal> ver-tical checkerboards, peak at -4, -88, -4, Z = 5.37,FDR). Both occipital sites also showed a positivecorrelation with literacy when written sentenceswere presented (table S2). Overall, these resultssuggest that literacy results in a form of percep-tual learning (20-22) that refines the earlieststage of cortical visual processing. At this stage,learning is generic enough to generalize to checker-board stimuli presented at the trained location. Thegreater effect in left area V I fits with the largerletter-identification span in the right visual fieldin left-to-right readers (35).

Enhanced responses to spoken language.Finally, we examined how literacy affected spokenlanguage processing (Fig. 5). Several regionsshowed a decreasing activation to spoken sen-tences with greater reading performance: left pos-terior STS (-44, -52, 18, Z = 5.45), left and rightmiddle temporal gyri (-66, -22, -10, Z = 5.25;48, -30, -8, Z = 5.34), and midline anterior cin-gulate cortex (4, 42, 42, Z=4.11). These reductions

probably reflect a facilitation of speech compre-hension in literate participants (8). In the con-verse direction, however, activation to spokensentences essentially doubled from illiterates toliterates in left and right superior temporal regionsjust posterior to HescW's gyrus (planum tempo-rale;-38,-28, 18,Z=5.52;42,-14, 16,Z= 5.43),with bilateral subpeaks near HescW's gyrus (-60,-14,10; Z = 4.28; 66, -2, 24, Z = 4.41) and asignificant left-hemispheric asymmetry. The ef-fect was replicated in the independent auditorylexical decision runs, with both words and pseudo-words (correlations with reading performance:? = 0.20, P= 0.0002; and? = 0.18, P= 0.0005).The enhanced temporal response was restrictedto spoken language, with no trace of activation towritten sentences at this site.

The planum temporale is involved in phono-logical coding of speech (36) and is sensitive tothe congruity between a speech sound and a simul-taneous visually presented letter (37), an effect thatis reduced or absent in dyslexic subjects (38). Ourresults make this region a prime candidate for theenhanced phonemic processing that accompaniesreading acquisition [(10-12); see also (39)]. Theyalso suggest that the reduced planum temporaleactivation seen in dyslexic children, rather thanbeing a cause of dyslexia (38), could be a con-sequence of abnormal reading acquisition.

faces

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left hemisphere -24 2'1 right hemisphere 56

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Fig. 4. Mosaic of preferences for different visual categories in ventral visual cortex. Slices at right showthe activation difference between a given category and all the others [for greater comparability betweengroups with different numbers of subjects, the figure does not show statistical t maps, but blood oxygenlevel-dependent (BOLD) signal maps arbitrarily thresholded at 0.66% of the mean BOLD signal overthe whole brain; similar results were seen with t maps]. Graphs at left shows the evolution of the signalrelative to rest for the different categories (mean ± 1SE),at successive cortical sites tracing a horizontalline through the classical coordinates of the VWFA (-42, -57, -12; dotted line).

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During auditory lexical decision, but not sen-tence listening, a second site in left inferiortemporal cortex also increased its activation as afunction of reading performance (-48, -52, -8,Z = 8.62). This site showed no activation in il-literates, but a strong one in all literate groups(Fig. 5). Its coordinates strongly suggest a top-down activation of the VWFA and the neighbor-ing lateral inferior temporal cortex (40). Indeed,its activation to spoken words and pseudowordswas positively correlated to its activation bywritten strings in the independent visual runs (r =

+0.46; no such correlation was found with othervisual categories). Overlap with the VWFA wasalso established by first identifYing the peakresponse to written sentences versus checker-boards in each participant, and then correlatingits activation during spoken lexical decision withthe participant's reading performance (P = 0.005).Altogether, those results confirm that the VWFAcan be activated in a top-down manner duringspeech processing (41--43), even in a lexicaldecision task that does not require orthographicprocessing. Because this activation is presentonly inasmuch as the participants can read, ourfindings suggest that it reflects the recruitment of

an orthographic code rather than a generic picturecode (44).

Previous psycholinguistic research has dem-onstrated that orthography affects spoken lan-guage processing (11-14), but it remains debatedwhether an orthographic code is activated onlinewhenever we hear a spoken word, or whether or-thography merely changes the nature of phono-logical representations (12). Our results show thatboth phenomena coexist: The planum temporaleincrease suggests erihanced phonological coding,compatible with a recent study using low-resolutionelectroencephalography (12), whereas the VWFAactivation indicates an additional and optional or-thographic recruitment.

Effects of early schooling and late literacy.The above fMRI findings are based on globalcorrelations of brain activation with reading per-formance, and therefore reflect the joint influencesof schooling and literacy. To separate these var-iables, we performed additional regression analy-ses on all previously identified peaks (29). Oneanalysis evaluated the impact of literacy acquiredduring adulthood by testing the effect of read-ing performance within unschooled subjects only.Another analysis, conversely, probed the impact

A Modulated activation of Planum Temporale to spoken languageSpoken sentences in localizer Auditory lexical decision

Response at [-38, -28, 18]

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Fig. 5. Effectsof literacy on brain responses to spoken language. (A)SPMmaps of the effect of literacy onthe activation to spoken sentences (left), words and pseudowords (right; voxel P < 0.001, cluster-sizecorrected P < 0.05). Plots show the effect observed in the left planum temporale: Activation to spokenlanguage, words, and pseudowords was doubled or more after the acquisition of literacy (peak selectedusing the localizer run, left panel, and replicated in the independent lexicaldecision runs, right paneD. (B)SPMmaps of the effect of literacy on activations in ventral occipito-temporal cortex to spoken language.Literacymodulated activation to words and pseudowords during auditory lexical decision (right), but notduring mere listening to spoken commands. Plots show the response at the a priori location of the VWFA,as defined by the effect of literacy on written sentences (same location as in Figs. 2 and 3A).

of early schooling by regressing out the effect ofreading performance and testing for a remainingdifferencebetween the Brazilian ex-illiterates(EXB)and the low-SES Brazilian literates (LB2 group),who only differed in early schooling.

The results were clear-cut. Essentially all ofthe above effects of literacy were present in ex-illiterates who learned to read during adulthood(table S2). Such was the case for the increasedVWFA response to letter strings; the capacity toactivate the spoken language network throughreading (except in left temporal pole); the generalvisual increase in right occipital cortex; the greaterresponse of area VI to horizontal checkerboardsand written sentences; and the enhanced planumtemporale and top-down VWFA activation tospoken words and pseudowords. Thus, the neuralmodifications induced by adult literacy educationwere considerable. Furthermore, the vast majoritywere unaffected by early schooling (table S2).There were only two interesting exceptions. Thefirst was the reduced activation to faces in theVWFA, which was indeed particularly prominentin the LB2 group, who benefited from earlyschooling, relative to the EXB group. This findingsuggests that competitive interactions betweenwritten words and faces in ventral visual cortexprimarily occur when reading is acquired inchildhood, a time when visual maps are knownto be highly malleable (28). The other effect ofearly schooling concerned a marginal left pre-motor increase in activation to written sentences.This region overlaps with Exner's writing centerand is thought to code handwriting gestures (45).Whereas early-schooled participants were fluentin handwriting, it is possible that the ex-illiteratesdid not receive enough training to automaticallyactivate a gesture code from the mere vision ofwritten sentences.

We caution that these conclusions may only bevalid for the moderate level of reading fluencyachieved by our ex-illiterate participants. Whetherearly-schooling effects truly reflect a limit on adultsensory plasticity or would vanish with more in-tense reading practice remains an open question.However, our results also indicate that, in liter-ates, most of the observed effects do not changefurther as reading expertise increases (table S2;the only exceptions were increases in planum tem-porale and left pSTS, and reduced VWFA acti-vation to checkerboards). In particular, the VWFAactivation to words and strings increases brisklyfrom illiterates to ex-illiterates and then reachesa plateau uncorrelated with ultimate proficiency,in agreement with developmental evidence thatminimal literacy training suffices to establish itin 6 year olds (18).

Conclusion. Literacy, whether acquired inchildhood or through adult classes, enhances brainresponses in at least three distinct ways. First, itboosts the organization of visual cortices, partic-ularly by inducing an enhanced response to theknown script at the VWFA site in left occipito-temporal cortex and by augmenting early visualresponses in occipital cortex, in a partially retina-

topic manner. Second, literacy allows practicallythe entire left-hemispheric spoken language net-work to be activated by written sentences. Thusreading, a late cultural invention, approaches theefficiency of the human species' most evolvedcommunication channel, namely speech. Third,literacy refines spoken language processing byenhancing a phonological region, the planumtemporale, and by making an orthographic codeavailable in a top-down manner. These largelypositive changes should not hide that literacy, likeother forms of expertise, also leads to corticalcompetition effects (23-26). At the VWFA site, asignificantly reduced activation was found forcheckerboards and faces. The intriguing possibil-ity that our face perception abilities suffer in pro-portion to our reading skills will be explored infuture research.

References a nd Notes1. ). Henrich,S. ]. Heine, A. Norenzayan, Behav. Brain Sci.

33, 61 (2010).2. 5. Dehaene, L. Cohen, Neuron 56, 384 (200n3. A. Castro-Caldas et 01., fur. ]. Neurol. 6, 23 (1999).4. M. Carreiras et 01., Nature 461, 983 (2009).5. K. M. Petersson, C. Silva, A. Castro-Caldas, M. Ingvar,

A. Reis, fur. ]. Neurasci. 26, 791 (2007).6. G. Li et 01., Hum. Brain Mapp. 27, 144 (2006).7. K. M. Petersson, A. Reis, 5. Askel6f, A. Castro-Caldas,

M. Ingvar, ]. Cogn. Neurosci. 12, 364 (2000).8. A. Castro-Caldas, K. M. Petersson, A. Reis,

5. 5tone-E1ander, M. Ingvar, Broin 121, 1053 (1998).9. K. M. Petersson, A. Reis, A. Castro-Caldas, M. Ingvar,

Neuroimage 10, 45 (1999).10. ]. Morais, P. Bertelson, L. Cary, ]. Alegria, Cognition 24,

45 (1986).11. H. Cheung, H. C. Chen, Lang. Cogn. Process. 19, 1 (2004).12. L. Perre, C. Pattamadilok, M. Montan\, ). C. Ziegler,

Broin Res. 1275, 73 (2009).

13. P. Ventura, ]. Morais, R. Kolinsky, Cognition 105, 547(200n

14. ]. C. Ziegler, A. Petrova, L. Ferrand,]. fxp. Psychal. Learn.Mem. Cogn. 34, 643 (2008),

15 .. B. A. 5haywitz et 01., Bioi. Psychiatry 52, 101 (2002).16. L. Cohen,S. Dehaene, Neuroimage 22, 466 (2004).17. c. I. Baker et 01., Proe. Notl. Acad. Sci. U.S.A. 104,

9087 (2007).18. S. Brem et 01., Prae. Notl. Acod. Sci. U.S.A. 107, 7939

(2010).19. U. Maurer et 01., Neuroimage 33, 749 (2006).20. D. B. Polley, E. E. Steinberg, M. M. Merzenich,]. Neurosci.

26, 4970 (2006).21. W. li, V. Piech, c. D. Gilbert, Not Neurosci. 7, 651 (2004).22. M. Sigman et 01., Neuron 46, 823 (2005).23. S. Dehaene, Reading in the Brain (Penguin Viking,

New York, 2009).24. I. Gauthier, T. Curran, K. M. Curby, D. Collins,

Not. Neurasci. 6, 428 (2003).25. A. Harel, S. Gilaie-Dotan, R. Malach, 5. Bentin, Cereb.

Cortex 20, 2304 (2010).26. B. Rossion, C. C. Kung, M. ]. Tarr, Proe. Natl. Acad.

Sci. U.S.A. 101, 14521 (2004).27. D.]. Bolger, C. A. Perfetti, W. Schneider, Hum. Broin Mapp.

25, 92 (2005).28. G. Golarai et 01., Not. Neurosci. 10, 512 (200n29. Materials and methods are available as supporting

material on Science Online.30. R. Gaillard et 01., Neuron 50, 191 (2006).31. L. Cohen,S. Dehaene, F. Vinckier, A. Jobert, A. Montavont,

Neuroimage 40, 353 (2008).32. E. Eger, 5. R. 5chweinberger, R. ]. Dolan, R. N. Henson,

Neuroimage 26, 112B (2005).33. P. E. Downing, A. W. Chan, M. V. Peelen, C. M. Dodds,

N. Kanwisher, Cereb. Cortex 16, 1453 (2006).34. T. A. Nazir, N. Ben-Boutayab, N. Decoppet, A. Deutsch,

R. Frost, Brain Lang. 88, 294 (2004).35. K. Rayner, Psychal. Bull. 124, 372 (1998).36. C. ]acquemot, C. Pallier, D. LeBihan, 5. Dehaene,

E. Dupoux, ]. Neurosci. 23, 9541 (2003).37. N. van Atteveldt, E. Formisano, R. Goebel, L. Blomert,

Neuron 43, 271 (2004).38. V. Blau et 01., Brain 133, 868 (2010).

39. P. E. Turkeltaub, L. Gareau, D. L. Flowers, T. A. Zeffiro,G. F. Eden, Not. Neurosci. 6, 767 (2003).

40. L. Cohen, A. ]obert, D. Le Bihan, 5. Dehaene, Neuraimage23, 1256 (2004).

41. Y. N. Yoncheva, ]. D. Zevin, U. Maurer, B. D. McCandliss,Cereb. Cortex 20, 622 (2010).

42. A. 5. Desroches et 01., Brain Res. 1356, 73 (2010).43. ). R. Booth et 01., Hum. Brain Mapp. 19, 155 (2003).44. F. Kherif, G. ]osse, C. ]. Price, Cereb. Cortex

10.1093lcercorlbhq063 (2010).45. M. Longcamp, ]. L. Anton, M. Roth, ]. L. Velay,

Neuroimage 19, 1492 (2D03).46. This work was supported by Institut National de la

Sante et de la Recherche Medicale (IN5ERM),Commissariat a I'Energie Atomique «EA), College deFrance, Agence Nationale de la Recherche (projectCORELEX), Funda~ao para a Ciencia e a Tecnologia,the European Community FEDER funding (ProjectPTDClPSI166077/2006, "Cognitive consequences ofliteracy"), SARAH Network of Rehabilitation Hospitals,and by two grants from the Belgian French community(Fonds de la Recherche Fondamentale Collective2.4586.07 and Action de Recherche Concertee06/11-342). We gratefully acknowledge A. Amadon,M.-H. Baju, L. Labruna, D. Le Bihan, L. Hertz-Pannier,P. Pinel, and the Neur05pin infrastructure groups atNeuroSpin; C. Carvalho, L. Querida,S. Fernandes, andT. Fernandes at the Faculty of Psychology, University oflisbon; and D. Y. 5uguieda, R. S. Vera, A. G. Tauil,E. Amemiya, L. G. N. Nunes,S. B. de Oliveira, andC. L. M. Gillis at SARAH Brasilia.

Supporting Online MaterialwWIV.sciencemag .orglcgilcontenUfu IVscience .11941401DClMaterials and MethodsSaM TextFigs. 51 to S8Tables Sl and S2References

23 June 2010; accepted 20 October 2010Published online 11 November 2010;10.1126/science.1194140