Doble Ruta

8/14/2019 Doble Ruta

http://slidepdf.com/reader/full/doble-ruta 1/20

Evaluation of the dual route theory of reading:a metanalysis of 35 neuroimaging studies

G. Jobard, F. Crivello, and N. Tzourio-Mazoyer*

Groupe d’Imagerie Neurofonctionnelle, CNRS, UMR 6095, CEA LRC36V, Universite de Caen, Universite de Paris 5, 14074 Caen Cedex, France

Received 4 March 2003; revised 15 May 2003; accepted 29 May 2003

Abstract

Numerous studies concerned with cerebral structures underlying word reading have been published during the last decade. A few

controversies, however, together with methodological or theoretical discrepancies between laboratories, still contribute to blurring the

overall view of advances effected in neuroimaging. Carried out within the dual route of reading framework, the aim of this metanalysis was

to provide an objective picture of these advances. To achieve this, we used an automated analysis method based on the inventory of

activation peaks issued from word or pseudoword reading contrasts of 35 published neuroimaging studies. A first result of this metanalysis

was that no cluster of activations has been found more recruited by word than pseudoword reading, implying that the first steps of word

access may be common to word and word-like stimuli and would take place within a left occipitotemporal region (previously referred to

as the Visual Word Form Area—VWFA) situated in the ventral route, at the junction between inferior temporal and fusiform gyri. The

results also indicated the existence of brain regions predominantly involved in one of the two routes to access word. The graphophonological

conversion seems indeed to rely on left lateralized brain structures such as superior temporal areas, supramarginal gyrus, and the opercular

part of the inferior frontal gyrus, these last two regions reflecting a greater load in working memory during such an access. The

lexicosemantic route is thought to arise from the coactivation of the VWFA and semantic areas. These semantic areas would encompass a

basal inferior temporal area, the posterior part of the middle temporal gyrus, and the triangular part of inferior frontal gyrus. These resultsconfirm the suitability of the dual route framework to account for activations observed in nonpathological subjects while they read.

© 2003 Elsevier Inc. All rights reserved.

Introduction

Despite the large number of neuroimaging studies inter-

ested in unraveling brain organization sustaining reading,

acquiring a clear picture of cerebral areas involved in visual

word access and the specific cognitive processes thought to

take place in these regions remains quite a tricky enterprise.

The difficulty of such a task arises from many combined

elements that contribute to mask the picture one can get bysimply looking at the results that are already published.

A first element is the lack of explicit definition of the

theoretical framework in which studies are undertaken. This

is of prime importance in the interpretation of activation

results, since theoretical concepts and the suspected neces-

sary cognitive processes may vary from one study to an-

other. Models of dual route theory provide a framework

commonly used in studies of reading. This theory develops

the view that word reading can be achieved through two

distinct routes, relying on discrete processes (Fig. 1). The

graphophonological route, also called indirect route, re-quires visual words to be transformed into their auditory

counterparts, thanks to the application of grapheme-to-pho-

neme correspondences. The pronunciation of words being

available, subjects can then access their meanings. These

grapheme-to-phoneme correspondences are however more

or less univocal according to the language considered and

its degree of transparency: while the same group of letters

will invariably lead to the same pronunciation in Spanish,

some letter combinations in English will be read aloud

* Corresponding author. Groupe d’Imagerie Neurofonctionnelle, Cen-

tre Cyceron, 22, Boulevard Becquerel, BP5229, 14074 Caen Cedex,

France. Fax: 33-231-470-220.

E-mail address: [email protected] (N. Tzourio-Mazoyer).

NeuroImage 20 (2003) 693–712 www.elsevier.com/locate/ynimg

1053-8119/$ – see front matter © 2003 Elsevier Inc. All rights reserved.

doi:10.1016/S1053-8119(03)00343-4





varying anatomical labels among studies may also contrib-

ute to complicate a general overview of the literature, since

it can induce readers to conclude that different brain areas

are implicated despite activations that are congruent in

terms of spatial coordinates.

The goal of this metanalysis was to clarify results pub-

lished in the reading literature and to determine (a) whether

there exists a system dedicated to the processing of visual

word form as postulated by the dual route models, and (b)

whether neuroimaging results support the possibility of two

distinct routes for accessing words. To answer these ques-

tions, we performed an analysis that was as observer inde-

pendent as possible, based on the core exploitation of co-

ordinates related to cognitive contrasts obtained in 35

different neuroimaging studies. This analysis relied on the

use of an automated spatial segregation of activation peaks

coordinates, coupled with an automated anatomical labeling

of the spatially congruent activations in the Montreal Neu-

rological Institute stereotactic space (Tzourio-Mazoyer et

al., 2002).

Materials and methods

Raw data

The raw data of this metanalysis was constituted by

activation peak coordinates reported in 35 neuroimaging

studies (using PET and fMRI exclusively, see Table 1) and

obtained in contrasts, implying the reading of words or

pseudowords. Only studies ranging from years of publica-tion 1990 to 2002 were used, in which stereotactic coordi-

nates were made available exclusively for tasks submitted to

nonpathological subjects. These activation tasks were either

directly compared to each other or contrasted to baselines.

No a priori selection was applied to the set of coordinates

and strictly all coordinates issued from contrasts of interest

of all studies were used.

Stereotactic space and template used

Although authors almost constantly refer to their coor-

dinates as being in the Talairach space (Talairach and Tour-

Table 1

List of the studies used in this metanalysis

References Imaging technique Subjects Threshold

Beauregard et al., 1997 PET 10 0.001 uncorr.

Bookheimer et al., 1995 PET 8 men, 8 women 0.001 uncorr.

Booth et al., 2002 FMRI 13 0.001 uncorr., 2nd level

Buchel et al., 1998 PET 6 sighted, 6 blind, 3 late-blind 0.05Cappa et al., 1998 PET 13 0.001 uncorr.

Chee et al., 1999 FMRI 5 men, 3 women 105 uncorr

Cohen et al., 2000 FMRI 1 man, 4 women 0.001

Cohen et al., 2002 FMRI 1 man, 6 women 0.01 uncorr.

Dehaene et al., 2001 FMRI 12 men, 25 women 105 uncorr. to 0.02

Fiebach et al., 2002 FMRI 5 men, 8 women 0.001 uncorr.

Fiez and Balota, 1999 PET 6 men, 5 women 0.01 uncorr.

Hagoort et al., 1999 PET 8 men, 3 women 0.01 uncorr.

Herbster et al., 1997 PET 5 men, 5 women 0.001 uncorr.

Horwitz et al., 1998 PET 14 normal men 0.001 uncorr.

Howard et al., 1992 PET 7 men, 5 women 0.001 uncorr.

Jernigan et al., 1998 PET 6 men, 2 women 0.05

Kiehl et al., 1999 FMRI 6 men 0.05

Mechelli et al., 2000 FMRI 5 men, 1 woman 0.001 uncorr.

Menard et al., 1996 PET 8 men 0.05Moore and Price, 1999 PET 8 men 0.001 uncorr.

Mummery et al., 1998 PET 10 men 0.001 uncorr.

Paulesu et al., 2000 PET 12 0.001 uncorr. To 0.01 uncorr.a

Perani et al., 1999 PET 14 men 0.001 uncorr.

Petersen et al., 1989 PET Variable from 5 to 12 0.03 uncorr.

Petersen et al., 1990 PET 5 men, 3 women Nonavailable

Price et al., 1994 PET 12 men 0.001 uncorr.

Price et al., 1996a PET 6 men 0.001 uncorr.

Price et al., 1996b PET Variable from 4 to 8 0.001 uncorr.

Price et al., 1997 PET 6 0.001 uncorr.

Rumsey et al., 1997 PET 14 men 0.001 uncorr. to 0.01 uncorr.a

Small et al., 1996 FMRI 1 man, 1 woman Nonavailable

Tan et al., 2001 FMRI 10 men 0.01 uncorr.

Tokunaga et al., 1999 PET 8 men 0.05 to 0.001 uncorr.a

Xu et al., 2001 PET 12 0.001 uncorr.

a More conservative thresholds were used for task vs baseline comparison while a more leniant threshold was used when tasks were directly compared to

each other.

695G. Jobard et al. / NeuroImage 20 (2003) 693 – 712



noux, 1988), some uncertainty remains concerning the pos-

sibility to compare activation coordinates from one study to

another (Brett et al., 2002). One source of discrepancy can

arise from the nature of the template brains used for the

spatial normalization. Reference brains indeed may not be

exactly the same size, even though their space has been

defined according to the AC/PC specification indicated byTalairach, and it is therefore crucial to correct for this

possible discrepancy if one whishes to compare activation

peaks issued in studies using different templates. When

necessary, we applied a correction to locate all coordinates

in the MNI single subject reference space (see http://www.

mrc-cbu.cam.ac.uk/Imaging/mnispace.html).

Coordinates found in studies performed with SPM soft-

ware prior to SPM96 — or with other methods without spec-

ifying any template—were considered as using Talairach-

compatible brain templates, while studies done with SPM96

or later versions were considered as using MNI template

and therefore did not require any transformation.

Spatial segregation

A total of 622 activation peak coordinates was reported.

To constitute groups of spatially congruent activations, it is

necessary to determine which of the collected coordinates

can objectively be assembled in the same groups. For this

purpose, we computed euclidian distances between all ac-

tivation peaks and then classified them in a hierarchical tree

using a “ward” classification algorithm aimed at minimizing

the intragroup standard deviation while keeping intergroup

standard deviation as high as possible. This has been doneusing the statistical software “R” (http://cran.r-project.org/),

with the “mva” library in which these functions are directly

implemented (see Murtagh (1985) for classification algo-

rithm details). The result of this classification is a hierar-

chically organized tree in which every single coordinate is

present as a single group at its bottom. Progressive group-

ings of nearest neighbors occur while one gets higher along

this tree (going from N groups at the bottom to 1 group at

the top involving all coordinates: see Fig. 2 for an example).

This tree has then to be cut at a certain level to determine the

constitution of the different clusters. The result of such a

section is a set of clusters, each characterized by their centercoordinates and standard deviations in x, y, and z directions.

It is worth emphasizing the fact that information concerning

the nature of the contrasts used was in no way taken into

account during the spatial segregation processing.

The section of this hierarchical tree was performed so

that the averaged standard deviations for all clusters in x, y,

and z were less than 7.5 mm. This criterion ensures that 95%

of coordinates aggregated in a group lie within a spatial

limit of 15 mm from the center of this group, which roughly

corresponds to the final spatial resolution of most functional

imaging studies. Using this criterion, the 622 coordinates

were divided in 55 groups, which resulted in mean standard

deviations of 6.08, 7.09, and 7.47 mm in x, y, and z direc-

tions, respectively.

Automated anatomical labeling of clusters

To ensure reproducibility and uniformity in the anatom-

ical localization, we used a home-made program called“Guiplot” (Graphic User Interface plot) to anatomically

label each cluster of spatially congruent activation peak

coordinates. For each group, mean coordinates were com-

puted and projected into the MNI single-subject MRI ref-

erence brain. Using a macroscopic anatomical parcellation

of this MRI (Tzourio-Mazoyer et al., 2002), each mean

cluster coordinate was further automatically assigned an

anatomical label. This observer-independent procedure al-

lows an unbiased anatomical report of the areas engaged in

this metanalysis study.

Contrast classification

Even though this did not interfere in any way with the

spatial segregation process, information concerning the na-

ture of contrasts leading to the different activation peaks

was conserved. We determined different classes of contrasts

to interpret the results, depending on their hypothesized

underlying cognitive processes. A different color was attrib-

uted to each class of contrast, so that the proportion of the

corresponding processes could be visually rendered.

Direct route contrasts

(a) Words vs pseudowords: while words may have been

encountered before by readers and therefore can be presentin a visual word-form lexicon, pseudowords are thought to

require the indirect route to be read. Such contrasts are

therefore more likely to engage the lexicosemantic access

and reveal areas involved in the recognition of stored visual

word forms.

(b) Kanji vs fixation and kanji words vs kana words: In

Japanese, Kanji writing corresponds to ideograms where a

symbol globally refers to a meaning, while kana writing

refers to syllables constituting the words. In the dual-route

framework, each type of writing is thought to rely on a

different route, with Kanji being read by the direct route and

kana by the graphophonological route.(c) Lexical or semantic decision vs phonological deci-

sion: lexical or semantic decision tasks require the subject to

decide if the stimulus presented is a word or to access its

meaning, which can be effected without accessing to its

pronunciation (although it can occur implicitly). When sub-

jects have to do phonological decision tasks, however, they

have access to the sounds of the words and are therefore

more likely to engage the indirect route. The probability is

then higher than the contrast between these two tasks and

reveals the use of lexicosemantic associations.

(d) Irregular vs regular words: while regular words can

be accessed indifferently by means of the two routes, irreg-

696 G. Jobard et al. / NeuroImage 20 (2003) 693–712

http://www.mrc-cbu.cam.ac.uk/Imaging/mnispace.html

http://cran.r-project.org/





ular words such as “yacht” cannot be properly pronounced

following the application of GPC rules and therefore need to

engage the direct route. Brain areas being more active in this

condition are therefore supposed to be involved in processes

selective to the direct route.

Indirect route contrasts

Many contrasts belonging to this category are the oppo-

site of the direct route contrasts: pseudowords vs words,

kana words vs fixation, kana pseudowords vs fixation, kana

words vs kanji words, and regular vs irregular words. We

considered additionally another type of contrasts; that is,

aloud vs silent reading. While both routes can be involved

in both reading tasks, aloud reading is thought to emphasize

the application of GPC rules since it requires an explicitaccess to the sounds of words.

Nonconclusive contrasts

These contrasts were word vs baseline comparisons (the

different baselines entailed fixation, visual baselines, or

alphabetical baselines). Since words can supposedly be read

by means of two routes, word reading vs baseline contrasts

were considered as nonspecific to any reading route. While

regions being activated during these contrasts could be

assessed as being involved in reading, these comparisons

were too lose to conclude on the exact contributions of these

regions.

Words vs pictures contrasts

These contrasts were set apart from the other classes

since it compared activities that were traditionally not con-

sidered in relation to each other in the field of psychology

and were therefore not predicted in the dual-route frame-

work. The potentials of such a comparison was double. On

one hand, it could bring into light some brain areas special-

ized in the visual processing of words (i.e., testing the

existence of a visual word-form lexicon) and participate in

the investigation on direct route neural bases. On the other

hand, while object and word perception shared some pro-

cesses such as early visual analyses and semantic access,

they differed on the possibility these tasks offer for the

application of GPC rules (since the use of such rules is

possible only when subjects are presented words) and could

therefore enlighten brain areas involved in the indirect

route.

Results

Thirty-five clusters were located in the left hemisphere;

15 were in the right hemisphere and 5 clusters were consti-

tuted by isolated peaks dispersed in the brain with a high

spatial standard deviation (many of these peaks were lo-cated in white matter and some even fell out of the brain).

The aim of this work was to provide a global view of the

results published in the last few years concerning two main

controversies related to the dual route of reading frame-

work. For this reason, we chose to focus, among all activa-

tion clusters, especially on regions in the left hemisphere

that have been described previously in the literature as

having a role in word reading. Even though they will not be

discussed here, it must be kept in mind however that other

regions, such as posterior visual brain regions or precentral

gyrus, have been reliably found as activated in reading by

different studies.

Left medial extrastriate cortex

Two clusters have been found that correspond to the

medial extrastriate region described by the princeps reading

study of Petersen (Petersen et al., 1989). The first cluster,

situated in the left lingual gyrus, gathered eight activation

peaks at mean coordinates, x 22 7; y 47 5; z

1 4; obtained in five different studies (see Table 2).

Within this cluster, the analysis of the contrasts revealed

that activation peaks were mainly issued from direct route

contrasts (five Direct Route against one Indirect Route and

Table 2

Activation peaks constituting the left lingual gyrus cluster

References Coordinates Contrasts

x y z

Petersen et al., 1990 29 55 1 Passive word—fixation NC


Rumsey et al., 1997 10 54 3 Lexical decision—phonological decision on pseudoword DR



Hagoort et al., 1999 18 50 3 (Aloud and silent) word—pseudoword DR

Horwitz et al., 1998 34 39 2 Correlated with Angular Gyrus in pseudoword reading IDR

Fiebach et al., 2002 23 46 11 Word—pseudoword DR

Mean 22 47 1 Left lingual gyrus

Standard deviation 7 5 4

Note. Coordinates of activation peaks are given in the MNI stereotactic space. IDR: indirect route contrast; DR: direct route contrast; W-P: Word-Picture;

NI: nonidentified; NC: nonconclusive.




two Nonconclusive contrasts), even if three of the five peaks

were issued from the same contrast of the same study.

The second cluster was constituted of 11 maxima found

in 9 different studies with activation belonging to different

anatomic structures of the occipital lobe, such as the lingual,

the superior, the inferior and middle occipital gyri, and the

calcarine. Mean coordinates were x 20 6; y 77

8; z 5 6, and contrasts observed in this cluster were

mainly Indirect Route (five) and Nonconclusive (five) (see

Fig. 3 and Table 3).

Left fusiform gyrus/occipitotemporal region

The center of this cluster was situated in the fusiform

gyrus, at the margin of the occipitotemporal sulcus (at mean

coordinates x 44 4; y 58 5; z 15 6) and

was constituted by 28 activation peaks issued from 17

different studies. Among these contrasts nine were Noncon-

clusive, nine Indirect Route, six Direct Route, and four

Nonidentified (see Table 4 and Fig. 4).

Left inferior temporal gyrus

A brain region, situated more anterior in the ventral route

than the occipitotemporal junction described earlier, has

also been found active by 10 studies (at mean coordinates x

48 4; y 41 6; z 16 6, details in Table

5). The 14 activation peaks were issued from Nonconclusive

(six), Indirect Route (five), and Direct Route Contrasts

(three).

Left supramarginal gyrus

The supramarginal gyrus has been found activated in

seven reading studies, in which 10 activation maxima were

detected (at mean coordinates x 60 4; y 41 6;

z

25

6). Four activation peaks belonging to this clusterhave been elicited by word-picture contrasts, 4 others by

Indirect Route contrasts, and the remaining two were either

Nonconclusive or Nonidentified contrasts (see Table 6 and

Fig. 6).

Left posterior middle temporal cluster

This cluster was constituted by spatially close coordi-

nates of 13 different studies and was constituted by 16

activation peaks. This cluster was labeled on the MNI single

subject as the posterior part of the middle temporal gyrus

and was situated very close to the most posterior part of the

superior temporal sulcus ( x 49 8; y 54 4; z

Fig. 2. Example of hierarchical tree provided by the spatial segregation procedure — hierarchical tree containing 50 points of activation. Each vertical branch

at the very bottom of the tree corresponds to each point, and horizontal branches correspond to grouping of gradually more distant points as one gets higher

in the tree. In this example points 17 and 44 (on the bottom right) are very close, the closest point they can be further grouped with is point 6. Cutting the

tree close to the bottom (blue dotted line) will ensure small standard deviation among groups (mean standard deviations of 2.59, 3.87, and 4.91 in x, y, and

z directions, respectively) while providing many groups (15 in this example, indicated by a blue background) with the risk of separating some groups that

are comparable in terms of location. On the other hand, cutting high in the tree (orange dotted line) will reduce the number of clusters (to four as figured

with the orange background) and result in an increased standard deviation for each cluster (mean standard deviations of 6.98, 6.87, and 8.38 in x, y, and z

directions, respectively).

Fig. 3. Clusters of activations in medial extrastriate areas. The first raw corresponds to the first cluster located in the occipital cortex, while the second raw

depicts the second cluster located in the lingual gyrus. The mean coordinates for these clusters are x 22 7; y 47 5; z 1 4, and x 21

5; y 79 8; z 6 8, respectively. Nature of contrasts is indicated by their color.

Table 3

Activation peaks constituting the left occipital cluster


x y z

Menard et al., 1996 30 77 5 Passive word—xxXxx NC




Petersen et al., 1990 23 67 1 Passive pseudoword—fixation IDR

Bookheimer et al., 1995 20 87 4 Passive word—lines NC

Hagoort et al., 1999 27 89 12 (Aloud and silent) pseudowords—words IDR

Price et al., 1996a 14 85 4 Mot aloud—mot silent (avec articulation sans sons) IDR

Price et al., 1997 14 84 18 Phonological decision—semantic decision IDR

Cappa et al., 1998 22 76 12 Pseudoword—fixation IDR

Booth et al., 2002 12 74 1 Visual word rime spelling—auditory word rime spelling NI

Mean 21 79 6 White matter




698 G. Jobard et al. / NeuroImage 20 (2003) 693 – 712






Table 4

Activation peaks constituting the occipito-temporal junction cluster


x y z

Kiehl et al., 1999 41 60 12 Lexical decision—***** NC

Fiez and Balota, 1999 43 65 8 Overall word—fixation NC

Cohen et al., 2000 42 57 6 Passive word—fixation NCMoore and Price, 1999 44 54 14 Word and object naming—word and object perception NI

Sakurai et al., 2000 44 54 22 Kanji—fixation DR

Sakurai et al., 2000 42 52 22 Conjunction kana and kanji NC

Hagoort et al., 1999 34 56 16 (Aloud and silent) pseudowords—words IDR

Simos et al., 2000 50 56 12 Kanji writing—kana writing DR

Paulesu et al., 2000 48 58 6 Pseudowords—words (for English and Italian subjects) IDR




Xu et al., 2001 46 66 10 Pseudowords rhyming—word rhyming IDR

Price et al., 1996a 51 66 13 Word aloud—word silent (with speechless pronunciation) IDR


Horwitz et al., 1998 48 66 18 Correlated with Angular Gyrus in irregular word reading DR

Horwitz et al., 1998 46 63 27 Correlated with Angular Gyrus in irregular word reading DR

Chee et al., 1999 34 61 18 Word—fixation NCCappa et al., 1998 46 52 20 Pseudoword—fixation IDR

Cappa et al., 1998 46 60 8 Word—pseudoword DR

Cohen et al., 2002 39 57 9 Word—consonants NC

Dehaene et al., 2001 40 56 24 Word—fixation NC

Dehaene et al., 2001 48 60 12 Masked word—masked fixation NC

Dehaene et al., 2001 44 52 16 Masked word—masked fixation NC

Dehaene et al., 2001 44 52 20 Priming effect of word independent of letter case NI

Booth et al., 2002 39 61 25 Visual word rhyme spelling—auditory word spelling NI

Booth et al., 2002 45 58 18 Auditory word rime spelling—auditory word rhyming NI

Mean 44 58 15 Left fusiform gyrus




Table 5

Activation peaks constituting the left inferior temporal gyrus cluster


x y z

Fiez and Balota, 1999 43 46 12 Pseudowords—words IDR


Buchel et al., 1998 40 38 16 Word—consonants NC

Price et al., 1996b 48 42 12 Words—false font NC

Price et al., 1996b 46 36 8 Words—consonants NC

Rumsey et al., 1997 51 35 16 Phonological decision—lexical decision IDR

Hagoort et al., 1999 51 35 16 Words—pseudowords DR



Beauregard et al., 1997 55 46 24 Concrete words— (blinking) NC

Beauregard et al., 1997 55 46 20 Abstract words— (blinking) NC

Horwitz et al., 1998 46 34 26 Area correlated with Angular Gyrus in pseudoword reading aloud IDR

Horwitz et al., 1998 51 47 26 Area correlated with Angular Gyrus in irregular word reading aloud DR

Cappa et al., 1998 46 48 4 Word—pseudoword DR

Mean 48 41 16 Left inferior temporal gyrus







13 6). The dominant contrasts represented in this cluster

were mainly “Nonconclusive” (11 NC, 2 Indirect Route,

and 1 Direct Route contrast; see Table 7 for details and

Fig. 5).

Left posterior superior temporal gyrus

A region of the superior temporal gyrus, posterior to

Heschl’s gyrus and that might correspond to the planum

temporale, has also been found activated in seven studies (at

mean coordinates x

37

7; y

35

7; z

12

7). The 12 peaks of activation mainly issued from Indirect

Route (seven) and word-pictures (two) contrasts, while one

peak came from Nonconclusive and two from Nonidentified

contrasts (see Table 8 for details, and Fig. 6).

Left middle temporal gyrus

Another spot of consistent activation was found in the left

middle temporal gyrus, at the very margin of the middle part of

the superior temporal sulcus (at mean coordinates x 63

5; y

30

7; z

4

6: see Table 9 and Fig. 5. This cluster

Table 6

Activation peaks constituting the left supramarginal gyrus cluster


x y z

Menard et al., 1996 59 49 28 Passive word—passive picture W-P

Menard et al., 1996 58 54 28 Passive word—xxXxx NC

Moore and Price, 1999 68 46 20 Word perception and naming—object perception and naming W-P


Moore and Price, 1999 68 44 22 Word naming—object naming W-P


Price et al., 1994 59 40 20 Word and pseudoword aloud—false font IDR

Mummery et al., 1998 56 34 34 Phonological decision—semantic decision IDR

Tan et al., 2001 61 37 24 Chinese character—fixation DR

Booth et al., 2002 58 44 24 Visual word rhyming—visual word rime spelling IDR


Mean 60 41 25 Left supramarginal gyrus




Table 7

Activation peaks constituting the left posterior middle temporal gyrus cluster


x y z

Howard et al., 1992 51 50 6 Word reading aloud—see and say crime NC

Menard et al., 1996 53 58 19 Passive word—passive picture W-P

Menard et al., 1996 44 56 23 Passive word—fixation NC

Kiehl et al., 1999 52 52 4 Lexical decision—***** NC


Cohen et al., 2000 57 54 6 Passive word—fixation NC

Cohen et al., 2000 27 57 21 Passive word—fixation NC

Simos et al., 2000 36 66 20 Kana writing—kanji writing IDR


Price et al., 1994 57 48 2 Silent viewing—false font NC

Price et al., 1994 48 46 19 Silent viewing—false font NC

Horwitz et al., 1998 44 57 23 Angular Gyrus described by Horwitz active in reading NC

Small et al., 1996 51 56 17 Word reading aloud—false font aloud NC

Fiebach et al., 2002 53 54 9 Words—pseudowords DR

Perani et al., 1999 60 50 12 All kind of words—consonants NC

Booth et al., 2002 45 56 10 Visual word rhyme spelling—auditory word rhyme spelling NI

Mean 49 54 13 Left middle temporal gyrus







included 13 peaks of nine different studies, most being activa-

tion peaks from Indirect Route contrasts (six), and Nonconclu-

sive contrasts (five). The other two peaks corresponded to

word vs picture and nonidentified contrasts.

Left superior temporal gyrus

This cluster, whose center was situated in the mid-

dle part of the superior temporal gyrus, close to the

superior temporal sulcus (at mean coordinates x 53

6; y 13 7; z 0 4), gathered 12 activation

maxima of eight studies (see Table 10 and Fig. 6). Four

contrasts were involved in Indirect Route access, two

were issued from the comparison between words and

pictures, three were Nonconclusive, and two were Non-

identified.

Left inferior frontal gyrus (opercular part)

Some clusters situated more generally in Broca’s area

have been found during this metanalysis. Among these, a

cluster situated in the most dorsal part, in the frontal oper-cular part (at mean coordinates x 50 5; y 10 5;

z 4 8, see Table 11 and Fig. 6), gathered 13 activation

peaks issued from 11 different studies. Contrasts leading to

an activation of this region were Indirect Route (three),

Direct Route (three), Word-Picture (one), and Nonconclu-

sive contrasts (six).

Left inferior frontal gyrus (triangular part)

Seventeen activation peaks of 11 different studies were

included in this cluster located more anterior and ventrally

Fig. 4. Cluster of activations obtained in the left occipitotemporal junction cluster. The mean coordinates for this cluster are: x 44 4; y 58 5;

z 15 6. Nature of contrasts is indicated by their color.

Fig. 6. Cluster of activations obtained in the left posterior middle temporal gyrus cluster. The mean coordinates for this cluster are x 49 8; y 54

4; z 13 6. Nature of contrasts is indicated by their color.




Fig. 5. Dual route model of reading as suggested by the metanalysis of results published in neuroimaging studies



than the previous cluster, in the triangular part of Broca’s

area (at mean coordinates x 44 4; y 23 6; z

17 3, see Table 12 and Fig. 6). Six peaks were issued

from Direct route contrasts, five from Indirect Route con-

trasts, five from Nonconclusive, and one from a Noniden-

tified contrast.

Discussion

This method of spatial segregation resulted in a set of clusters of reliable activations that corresponded in large

parts to structures previously described as playing a key role

in reading. A first question that we wished to investigate in

the light of this method of review concerned the possible

specialization of a brain area for the processing of visual

words.

Is there a region dedicated to orthographic processing?

Since the first neuroimaging studies of reading, the hy-

pothesis concerning the existence of a brain region dedi-

cated to the processing of visual features of words exclu-

sively has always been present and is still a matter of debate.

This issue addresses the first steps of word access andquestions the existence of a lexicon involved in the storage

of the orthographic forms that have previously been en-

coded by readers. Among 10 clusters identified in the re-

Table 8

Activation peaks constituting the left posterior superior temporal gyrus/planum temporale cluster


x y z



Sakurai et al., 2000 48 40 10 Kana pseudoword—fixation IDR

Sakurai et al., 2000 46 42 8 Kana word and kana pseudoword conjunction IDR

Sakurai et al., 2000 34 40 24 Kana word and kana pseudoword conjunction IDR

Price et al., 1996b 34 42 20 Word—consonants NC

Price et al., 1996b 24 42 28 Pseudoword—word IDR


Price et al., 1994 32 23 3 Word and pseudoword conjunction—false font IDR

Horwitz et al., 1998 48 35 7 Area correlated with Angular Gyrus in pseudoword reading aloud IDR

Booth et al., 2002 39 35 18 Auditory word rhyme spelling—visual word rhyme spelling NI

Booth et al., 2002 42 44 8 Auditory word rhyme spelling—auditory word rhyming NI

Mean 37 35 12 Left superior temporal gyrus




Table 9

Activation peaks constituting the left middle temporal gyrus/T1 cluster


x y z

Herbster et al., 1997 60 18 0 Regular word—fixation NC

Herbster et al., 1997 60 22 4 Pseudoword—fixation IDR

Moore and Price, 1999 68 38 10 Word naming—object naming W-P



Rumsey et al., 1997 61 27 7 Pseudoword—irregular word IDR

Paulesu et al., 2000 70 30 0 Pseudoword—word (for English and Italian subjects) IDR

Beauregard et al., 1997 59 39 5 Concrete words— (blinking) NC

Beauregard et al., 1997 58 38 3 Abstract words— (blinking) NC

Jernigan et al., 1998 61 31 2 Word—fixation NC

Perani et al., 1999 56 38 4 All types of words—consonants NC


Booth et al., 2002 64 32 15 Visual word rhyming—visual word rhyme spelling IDR

Mean 63 30 4 Left middle temporal gyrus







sults, no one seemed to be reliably found activated exclu-

sively or predominantly by direct route contrasts. Three

different possible specialized structures have been proposed

in the literature that we will evaluate.

Left angular gyrus

De jerine emitted the first hypothesis concerning a brain

region dedicated to orthographic processing in 1892 after

the observation of patients presenting reading impairments

associated or not with writing deficits. He pointed out this

region as a major center for reading and writing since hethought it was supporting the storage of the visual images of

letters. In this view, reading was achieved by relaying visual

information from the visual cortex of both hemispheres to

the angular gyrus, where the connection between letters’

sounds and shapes could be accomplished before being

transmitted to the language areas for understanding, or to

motor cortex for writing. A disconnection between the vi-

sual areas and angular gyrus (AG) would then result in

dyslexia without agraphia. Such dyslexic patients would be

able to write self-initiated words or on dictation but would

be incapable of reading what they just wrote since informa-

tion cannot be passed on to AG to be relayed to languageareas. In the case of a complete destruction of the angular

Table 10

Activation peaks constituting the left superior temporal gyrus/T1 cluster


x y z




Sakurai et al., 2000 62 8 2 Kanji—fixation DR


Price et al., 1996b 48 18 4 Word—false font NC

Price et al., 1996b 50 8 8 Word—false font NC

Rumsey et al., 1997 51 14 1 Pseudoword—irregular word IDR

Hagoort et al., 1999 58 6 3 (Aloud and silent) pseudoword—word IDR



Booth et al., 2002 48 22 5 Auditory word rhyming—visual word rhyming NI

Mean 53 13 0 Left superior temporal gyrus




Table 11

Activation peaks constituting the left inferior frontal gyrus (opercular part) cluster


x y z

Menard et al., 1996 53 6 9 Word—picture W-P

Menard et al., 1996 43 7 0 Word—xxXxx NC

Fiez and Balota, 1999 49 11 11 Irregular word—regular word DR


Herbster et al., 1997 48 6 0 Regular word aloud—fixation aloud NC

Hagoort et al., 1999 46 18 9 (Aloud and silent) pseudoword—words IDR

Xu et al., 2001 52 10 12 Pseudoword rhyming—word rhyming IDR

Price et al., 1994 51 10 5 Word—false font NC

Price et al., 1994 55 4 13 Word—false font NC

Fiebach et al., 2002 47 10 15 Pseudoword—frequent word IDR

Dehaene et al., 2001 48 8 4 Word—blank NC

Perani et al., 1999 52 20 8 Word—consonant NC



Booth et al., 2002 42 6 7 Visual word rhyming—visual word rime spelling IDR

Mean 50 10 4 Left inferior frontal opercular gyrus







gyrus, patients would be affected by dyslexia with agraphia.

This type of dyslexia would be characterized by an impos-

sibility for the patients to read and write, since they would

be unable to access letter shapes, even from another modal-

ity, and link them to sounds (patients would then reproduce

letters the same way they would reproduce any meaningless

line drawing) (De jerine, 1892).

This hypothesis for the central role of angular gyrus inword access was taken up and extended by Howard one

century later in a neuroimaging study (Howard et al., 1992).

Howard gave up the concept of De jerine’s visual letter

shape center and used rather the concept of visual word

lexicon developed in the dual route theory, which postulates

the existence of a structure devoted to the storage of the

visual forms of familiar words. Finding a region in the

posterior part of the middle temporal gyrus, “at the margin

of the angular gyrus,” activated in word reading aloud

contrasted to a cross fixation including a control for the

articulated response, he interpreted it as being the “site for

the written word lexicon.”The cluster of activations containing Howard’s written

lexicon site was identified (see Fig. 5 and Table 7) and, with

the method used in the present analysis, anatomically la-

beled as posterior middle temporal gyrus, not angular gyrus.

Activations found in this region by other word reading

studies have not been generally interpreted in terms of

access to a written word lexicon but rather in terms of

access to the meaning of words (Pugh et al., 1996; Price et

al., 1997; Price, 1997; Fiebach et al., 2002). Similarly, other

language studies found this region active during auditory

tasks involving semantic access (Stromswold et al., 1996;

Bookheimer et al., 1998; Thompson-Schill et al., 1999) and

labeled it as Wernicke’s area. Furthermore, the fact that this

region can also be activated in oral comprehension tasks

constitutes a serious argument for dismissing its interpreta-

tion as a unimodal area dedicated to the storage of visual

word forms. In our view, this latest observation would

rather constitute additional evidence confirming its role as a

multimodal integration region working as a semantic access

node.

Left medial extrastriate region

An alternative hypothesis concerning the possible loca-

tion of an area dedicated to orthographic processing comes

from Petersen, who proposed in a princeps study that this

process could be achieved in a left medial extrastriate region

(Petersen et al., 1990). In this study, Petersen observed that

word or pseudoword reading activated this region of the

lingual gyrus, while consonant strings failed to elicit similar

activation. He concluded then that this region was respon-

sible for the processing of orthographically legal letter

strings. Petersen provided four activation coordinates forthis medial extrastriate region that he considered as a single

brain structure. In our metanalysis, these four coordinates

fell in two different clusters of activation located in different

cerebral structures (Fig. 3).

As can be seen in the first cluster located in the lingual

gyrus, very few studies found an activation of this area

despite the use of similar contrasts. Interestingly, authors

finding analogous activations did not discuss it (Fiebach et

al., 2002) or even wondered about its role after dismissing

Petersen’s results in light of other studies (Hagoort et al.,

1999), probably because they were referring to the coordi-

nates found in the second cluster. Five of the six contrasts

Table 12

Activation peaks constituting the left inferior frontal gyrus (triangular part) cluster


x y z

Price et al., 1996b 42 28 20 Word—letters NC

Rumsey et al., 1997 36 33 10 Phonological decision—lexical decision IDR

Paulesu et al., 2000 42 24 14 pseudoword—word (for English and Italian subjects) IDR

Price et al., 1994 51 22 23 Lexical decision on word and pseudoword—false font IDR

Horwitz et al.,1998 36 30 19 Area correlated with angular gyrus in pseudoword reading IDR

Chee et al., 1999 46 12 20 Word—fixation NC

Chee et al., 1999 40 33 15 Word—fixation NC

Cappa et al., 1998 44 22 20 Semantic decision on Word—pseudoword viewing DR

Cappa et al., 1998 42 24 16 Visual semantic decision on Word of living object—pseudoword viewing DR

Cappa et al., 1998 44 22 20 Visual semantic decision on Word of object—pseudoword viewing DR

Cappa et al., 1998 46 22 20 Functional semantic on word of object—pseudoword viewing DR

Fiebach et al., 2002 52 32 13 Infrequent word—frequent word IDR






Mean 44 23 17 Left inferior frontal triangular gyrus







(other than Petersen’s) leading to activation in this area

belonged to quite selective contrasts of the lexicosemantic

route, but it is worth noting that three of these direct route

contrasts originate from the identical comparison effected in

the study of Rumsey et al. (1997).

The second cluster center fell into white matter, but was

constituted by coordinates of more studies than the first one.Activity in this region has usually been explained in terms

of stimulus visual complexity (Price, 1997). Some authors

showed an effect of stimulus length in this region rather

than orthographic legality by comparing different sizes of

false-font strings to pseudowords, although coordinates of

activation were not always provided for an accurate com-

parison (Indefrey et al., 1997). Considering these last results

and the lack of obvious convergence among studies that

would indicate a specialization for words in this area, it

appears that this region described by Petersen is more likely

to be involved in low-level visual processing, not necessar-

ily verbal.

Fusiform gyrus/occipitotemporal region

More recently, Cohen et al. proposed yet another cere-

bral region that would be situated at the ventral junction

between the occipital and temporal lobes, which they la-

beled “visual word form area” (VWFA) (Cohen et al.,

2000). The visual word form area refers here to a similar

view as the one developed in the dual route model of

Warrington and Shallice (1980), since it is thought to be

activated by words and pseudowords but not by consonant

letter strings or orthographically illegal letters strings (or at

least at a much lesser degree). Cohen showed that this

region was more recruited by word reading than checker-boards or consonant strings and that its activity did not

depend on the visual hemifield of presentation or on the

stimulus location on the retina (Cohen et al., 2000). This

area would hence take charge of prelexical processing spe-

cific for words or word-like stimuli, and this prelexical role

has been highlighted by recent works of Dehaene, demon-

strating a priming effect in this same region for real word

reading independently of the letter case used. This last result

asserts that this region may underlie the access of abstract

letter identity whatever its actual visual shape (Dehaene et

al., 2001). Finally, some results indicated that its activity

would be visual modality specific since it would respond towritten words but not to heard words and it was additionally

shown that no semantic modulation would occur in this area

(Dehaene et al., 2002). The corresponding cluster in our

metanalysis was located in the fusiform gyrus, or rather at

the junction between inferior temporal and fusiform gyri on

the occipitotemporal sulcus and gathered peaks of activity

found by many studies, as testifies the compact and crowded

resulting cluster (see Table 4 and Fig. 4).

While this consistency demonstrates a critical role in

reading for this structure, its characterization has been de-

veloped in neuroimaging studies in terms of a categorical

specialization for visual alphabetically legal letter strings

rather than in terms of reading processes. However, the

question can be raised concerning why the visual word form

area reveals to be more activated in a number of studies for

pseudowords than for words (Hagoort et al., 1999). As

suggested by Dehaene, pseudowords requiring longer read-

ing times, an increase in the region dedicated to their pro-

cessing could occur. It is nonetheless possible to proposeanother hypothesis in relation to the role of this region in the

segmentation and classification of word-like stimuli into

familiar units as suggested by Warrington (Warrington and

Shallice, 1980). In the case of such a processing, the search

for several familiar sublexical units in pseudowords could

produce more activation in the VWFA than would be nec-

essary for recognizing a single word shape. While such an

explanation remains very hypothetical and needs experi-

mental evidence, it does not rely on the controversial as-

sumption that this region more specifically responds to the

presentation of word-like stimuli.

It is indeed of great interest to note that results exist in

the neuroimaging literature that may cast some doubts on

the specialization of this brain structure. Vandenberghe as

well as Moore found that this region was not specific for

words but rather equivalently active for naming both words

and pictures of objects (Vandenberghe et al., 1996; Moore

and Price, 1999). Similarly, many studies found analogous

activation in both hemispheres for object perception (Van

Turennout et al., 2000; Adams and Janata, 2002), or mental

imagery (Mazard et al., 2002; Mellet et al., 2000), but left

hemisphere selective activations were generally seen during

comparisons contrasting mental imagery of nameable ob-

jects to shapes devoid of labels (Mellet et al., 1998). These

results altogether invite for more refined investigationscharacterizing the nature of the specialization that may take

place in this area. While Cohen proposed a category-specific

specialization (since this area would be more activated by

orthographically legal letter strings than any other visual

stimuli), the fact that this area is also activated by pictures

at an analogous degree may lead us to consider a functional

specialization positing a role for this region in segmentation

and classification valid for any visual stimulus. In this view,

the VWFA could be hypothesized as playing a role in

segmenting and classifying all visual stimuli (and not only

word-like stimuli) in familiar units, such as the familiar

parts of an object (like the legs of a table), or the familiargroupings of letters (such as “tion”). This hypothesis could

find some support in the study of Bar that showed that the

more subjects thought they recognized a briefly presented

object, the more activity there was in this region (Bar et al.,

2001). This result indeed establishes a positive correlation

between the familiarity estimated by the subject and the

activity of the VWFA. Further evidence is nevertheless

needed to state about the exact spatial correspondences at a

subject level between the occipitotemporal region activated

by words and the one activated by pictures or during mental

imagery. Since specialization of brain regions can hardly be

unequivocally addressed by the observation of greater ac-




tivity amplitudes for a given stimulus than for another, a

fruitful means of investigation for this issue may be an

adaptation of the approach developed by Gauthier et al.

(2000). Using presentation of letters and faces to determine

what areas seemed to be more specialized in the processing

of these stimuli, Gauthier repeatedly showed to her subjects

letters or faces in preserving their identity but under differ-ent visual conditions (by changing font or faces aspect). The

idea underlying this paradigm was that only brain areas

dedicated to the processing of specific stimuli should exhibit

habituation effects through the repetitions. This approach

allowed the segregation of necessary activations from the

ones that cooccurred with each stimulus presentation but

were not critical for it, by identifying regions modulating

their activity when confronted to the different visual ver-

sions of the same stimuli. The use of this habituation effect

applied to words and pictures would certainly provide con-

structive answers to this specialization debate.

As a summary concerning the question of the specializa-

tion of one region for written words, we showed that neu-

roimaging studies failed so far to uncover a cerebral area

that would be the functional equivalent of a written word

lexicon (in the sense of a region devoted to the storage of

most familiar real words global shapes). The discovery of a

region in which priming effects for words take place inde-

pendently of fonts used (Dehaene et al., 2001) and which is

more activated by alphabetically legal letter strings than

consonant strings brings us to consider an alternative ver-

sion of the first steps of the dual route theory. Indeed, even

though the exclusive specialization of this region for words

remains to be determined, these evidences argue altogether

in favor of a prelexical processing of words and word-likestimuli taking place in the occipitotemporal junction, rather

than the processing of previously stored word shapes. The

role of this occipitotemporal junction would be to segment,

classify, and relay visual word information to other regions

for further analysis.

Two distinct routes for accessing words

Another objective of this metanalysis was to determine

whether neuroimaging results could provide the confirma-

tion that words can be accessed by means of two distinct

routes. We therefore analyzed the constitution of the clus-ters in light of the nature of the contrasts involved, paying

particular attention mainly to classes of contrasts that were

prone to involve the indirect route, relying on the transfor-

mation from letters to sounds.

Direct route

The preceding part showed that an occipitotemporal area

was thought to underlie the prelexical processing of words

as well as word-like stimuli. A result of great interest con-

cerns the fact that no cluster in this metanalysis showed

significantly more involvement in contrasts favoring direct

route implication. According to dual route models’ predic-

tions, subtracting pseudowords activations to that of words

should reveal brain areas involved in lexicosemantic access

while the reverse contrast would reveal regions involved in

graphophonological conversion. Yet, some studies have

brought counterintuitive results showing that pseudowords

can actually recruit lexicosemantic areas, even at a higher

degree than words, because their processing would auto-matically initiate a search for these missing representations

(Price, 1997; Mechelli et al., 2003). As a consequence,

words—pseudowords contrasts may fail to reveal areas that

are however included in direct route. It nevertheless remains

that other direct rout contrasts (such as comparison of kanji

vs fixation, kanji words vs kana words, lexical decision vs

phonological decision, or irregular vs regular word reading)

failed to reveal a brain region that seems specific to this

route. This observation inclines us to postulate that direct

access from word shape to meaning would occur by the

coactivation of the prelexical occipitotemporal junction in

the fusiform gyrus and semantic areas (such as the inferior

temporal, the posterior middle temporal, and inferior frontal

gyri detailed in the following sections).

Graphophonological conversion

Information about the contrasts leading to the activation

peaks observed in different studies enabled us to highlight

five different clusters quantitatively more involved in com-

parisons favoring the conversion from graphemes to pho-

nemes in reading by either the choice of stimuli requiring

more specifically the use of this route (like pseudoword,

kana, or infrequent word reading) or the choice of tasks

magnifying the relevance of this route for accomplishing the

task (such as reading aloud or phonological judgments). Thefirst set of three clusters was located in the superior tempo-

ral gyrus, with two lying along the superior temporal sulcus.

Among these two, the most anterior cluster was situated in

the superior temporal gyrus, while the second lay in the

middle temporal gyrus and the most posterior was situated

in the superior temporal gyrus. These clusters showed a

clear specialization in indirect route contrasts with four, six,

and seven indirect route contrasts against one direct route

contrast in the most posterior cluster (Tables 8, 9, and 10).

The left superior temporal sulcus and posterior temporal

gyrus have been generally found activated in oral studies

also with contrasts maximizing phonological processes(Wise et al., 1991). These regions being consistently re-

cruited by the processing of human voice and especially in

phonological expertise tasks, their involvement in reading is

likely to manifest the use by subjects of correspondences

between graphemes and phonemes to compute words or

pseudowords pronunciations. This role in reading for brain

areas of the superior temporal gyrus has found recent sup-

port by some authors (Simos et al., 2002). A further argu-

ment can probably be found in the fact that, while no word

vs picture contrasts were present in previous clusters, they

are found in clusters where the proportions of indirect route

contrasts are higher. In accordance with the fact that no




sound can be reconstructed from pictures as is the case with

words, it seems to us that the presence of such contrasts

emphasizes the role of these regions in the application of

graphophonological rules.

The second group was composed of a first cluster situ-

ated in the supramarginal gyrus, and another situated in the

opercular part of the left inferior frontal gyrus. Even thoughthe opercular cluster contained as many “indirect route” as

“direct route” contrasts (three in both cases), we chose to

insert it as a part of the network involved in the graphopho-

nological conversion, as we think such a claim is supported

by additional experimental evidence. Paulesu, contrasting

rhyming judgment (thought to engage the subvocal re-

hearsal system but not the phonological store) to the main-

tenance of letters strings, demonstrated the involvement of

the supramarginal gyrus as the site of the phonological store

while he discussed the strong involvement of the opercular

part of Broca’s area in both tasks as evidence for its impli-

cation in the subvocal rehearsal system (Paulesu et al.,

1993). The proposition for this set of brain regions as

sustaining working memory has found support by other

authors (Fiez et al., 1996) and evidence further demon-

strated the implication of Broca’s opercular part in the

manipulation of phonology (Fiez, 1997). According to this

view, the activation of the opercular region in direct route

contrasts could be due to the rehearsal in working memory

of accessed words. The location of the phonological store is

more subject to debate, and several loci have been reported

in the literature (for a comment on the different localizations

of the phonological store, see Becker et al., 1999). The

mean coordinates of the present cluster correspond however

to a more inferior locus described by Becker et al. and is inthe vicinity (even if more lateral) of the one described by

Paulesu (1993). This somehow different location from other

verbal working memory addresses the question of a special-

ization of this region in a phonological store ascribed to

reading subprocesses at the letter level. The hypothesis of

the phonological loop attested by the activation of this set of

regions would be consistent with the necessity in grapheme-

to-phoneme mapping for storing, maintaining, and assem-

bling intermediate results of the sequential computations

transforming letters to sounds to compute words or

pseudowords final pronunciations.1

Semantic access

Since understanding is the ultimate goal of reading, se-

mantic access is known to be achieved in normal subjects

whatever route is used to access words. For this reason,

clusters of activations supposedly related to semantics

should combine contrasts specific for both routes. We dis-

tinguished three clusters that were good candidates for suchan access to the meanings of words read, as they were

constituted by contrasts of both routes or that were not

conclusive with regard to the route involved.

The first cluster, situated in the very posterior portion of

the middle temporal gyrus, has already been described in the

first part of this article, since it is a region that has been

pointed out by Howard as a possible site for the written

lexicon (see Fig. 5 and Table 7). As argued before, this

region rather seems to be an integration node for language

comprehension, since it is a region receiving information

from other modalities than vision, and whose activity is

modulated by semantic demands of tasks.The second cluster lies within the ventral route, in the

posterior part of the inferior temporal gyrus, and is in fact

situated in the prolongation of the occipitotemporal junc-

tion. This area has also been found activated in word read-

ing in blind subjects (Buchel et al., 1998), in oral word

comprehension studies (Binder and Mohr, 1992), and seems

to correspond to the basal temporal language area described

in TMS and evoked potentials studies (Stewart et al., 2001).

This region is supposed to sustain semantic processing of

words and objects (Thompson-Schill et al., 1999) and fits

into a more general view of the ventral route in which

information would spread ventrally from low-level, unimo-dal occipital cortex devoted to the processing of visual

features to gradually more highly integrated processes in

multimodal regions (Nobre et al., 1994). It is of interest to

note that all studies reporting activation in this region have

been conducted with PET techniques, susceptibility artifacts

probably preventing signal detection in the inferior temporal

parts of the brain with fMRI.

The third and last cluster of activation was located in the

triangular part of the inferior frontal gyrus. This more an-

terior region of Broca’s area has been extensively described

in a variety of language studies implying semantic judgment

tasks or verb generation (Poldrack et al., 1999), confirming

its implication in the monitoring of semantic attributes (Pe-

tersen et al., 1988).

Even though these three clusters thought to be involved

in semantics seem to exhibit reliable activation in reading,

very few studies have found conjoined activation of all of

these regions while subjects were reading. This observation

leads us to the question of whether semantic access should

be thought of as a distributed mechanism requiring the

coactivation of a set of distinct brain areas to allow the

emergence of word properties, or whether it could be ac-

complished by the recruitment of only certain of these brain

areas, depending on the tasks demands.

1 As we mentioned earlier, pseudowords–words contrasts may reflect

greater demands on semantics rather than graphophonological conversion,

due to a search for missing representations, compromising the value of

such contrasts in accounting for brain areas involved in indirect route

specific computations. However, in the clusters described in this part,

“pseudowords vs words” contrasts appeared conjointly with other more

specific comparisons in which stimuli only differ with respect to their

graphophonological processing demands (e.g., word vs picture, word read

aloud vs word read silently, and visual word rhyming vs visual word

spelling). The conjoint activation of these clusters for specific and

pseudowords vs words contrasts makes it more likely to enlighten brain

areas actually involved in the computations needed to transform a written

word into its phonological counterpart.




Conclusions

This metanalysis based on the gathering and spatial seg-

regation of activation peaks obtained in reading studies

revealed an overall reliability of published results. Despite

methodological and experimental differences inherent to the

comparison of studies issued in worldwide laboratories, aconsensus can be drawn within the technique’s spatial lim-

itation as to which sites are critical for identified processes.

The main result consists of the demonstrated suitability

of the dual route model framework to account for observed

reading activations. The failure for discovering a brain re-

gion dedicated to the storage of visual word-form shapes led

us to renounce the concept of written word lexicon, in favor

of the view of a common prelexical stage necessary for the

segmentation and classification of word-like stimuli. Fur-

ther evidence is however needed to assess this orthographic

specialization supposed to take place at the occipitotempo-

ral junction, on the occipitotemporal sulcus separating the

fusiform gyrus from the ventral inferior temporal cortex.

Visual word access is thought to rely on two different

routes summed up in Fig. 6.2 Access through the phonolog-

ical route would be performed thanks to the recruitment of

regions dedicated to phonological analysis and expertise

mainly situated in the superior temporal gyrus or along the

middle part of the superior temporal sulcus. This route

would also require the participation of regions supporting

working memory processes necessary for storing and main-

taining intermediate grapheme-to-phoneme computation re-

sults situated in the opercular part of Broca’s area and the

supramarginal gyrus. Direct access would be accomplished

through direct association from prelexical processing re-gions (i.e., the occipitotemporal junction) to areas devoted

to the semantic processing. These areas that enable the

access to the meaning and properties of words read are the

basal temporal language area, situated anteriorly to the oc-

cipitotemporal junction in the ventral route, the posterior

middle temporal region (very close to the posterior part of

the superior temporal sulcus), and the triangular part of

Broca’s area.

Rather than confirming approaches postulating the exis-

tence of regions specialized in the processing of written

language (e.g., written word lexicon), these results seem to

indicate that brain areas critical for reading tend to berecruited also by other cognitive domains such as object

perception, oral language comprehension, or phonological

analysis, arguing in favor of a colonization of existing brain

resources through individual’s reading experience to

achieve decoding and semantic access.

Acknowledgments

We thank Laure Zago and Emmanuel Mellet for thought-

ful comments on the manuscript. We are grateful to the two

anonymous referees, the constructive comments of which

allowed us to substantially improve the manuscript. This

work was presented in part at the 8th International Confer-

ence on Functional Mapping of the Human Brain, June 2– 6

2002, Sendai, Japan.

References

Adams, R.B., Janata, P., 2002. A comparison of neural circuits underlying

auditory and visual object categorization. NeuroImage 16, 361–377.

Bar, M., Tootell, R.B., Schacter, D.L., Greve, D.N., Fischl, B., Mendola,

J.D., Rosen, B.R., Dale, A.M., 2001. Cortical mechanisms speci fic to

explicit visual object recognition. Neuron 29, 529 –535.

Beauregard, M., Chertkow, H., Bub, D., Murtha, S., Dixon, R., Evans, A.,

1997. The neural substrates for concrete, abstract, and emotional word

lexica: a positron emission tomography. J. Cog. Neurosci. 9, 441– 461.

Becker, J.T., MacAndrew, D.K., Fiez, J.A., 2002. A comment on the

functional localization of the phonological storage subsystem of work-

ing memory. Brain Congn. 41, 27–38.

Binder, J.R., Mohr, J.P., 1992. The topography of callosal reading path-

ways: A case-control analysis. Brain 115 (Pt. 6), 1807–1826.

Bookheimer, S.Y., Zef firo, T.A., Blaxton, T., Gaillard, W., Theodore, W.,

1995. Regional cerebral blood flow during object naming and word

reading. HBM 3, 93–106.Bookheimer, S.Y., Zef firo, T.A., Blaxton, T.A., Gaillard, W.D., Malow, B.,

Theodore, W.H., 1998. Regional cerebral blood flow during auditory

responsive naming: evidence for cross-modality neural activation.

NeuroReport 9, 2409 –2413.

Booth, J.R., Burman, D.D., Meyer, J.R., Gitelman, D.R., Parrish, T.B.,

Mesulam, M.M., 2002. Functional anatomy of intra- and cross-modal

lexical tasks. NeuroImage 16, 7–22.

Brett, M., Johnsrude, I.S., Owen, A.M., 2002. The problem of functional

localization in the human brain. Nat. Rev. Neurosci. 3, 243–249.

Buchel, C., Price, C., Friston, K., 1998. A multimodal language region in

the ventral visual pathway. Nature 394, 274 –277.

Cappa, S.F., Perani, D., Schnur, T., Tettamanti, M., Fazio, F., 1998. The

effect of semantic category and knowledge type on lexial-semantic

access: a PET study. NeuroImage 8, 350 –359.

Chee, M.W., OCraven, K.M., Bergida, R., Rosen, B.R., Savoy, R.L., 1999.Auditory and visual word processing studied with fMRI. Human Brain

Mapping 7, 15–28.

Cohen, L., Dehaene, S., Naccache, L., Lehericy, S., Dehaene-Lambertz, G.,

Henaff, MA., Michel, F., 2000. The visual word form area: spatial and

temporal characterization of an initial stage of reading in normal

subjects and posterior split brain patients. Brain 123, 291–307.

Cohen, L., Lehericy, S., Chochon, F., Lemer, C., Rivaud, S., Dehaene, S.,

2002. Language-specific tuning of visual cortex? Functional properties

of the Visual Word Form Area. Brain 125, 1054 –1069.

Coltheart, M., Curtis, B., Atkins, P., Haller, M., 1993. Models of reading

aloud: dual-route and parallel-distributed-processing approaches.

Psych. Rev. 100, 589 – 608.

Coltheart, M. Rastle, K. 1994. Serial processing in reading aloud: evidence

for dual route models of reading. J. Exp. Psych. 6, 1197 –1211.

2 This model of word access does not aim at representing exhaustively

the network activated during reading, but rather to underline the most

reliable sites of activations whose contribution has been previously dis-

cussed in the literature. Other regions such as the bilateral precentral or

cerebellum regions have been reliably found activated but rarely discussed,

and the implication of the homologues of the presented regions has been

described, even if with a much lesser consistency.




Dehaene, S., Le Clec’H, G., Poline, J.B., Le Bihan, D., Cohen, L., 2002.

The visual word form area: a prelexical representation of visual words

in the fusiform gyrus. NeuroReport 13, 321–325.

Dehaene, S., Naccache, L., Cohen, L., LeBihan, D., Mangin, J.F., Poline,

J.B., Riviere, D., 2001. cerebral mechanisms of word masking and

unconcious repetition priming. Nature 4, 752–758.

De jerine, M.J., 1892. Contribution a l’etude anatomo-pathologique et clin-

ique des differentes varietes de cecite verba le. Mem. Soc. Biol. 61–90.

Fiebach, C.J., Friederici, A.D., Muller, K., von Cramon, D.Y., 2002. fMRI

evidence for dual routes to the mental lexicon in visual word recogni-

tion. J. Cogn. Neurosci. 14, 11–23.

Fiez, J.A., 1997. Phonology, semantics and the role of the left interior

prefrontal cortex. Hum. Brain. Mapp. 5, 79 – 83.

Fiez, J.A., Balota, D.A., 1999. Effects of lexicality, frequency, and spelling

to sound consistency on the functionnal anatomy of reading. Neuron

24, 205–218.

Fiez, J.A., Raife, E.A., Balota, D.A., Schwarz, J.P., Raichle, M.E., 1996. A

positron emission tomography study of the short-term maintenance of

verbal information. J. Neurosci. 16, 808 – 822.

Gauthier, I., Tarr, M.J., Moylan, J., Skudlarski, P., Gore, J.C., Anderson,

A.W., 2000. The fusiform ‘face area’ is part of a network that processes

face at the individual level. J. Cogn. Neurosci. 12, 495–504.

Hagoort, P., Indefrey, P., Brown, C., Herzog, H., Steinmetz, H., Seitz, R.J.,1999. The neural circuitry involved in the reading of German words

and pseudowords: a PET study. J. Cogn. Neurosci. 11, 383 –398.

Herbster, A.N., Mintun, M.A., Nebes, R.D., Becker, J.T., 1997. Regional-

cerebral blood flow during word and nonword reading. Human Brain

Mapping 5, 84 –92.

Horwitz, B., Rumsey, J.M., Donohue, B.C., 1998. Functional connectivity

of the angular gyrus in normal reading and dyslexia. Proc. Natl. Acad.

Sci. USA 95, 8939 – 8944.

Howard, D., Patterson, K., Wise, R., Brown, W.D., Friston, K., Weiller, C.,

Frackowiak, R.S.J., 1992. The cortical localization of the lexicons.

Brain 115, 1769 –1782.

Indefrey, P., Kleinschmidt, A., Merboldt, K.D., Kruger, G., Brown, C.,

Hagoort, P., Frahm, J., 1997. Equivalent responses to lexical and

nonlexical visual stimuli in occipital cortex: a functional magnetic

resonance imaging study. NeuroImage 5, 78 – 81.Jernigan, T.L., Ostergaard, A.L., Law, I., Svarer, C., Gerlach, C., Paulson,

O.B., 1998. Brain activation during word identification and word rec-

ognition. NeuroImage 8, 93–105.

Kiehl, K.A., Liddle, P.F., Smith, A.M., Mendrek, A., Forster, B.B., Hare,

R.D., 1999. Neural pathways involved in the processing of concrete

and abstract words. HBM 7, 225–233.

Mazard, A., Mazoyer, B., Etard, O., Tzourio-Mazoyer, N., Kosslyn, S.M.,

Mellet, E., 2002. Impact of fMRI acoustic noise on the functional

anatomy of visual mental imagery. J. Cogn. Neurosci. 14, 172–186.

Mechelli, A., Friston, K.J., Price, C.J., 2000. The effects of presentation

rate during word and pseudoword reading: a comparison of PET and

fMRI. J. Cogn. Neurosci. 12 (Suppl. 2), 145–156.

Mechelli, A., Gorno-Tempini, M.L., Price, C.J., 2003. Neuroimaging stud-

ies of word and pseudoword reading: consistencies, inconsistencies and

limitations. J. Cogn. Neurosci. 15, 260 –271.Mellet, E., Petit, L., Mazoyer, B., Denis, M., Tzourio, N., 1998. Reopening

the mental imagery debate: lessons from functional anatomy. Neuro-

Image 8, 129 –139.

Mellet, E., Tzourio-Mazoyer, N., Bricogne, S., Mazoyer, B., Kosslyn,

S.M., Denis, M., 2000. Functional anatomy of high-resolution visual

mental imagery. J. Cogn. Neurosci. 12, 98 –109.

Menard, M.T., Kosslyn, S.M., Thompson, W.L., Alpert, N.M., Rauch,

S.L., 1996. Encoding words and pictures: a positron emission tomog-

raphy study. Neuropsychologia 34, 185–194.

Moore, C.J., Price, C., 1999. Three distinct ventral occipitotemporal re-

gions for reading and object naming. NeuroImage 10, 181–192.

Morton, J., Patterson K. 1980. A new attempt at an interpretation, or, an

attempt at a new interpretation, in: Coltheart, M., Patterson, K., Mar-

shall, J.C. Deep Dyslexia, Routledge & Kegan Paul, London.

Mummery, C.J., Patterson, K., Hodges, J.R., Price, C.J., 1998. Functional

neuroanatomy of the semantic system: divisible by what? J. Cog.

Neurosci. 10, 766 –777.

Murtagh, F. 1985. Multidimensional Clustering Algorithms. In COMP-

STAT Lectures 4.

Nobre, A.C., Allison, T., McCarthy, G., 1994. Word recognition in the

human inferior temporal lobe. Nature 372, 260 –263.

Paulesu, E., Frith, C.D., Frackowiak, R.S., 1993. The neural correlates of the verbal component of working memory. Nature 362, 342–345.

Paulesu, P., McCrory, E., Fazio, F., Menoncello, L., Brunswick, N., Cappa,

S.F., Cotelli, M., Cossu, G., Corte, M., Lorusso, M., Pesenti, S.,

Gallagher, A., Perani, D., Price, C., Frith, C.D., Frith, U., 2000. A

cultural effect on brain function. Nature 3, 91–96.

Perani, D., Cappa, S.F., Schnur, T., Tettamanti, M., Collina, S., Rosa,

M.M., Fazio, F., 1999. The neural correlates of verb and noun process-

ing—a PET study. Brain 122, 2337–2344.

Petersen, S.E., Fox, P.T., Posner, M.I., Mintun, M., Rauchle, M.E., 1989.

Positron emission tomography studies of the processing of single

words. J. Cogn. Neurosci. 1, 153–170.

Petersen, S.E., Fox, P.T., Posner, M.I., Mintun, M.A., Raichle, M.E., 1988.

Positron emission tomographic studies of the cortical anatomy of sin-

gle-word processing. Nature 331, 585–589.

Petersen, S.E., Fox, P.T., Snyder, A.Z., Raichle, M.E., 1990. Activation of extrastriate and frontal cortical areas by visual words and word-like

stimuli. Science 249, 1041–1044.

Poldrack, R.A., Wagner, A.D., Prull, M.W., Desmond, J.E., Glover, G.H.,

Gabrieli, J.D., 1999. Functional specialization for semantic and pho-

nological processing in the left inferior prefrontal cortex. NeuroImage

10, 15–35.

Price, C.J., 1997. Functional anatomy of reading, in: Human Brain Func-

tion, Academic Press, San Diego, pp. 301–328.

Price, C.J., Moore, C.J., Frackowiak, R.J., 1996a. The effect of varying

stimulus rate and duration on brain activity during reading. NeuroIm-

age 3, 40 –52.

Price, C.J., Moore, C.J., Humphreys, G.W., Wise, R.J., 1997. Segregating

semantic from phonological processes during reading. J. Cogn. Neu-

rosci. 9, 727–733.

Price, C.J., Wise, R.S., Frackowiak, R.J., 1996b. Demonstrating the im-

plicit processing of visually presented words and pseudowords. Cereb.

Cortex 6, 62–70.

Price, C.J., Wise, R.S., Watson, J.G., Patterson, K., Howard, D., Frack-

owiak, R.J., 1994. Brain activity during reading: The effect of exposure

duration and task. Brain 117, 1255–1269.

Pugh, K.R., Shaywitz, B.A., Shaywitz, S.E., Constable, R.T., Skudlarski,

P., Fulbright, R.K., Bronen, R.A., Shankweiler, D.P., Katz, L.,

Fletcher, J.M., Gore, J.C., 1996. Cerebral organization of component

processes in reading. Brain 119, 1221–1238.

Rumsey, J.M., Horwitz, B., Donohue, B.C., Nace, K., Maisog, J.M.,

Andreason, P.J., 1997. Phonological and orthographic components of

word recognition: A PET-rCBf study. Brain 120, 739 –759.

Sakurai, Y., Momose, T., Iwata, M., Sudo, Y., Ohtomo, K., Kanazawa, I.,

2000. Different cortical activity in reading of kanji words, kana wordsand kana nonwords. Cognitive Brain Res., 111–115.

Simos, P.G., Breier, J.I., Fletcher, J.M., Foorman, B.R., Castillo, E.M.,

Papanicolaou, A.C., 2002. Brain mechanisms for reading words and

pseudowords: an integrated approach. Cereb. Cortex 12, 297–305.

Simos, P.G., Breier, J.I., Wheless, J.W., Maggio, W.W., Fletcher, J.M.,

Castillo, E.M., Papanicolaou, A.C., 2000. Brain mechanisms for read-

ing: the role of the superior temporal gyrus in word and pseudoword

naming. NeuroReport 11, 2443–2447.

Small, S.L., Noll, D.C., Perfetti, C.A., Hlustik, P., Wellington, R., Schnei-

der, W., 1996. Localizing the lexicon for reading aloud: replication of

a PET study using fMRI. NeuroReport 7, 961–965.

Stewart, L., Meyer, B.U., Frith, U., Rothwell, J., 2001. Left posterior BA37

is involved in object recognition: a TMS study. Neuropsychologia 39,

1– 6.




Stromswold, K., Caplan, D., Alpert, N., Rauch, S., 1996. Localization of

syntactic comprehension by positron emission tomography. Brain

Lang. 52, 452– 473.

Talairach, J., Tournoux, P., 1988. Co-planar-stereotaxic atlas of the human

brain 3-dimensional-proportional system: an approach to cerebral im-

aging. Stuttgart, New York.

Tan, L.H., Feng, C.M., Fox, P.T., Gao, J.H., 2001. An fMRI study with

written Chinese. NeuroReport 12, 83– 88.

Thompson-Schill, S.L., Aguirre, G., D’Esposito, M., Farah, M.J., 1999. A

neural basis for category and modality specific of semantic knowledge.

Neuropsychologia 37, 671– 676.

Tokunaga, H., Nishikawa, T., Ikejiri, Y., Nakagawa, Y., Yasuno, F.,

Hashikawa, K., Nishimura, T., Sugita, Y., Takeda, N., 1999. Different

neural substrates for Kanji and Kana writing: a PET study. NeuroRe-

port 10, 3315–3319.

Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard,

O., Delcroix, N., Mazoyer, B., Joliot, M., 2002. Automated anatomical

labeling of activations in SPM using a macroscopic anatomical parcel-

lation of the MNI MRI single-subject brain. NeuroImage 15, 273–289.

Van Turennout, Ellmore T., Martin, A. 2000. Long-lasting cortical plas-

ticity in the object naming system. Nature 3, 1329 –1334.

Vandenberghe, R., Price, C., Wise, R., Josephs, O., Frackowiak, R.J., 1996.

Functional anatomy of a common semantic system for words and

pictures. Nature 383, 254 –256.

Warrington, E.K., Shallice, T., 1980. Word-form dyslexia. Brain 103,

99 –112.

Wise, R., Chollet, F., Hadar, U., Friston, K.J., Hoffner, E., Frackowiak,

R.S., 1991. Distribution of cortical networks involved in word com-

prehension and word retrieval. Brain 114, 1803–1817.

Xu, B., Grafman, J., Gaillard, W.D., Ishii, K., Vega-Bermudez, F., Pietrini,

P., Reeves-Tyer, P., DiCamillo, P., Theodore, W., 2001. Conjoint and

extended neural networks for the computation of speech codes: the

neural basis of selective impairment in reading words and

pseudowords. Cereb. Cortex 11, 267–277.


Documents

Doble Ruta