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Brain and Cognition 58 (2005) 217–225

Smooth pursuit eye movements are associated withphonological awareness in preschool children

D. Callua, I. Giannopulua, S. Escolanoa, F. Cusinb, M. Jacquier-Rouxb, G. Dellatolasa,*

a INSERM U.472, Epidemiology et Biostatistics, Villejuif, Franceb Health Services of the National Department of Education, France

Accepted 30 November 2004Available online 22 January 2005

Abstract

Phonological awareness is strongly related to reading ability, but reports are more conflicting concerning the association of highlevel oculomotor skills with reading. Here, we show that phonological awareness is specifically associated with the ability to performsmooth pursuit eye movements in preschool children. Two large independent samples of preschool children (n = 838 and n = 732)aged 5–6.4 years, without history of neurological disorder, were examined by school medical doctors for visual and oculomotorproblems. Nineteen percent of the children in the first sample and 14% in the second failed at the clinical evaluation of smooth pur-suit eye movements, and 17 and 15%, respectively, presented another visual or oculomotor problem. Ten short cognitive tests wereperformed by the same children. Visual and oculomotor problems other than a failure on smooth pursuit were not consistentlyrelated to the cognitive tasks, with one exception, the visual recognition of letters. Children who failed at smooth pursuit obtainedlower scores at a number of cognitive tasks, and especially phonological awareness tasks and copy of visually presented trajectories.Poor working memory and/or failure of anticipation during the tracking of a visual or auditory stimulus related to frontal corteximmaturity may explain these associations in preschool children.� 2004 Elsevier Inc. All rights reserved.

Keywords: Phonological awareness; Smooth pursuit eye movements; Working memory; Frontal cortex

1. Introduction

According to a common current opinion, develop-mental dyslexia, a specific difficulty in learning to read,is frequently related to phonological problems (Ramuset al., 2003). Phonological awareness, i.e., an inabilityto manipulate in an abstract form the sound constitu-ents of oral language is strongly related to reading skill(Castles & Coltheart, 2004; Lundberg, Frost, & Peter-son, 1988; Rohl & Pratt, 1995). It is generally acceptedthat low-level visual deficits, such as visual acuity, arenot major causes of poor reading performance (Ameri-can Academy of pediatrics, 1998; Evans, Drasdo, &

0278-2626/$ - see front matter � 2004 Elsevier Inc. All rights reserved.

doi:10.1016/j.bandc.2004.11.008

* Corresponding author. Fax: +33 1 45 59 51 69.E-mail address: dellatolas@vjf.inserm.fr (G. Dellatolas).

Richards, 1994a; Evans, Drasdo, & Richards, 1994b).Reports are more conflicting concerning an involvementof high-level visual and oculomotor difficulties in dys-lexia (Stein, Riddell, & Fowler, 1988). Some authors re-ported that dyslexic children made more erratic eyemovements than controls not only during reading butalso when trying to follow sequentially illuminated lightsources (Pavlidis, 1981), equidistantly spaced digits(Pavlidis, 1985), or other smoothly moving targets atlow velocity (Black, Collins, De Roach, & Zubrick,1984; Eden, Stein, Wood, & Wood, 1994; Eden, Stein,Wood, & Wood, 1995a; Eden, Stein, Wood, & Wood,1995b), however other reports did not confirm this asso-ciation (Brown et al., 1983; Stanley, Smith, & Howell,1983; Olson, Kliegl, & Davidson, 1983; Ygge, Lenner-strand, Rydberg, Wijecoon, & Pettersson, 1993).

218 D. Callu et al. / Brain and Cognition 58 (2005) 217–225

Smooth pursuit eye movements and reading skillsshare same cognitive components, such as attentionand working memory, and involve common brainareas.

Smooth pursuit improves during infancy and child-hood. In the newborn, the visual tracking of a movingstimulus is saccadic or steplike, and the eye movementsalways lag behind the movement of the stimulus, ratherthan predicting its trajectory. This absence of anticipa-tion of the position of the visual stimulus, which isincompatible with successful smooth pursuit, is gener-ally attributed to the immaturity of the prefrontal cor-tex, especially the frontal eye fields (Johnson, 1998).Smooth pursuit improves from 0 to 12 months (Rich-ards, 2001), and there is also evidence that binocularcoordination, latency of saccades, coordination betweensaccade and vergence movements, as well as smoothpursuit improve up to 12 or 15 years of age (Castellanoset al., 2000; Ross, Radant, & Hommer, 1993; Yang,Bucci, & Kapoula, 2002; Yang & Kapoula, 2003).

A frontal cortex involvement was postulated in dys-lexia (Levine, 1990), and also indirectly suggested byauthors who emphasized impairments of working mem-ory (Adams & Gathercole, 2000) or impaired awarenessof motor-articulatory gestures (Heilman, Voeller, &Alexander, 1996) in children with specific readingdifficulties.

Smooth pursuit as well as dyslexia are related toattention mechanisms. Smooth pursuit would requirenot only visual attention, but also keeping eye trackingin mind as a mental event (Chen, Holzman, & Nakay-ama, 2002), and voluntary control closely tied to atten-tional selection (Pashler, 1998). Language and readingskills are associated with attention and working memorydeficits according to numerous epidemiological (Beitch-man, Hood, Rochon, & Peterson, 1989; Levy, Hay,McLaughlin, Wood, & Waldman, 1996), clinical (Javor-sky, 1996; Montgomery, 2000) and experimental studies(Adams & Gathercole, 2000; Asbjornsen & Bryden,1998; Facoetti, Lorusso, Paganoni, Umilta, & Mascetti,2003).

Many brain areas potentially involved in reading dif-ficulties are also involved in the smooth pursuit eyemovements system (Tanabe, Tragellas, Miller, Ross, &Freedman, 2002): area V5/MT+ (Groh, Born, & New-some, 1997), posterior parietal cortex (Petit & Haxby,1999), frontal cortex (FEF, SEF, and cingulate eye field)(Gaymard & Pierrot-Deseilligny, 1999), and cerebellum(Fukushima, 2003).

Smooth visual pursuit implies motion perception andactivation of area V5/MT+, which is part of the dorsalvisual stream receiving inputs from the magnocellularsystem. A visual magnocellular deficit in dyslexics wassuggested, following a report of anatomical defects inthe magnocellular part of the Lateral GeniculateNucleus (Galaburda & Livingstone, 1993). Impaired

perception of coherent motion in dyslexics has beenrepeatedly reported (Cornelissen, Richardson, Mason,Fowler, & Stein, 1995; Hansen, Stein, Orde, Winter, &Talcott, 2001; Hill & Raymond, 2002; Iles, Walsh, &Richardson, 2000; Kubova, Kuba, Peregrin, & Nova-kova, 1995; Ridder 3rd, Borsting, & Banton, 2001; Ro-mani et al., 2001). A functional brain imaging studyfound impaired activation of area V5/MT by presenta-tion of moving stimuli in dyslexics (Eden et al., 1996a,Eden, VanMeter, Rumsey, & Zeffiro, 1996b), whereasa whole-scalp neuromagnetic recording study foundnormal activation of V5 by motion stimuli in these sub-jects (Vanni, Uusitalo, Kiesila, & Hari, 1997). A general-ized magnocellular deficit in dyslexics has beenproposed, involving not only the visual magnocellularsystem, but also ‘‘magnocellular homologues’’ of otherauditory or motor systems (Galaburda & Livingstone,1993). A parietal cortex dysfunction has been proposedfor this putative supramodal magnocellular deficit (Ileset al., 2000; Vidyasagar, 1999).

The magnocellular hypothesis in dyslexia has beenquestioned. Magnocellular impairment was not foundin 20 dyslexic boys (Kronbichler, Hutzler, & Wimmer,2002). Detailed neuropsychological testing of 16 dyslexicuniversity students showed magnocellular deficits inonly two of them (Ramus et al., 2003). A short term per-ceptual memory problem rather than a magnocellulardeficit was proposed as the characteristic difficulty ofdyslexic adults; indeed many dyslexics showed a specificdifficulty in tasks requiring to retain an accurate tracefor subsequent comparison in retain-and-compare tem-poral-forced choice paradigms (Amitay, Ben-Yehudah,Banai, & Ahissar, 2002; Ben-Yehudah, Sackett, Mal-chi-Ginzberg, & Ahissar, 2001).

A cerebellar deficit has also been suggested in devel-opmental dyslexia, based on behavioural characteristicsof some dyslexics (difficulties in motor skill automatiza-tion, balance, etc.) (Nicolson, Fawcett, & Dean, 2001),also supported by anatomical studies measuring cerebel-lum volumes in dyslexics and controls (Eckert et al.,2003).

The above observations incited us to study smoothpursuit eye movements in children just before readingacquisition and to examine the relationships betweensmooth pursuit and well-known preschool skills stronglyassociated with later reading performance, such as pho-nological awareness.

2. Participants and method

2.1. The Creusot-Montceau-les-Mines study

The general aim of this study in all public and pri-vate preschools and schools of the community of Creu-sot-Montceau-les-Mines, in Saone-et-Loire, France,

Table 1

2001 sample 2002 sample

N 838 732Sex (% boys) 53.1 50.6Age: mean (SD) 5.6 (0.3) 5.9 (0.3)

Visual examination (%)Right eye visual acuity < 8 8.1 5.4Left eye visual acuity < 8 7.2 5.1Hypermetropia 6.7 6.3Binocular vision problem 2.6 5.7Vergence problem 3.7 3.9Heterophoria 1.6 2.6Smooth pursuit failure 18.7 14.3

Cognitive examination: mean (SD)Phonological awareness (PAW) 15.6 (5.9) 16.5 (5.7)Vocabulary (VOC) 19.1 (3.9) 20.0 (4.4)Oral comprehension (COM) 7.5 (1.7) 7.6 (1.7)Visual recognition of letters (VRL) 15.8 (3.2) 16.3 (3.1)Oral repetition of sentences (REP) 13.7 (2.9) 13.9 (3.8)Verbal fluency (VFL) 5.1 (2.0) 5.6 (2.2)Cancellation task (CAN) 13.2 (4.1) 13.3 (3.8)Path copy (PAT) 4.1 (1.9) 4.2 (1.9)

D. Callu et al. / Brain and Cognition 58 (2005) 217–225 219

was to specify the factors related to learning difficultiesin the general population (Callu, Jacquier-Roux, Cusin,Giannopulu, & Dellatolas, 2003). In France, a verylarge majority of children are in preschools from age3 to 6 years, before entering primary school. In theCreusot-Montceau-les-Mines Community the vastmajority of (pre-)schools are public. The study beganduring the 2001–2002 school year, including all chil-dren aged 3–6 years who were in the pre-schools ofthe community. These children will be followed untilthird grade (i.e., 8–9 years of age). During the last yearof the preschool period, when the children are aged 5–6years, a systematic medical examination was performedby medical doctors attached to the National Depart-ment of Education. This included an examination of vi-sion and audition, as well as a cognitive batteryfocusing, mainly but not exclusively, on languagedevelopment. Vision examination included a clinicalassessment of smooth pursuit eye movements. Lan-guage assessment included tasks evaluating phonologi-cal awareness.

2.2. Participants

The present data concern 838 pupils at the last year oftheir preschool career during the school year 2001–2002(referred in the following as ‘‘2001 sample’’), and 732children at the last year of their preschool career duringthe school year 2002–2003 (‘‘2002 sample’’). Exclusioncriteria were: (i) age more than 6 years and 5 monthsat medical and cognitive examination; (ii) history of dis-ease or accident with probable neurological conse-quence, such as meningitis, epilepsy or traumatic headinjury with coma. Children with such a history presentedsignificantly lower performances at many cognitivetasks, as well as more visual problems and especiallypoorer smooth pursuit. Children with imperfect hearingat the examination of audition were not excluded, as thisvariable was not significantly related to the cognitive orthe visual variables. Table 1 gives a description of theparticipants.

Visual and oculomotor examination included: (i) vi-sual acuity from a distance of 5 m (Snellen; ‘‘trouble’’if less than 8/10); (ii) search for hypermetropia; (iii) bin-ocular vision (Lang II test); (iv) vergence; (v) search forheterophoria; and (vi) smooth pursuit. Smooth pursuiteye movements were tested by means of the subject�sability to follow a cube, held by the doctor, while mak-ing a smooth movement in form of lying ‘‘8’’ inside thesquare delimited by the two shoulders of the child, bythe top of his/her head and by the base of his/her neck.The stimulus was distant of 40 cm from the root of thenose of the child. The child was asked to not move thehead but only his/her eyes, and to announce each rota-tion of the cube imposed by the examiner during its slow‘‘lying 8’’ displacement. Before the study, all the partic-

ipating medical school doctors underwent demonstra-tion and training sessions.

The pre-school cognitive tasks included thefollowing:

1. Phonological awareness (PAW) was evaluated bythree syllable-manipulation oral tasks: rhyme identifi-cation, syllabic counting, and syllabic segmentation.In the rhyme task, after oral presentation of the targetword (eight items), three words were orally presentedand the child had to recognize the word that rhymeswith the target. The position of the correct word wasrandom. The score corresponds to the number of cor-rect answers. In the syllabic counting task, the childhad to count the number of syllables of bi- orthree-syllabic words (five items) presented to him/her orally. The score corresponds to the number ofcorrect answers. In the syllabic segmentation task,the child had to delete one syllable of bi-syllabicwords (10 items) presented orally (e.g., repeat ‘‘mar-teau’’ (hammer) without saying ‘‘teau,’’ expectedanswer, ‘‘mar’’). The score corresponds to the num-ber of correct answers. A total phonological aware-ness score was computed, summing the score of thethree tasks (max = 23) (Zorman & Jacquier-Roux,1999).

2. Vocabulary (VOC): the child was asked to point tothe image illustrating the best a word presented orallyby the examiner, among six images. There were 15items. The child received 2 points if he/she foundthe best answer, 1 point for a second acceptable butnot the best answer, and 0 points for the other fourchoices (Deltour & Hupkens, 1980).

220 D. Callu et al. / Brain and Cognition 58 (2005) 217–225

3. Oral comprehension task (COM): a sentence wasread once by the examiner. The child had to showthe corresponding image among four. There were 10items. One point was given for each correct answer(Lecocq, 1996).

4. Visual recognition of letters (VRL) (Fig. 1A) evalu-ated child�s ability to recognise letters and spacesbetween the letters (for instance, to avoid confusionof ‘‘qd’’ with ‘‘cpl’’). The child looked at a sequenceof letters (3–5) and then had to indicate these lettersin the same order on a frame containing 12 lettersspaced out, which was presented simultaneously withthe target letter sequence. Naming of the letters wasnot asked. The score was the number of letters cor-rectly recognized in five trials.

5. Sentences repetition task (REP): the child had to repeattwo sentences pronounced by the examiner (‘‘il y a ungarcondont la casquette est verte’’ [there is a boywhomthe cap is green], and ‘‘la fille a ete interrogee par lerobot’’ [the girl was questioned by the robot]). Eachsentence was coted from 0 to 8 points according tothe number of words correctly repeated (NB: ‘‘il y a’’[there is] counted for one word).

6. Semantic verbal fluency (VFL): the child was asked tocite as many animal names as possible in 20 s. Thescore was the number of different animal names cited.

7. Bells cancellation test (CAN): the child had to crossout with a pencil all the small bells randomly inter-spersed on a sheet containing a variety of small draw-ings. The score was the number of bells crossed out in1 min (maximum possible score = 35, the number ofbells on the sheet).

Fig. 1. Visual recognition of letters task (A) and an example of thepath copy task (B).

8. Path copy (PAT) was evaluated by the teacher. Thechild had to copy six figures of increasing complexity.The child could see the original figure all along thecopying time. One point was given for each correctcopy. One example of this task is given in Fig. 1B.

3. Data management and statistical analysis

The smooth pursuit eye movements task was codedas a binary variable contrasting ‘‘success’’ (trackingwas regular, without any stop, movement of the heador movement of the body, and the eyes were synchro-nous) and ‘‘failure’’ (presence of movements of the heador the body, irregularity, stops, asynchronous move-ment of the two eyes). This new variable will be named‘‘pursuit’’ in the following. All other visual items weredichotomized (i.e., presence/absence of the correspond-ing trouble), and also summed up in a single binary var-iable, named ‘‘other visual problem’’ in the following,denoting existence of at least one visual problem amongvisual acuity, hypermetropia, vergence, binocular vision,and heterophoria.

All analyses were performed with SAS 8.2 release. Ef-fect of pursuit on each cognitive task was estimated andtested in generalized linear model (GLM procedure),where age and ‘‘other visual problem’’ were also in-cluded as explanatory variables. Then, the different cog-nitive tasks significantly related with pursuit have beenput together as explanatory variables in a logistic modelfor pursuit (LOGISTIC procedure with backward elim-ination of variables), to take into account their interrela-tions and see which ones where specifically linked topursuit.

Although multiple comparisons were performed, nocorrection for p values were done. In effect, we consid-ered results from the 2002 sample as validation of theresults from the 2001 sample.

4. Results

4.1. Description of the samples (Table 1)

The two samples consisted in 838 and 732 childrenfor 2001 and 2002 respectively. Table 1 describes thetwo samples. In the 2002 sample compared to the 2001sample, age was significantly higher (p < .0001), pursuittroubles were less frequent (p = .03), visual acuity prob-lems were less frequent (p = .04) and binocular visionproblems were more frequent (p = .003).

Results at cognitive testing were consistent and sim-ilar in the 2001 and 2002 samples, with slightly betterperformances in 2002 probably due to the age differ-ence. Despite the narrow age range, the effect of age

D. Callu et al. / Brain and Cognition 58 (2005) 217–225 221

was significant for almost all tasks, with better perfor-mances in the older than in the younger children. Asignificant age effect was also observed for smooth pur-suit in the 2001 sample with mean age slightly lower inchildren who failed this task (p < .01). Thus, all thefollowing analyses were performed after taking intoaccount this age effect.

4.2. Relationships between visual and cognitive variables

Nineteen percent of the children in the first study and14% in the second failed at the clinical evaluation ofsmooth pursuit eye movements, and 17 and 15%, respec-tively, presented another visual or oculomotor problem.Association between pursuit and ‘‘other visual problem’’was assessed by Fisher�s exact tests and found significant(p = .009 and p < .001 for the 2001 and the 2002 sam-ples, respectively). Fig. 2 illustrates the findings of thegeneralized linear models, with a particular focus onthe link of cognitive tasks with smooth pursuit (Figs.2A and B) and with other visual problems (Figs. 2C

Fig. 2. Illustration of smooth pursuit effect (A and B) on the cognitive taskseffect. Least-squares means and their standard errors for the two smooth pursof other visual problem effect (C and D) on the cognitive tasks through model(D) is for 2002 sample. Least-squares means and their standard errors for th***(p < .001), **(p < .01), and *(p < .05). Abbreviations: SP+, SP�: normaland absence of other visual problem, respectively; PAW: phonological awrecognition of letters; REP: sentence repetition; VFL: semantic verbal fluenc

and D). The relationships were found similar in thetwo samples. Smooth pursuit was associated with mostcognitive tasks, and especially with phonological aware-ness, path copy, and letter recognition. The only cogni-tive task associated with ‘‘other visual problem’’ inaddition to smooth pursuit (i.e., when the effect ofsmooth pursuit was taken into account), was the visualrecognition of letters. For phonological awareness, theR2 statistics, which give the percentage of explained var-iance, were 11% in the 2001 sample and 5% in the 2002sample. These rather small values mean that a largeamount of variability for this cognitive task remainsafter taking into account the mentioned variables. Final-ly, a logistic regression with pursuit as the dependentvariable and backward elimination, selected phonologi-cal awareness and path copy in the 2001 sample, andphonological awareness only in the 2002 sample. When,in the same analyses, phonological awareness was re-placed by its three components (rhymes, syllabic count-ing, and syllabic segmentation), the selected variableswere rhymes, syllabic counting and path copy in 2001;

through models also accounting for age effect and other visual problemuit groups. (A) For 2001 sample and (B) is for 2002 sample. Illustrations also accounting for age and smooth pursuit. (C) For 2001 sample ande two other visual problem groups. Significant effects are signaled byand abnormal Smooth pursuit, respectively; OVP+, OVP�: presenceareness; VOC: vocabulary; COM: oral comprehension; VRL: visualy; CAN: cancellation task; PAT: path copy.

Fig. 3. Percentage of SP� in the five groups defined by the quintiles of phonological awareness. (A) For school-year 2001, and (B) is for school-year2002 (for abbreviations see Fig. 2).

222 D. Callu et al. / Brain and Cognition 58 (2005) 217–225

and rhymes only in 2002. Fig. 3 illustrates the relation-ship between smooth pursuit and phonological aware-ness in the 2001 and the 2002 samples. Both sampleshave been divided into five groups of equal size (quan-tiles), based on increasing phonological awareness re-sults. Fig. 3 shows that the percentage of children withsmooth pursuit failure decreases as the phonologicalawareness improves.

5. Discussion

Children who failed on smooth pursuit obtained low-er scores at many cognitive tasks. This smooth pursuitstatistical effect was especially consistent on the phono-logical awareness tasks. Visual and oculomotor prob-lems other than a failure at smooth pursuit were notconsistently related to the cognitive tasks, with oneexception, the visual recognition of letters. This resultis in accordance with other studies reporting that visualproblems are unlikely to be a major cause of learningand reading difficulties (American Academy of pediat-rics, 1998; Evans et al., 1994a, 1994b, Evans, Drasdo,& Richards, 1996), but it is also in agreement with a

degraded information about where letters are posi-tioned, due to visual problems (Cornelissen et al.,1998a, Cornelissen, Hansen, Hutton, Evangelinou, &Stein, 1998b). In a recent study, Pammer, Lavis, Han-sen, and Cornelissen (2004) reported that sensitivity tothe position of nonalphabetic but letter-like symbolsmay constrain children�s reading accuracy.

The association of smooth pursuit with ‘‘path copy’’suggests that most children used indeed a sequentialprocedure to perform this copy, favored by the presenceof the dots (i.e., they tried to reproduce a trajectory),rather than a global procedure (i.e., capture of the wholepattern and positioning it on the matrix). Adams andGathercole (2000) found that performance in the Corsiblocks test, that tests the ability to retain and reproducea trajectory, was related to speech production (reper-toire of words, length of utterances, and syntactic con-structions) in children aged 4-years; on the contrary,when visuospatial short-term memory was assessed byvisual pattern reproduction (matrices), there was no cor-relation with language skills. These findings agree withreports that reading ability is related to processing ofsequentially presented but not simultaneously presentedstimuli (Eden et al., 1995b).

D. Callu et al. / Brain and Cognition 58 (2005) 217–225 223

Association of visual with auditory impairments hasoften been reported in reading disabled subjects. Dyslex-ics may show a temporal processing deficit in both theauditory and the visual system (Stein & Walsh, 1997;Van Ingelghem et al., 2001). Auditory frequency dis-crimination of two tones occurring in sequence and vi-sual motion sensitivity could influence children�sreading skills (Talcott et al., 2000, 2002, 2003). A visualand auditory perceptual memory impairment leading todifficulties in frequency discrimination tasks requiring atemporal forced choice decision (i.e., in retain-and-com-pare paradigms) has been reported in adult reading dis-abled subjects (Amitay et al., 2002; Ben-Yehudah et al.,2001).

A more specific association between phonologicalawareness and smooth pursuit eye movements is lesswell documented. Eden et al. (1995a) reported that avertical tracking task, testing the child�s ability to followone of many vertical lines down the page using onlytheir eyes, was significantly correlated to phonologicaltasks in a mixed sample of 93 school-children with orwithout reading disability. The same authors also sug-gested a large overlap between visual deficits and phono-logical weakness (Eden et al., 1996b).

Phonological awareness in kindergarten children isrelated to later reading ability (Catts, 1991; Catts, Fey,& Proctor-Williams, 2000; Menyuk et al., 1991), and isimpaired in dyslexics (Pennington, Van Orden, Smith,Green, & Haith, 1990). A recent review questionnedthe presence of a causal link from phonological aware-ness to success in learning to read (Castles & Coltheart,2004). Existing literacy skills influence performance onphonological awareness tasks (Loureiro et al., 2004).The present results show that phonological awarenessand smooth pursuit are significantly correlated in pre-school nonreaders. As smooth pursuit improves withage in school-children (Biscaldi, Fischer, & Hartnegg,2000; Johnson, 1998; Richards, 2001; Tajik-Parvinchi,Lillakas, Irving, & Steinbach, 2003; Yang et al., 2002;Yang & Kapoula, 2003), these data do not necessarilyimply that those children who will present reading dis-ability will also present smooth pursuit difficulties. How-ever, the data strongly suggest that phonologicalawareness and smooth pursuit may share common cog-nitive components, possibly important for later reading.

What smooth pursuit and phonological awarenessmay have in common? In our view, both are ‘‘tracking’’tasks, of a visual target or of an auditory signal, andboth involve working memory (Baddeley, 1992), definedas a mechanism for short-term active storage and forprocessing stored information (Funahashi & Takeda,2002). Memory neurons in the frontal eye fields are nec-essary for the effectiveness and predictive capability ofthe smooth pursuit eye movement system; without thispredictive capability, i.e., anticipation of the positionof the visual target, smooth pursuit is not possible

(Johnson, 1998). The phonological awareness tasks usedin the present study involve active storage of the targetword, to correctly find the successively presented wordwhich rhymes, or to count the syllables or to deleteone syllable. For rhyme identification, it is necessaryto retain the target word in memory in order to compareit with the three successively presented words. This is aretain-and-compare task, and such tasks have been re-ported to be especially difficult in dyslexic subjects (Ami-tay et al., 2002; Ben-Yehudah et al., 2001). For syllabiccounting and syllabic segmentation, it is necessary to re-tain the heard word in mind in order to make an oper-ation on it, that is, segment it into syllables and countthem, or delete one of them.

Smooth pursuit involves the transformation of a vi-sual information to motor commands (eye movements),and phonological awareness involves the transformationof an auditory information (the heard word) to motorcommands (articulation) (Hickok, Bichsbaum, Humph-ries, & Muftuler, 2003). In smooth pursuit, there isanticipation of the position of the visual target (John-son, 1998). It is likely that articulatory anticipationplays some role in phonological awareness, as well asin phonological memory. Heilman et al. (1996) hypoth-esized that impaired phonological awareness in dyslexicchildren may be related to their inability to associate theposition of their articulators with speech sounds, due toa programming or a feedback deficit. The programminghypothesis of Heilman et al., is similar to an articula-tory–anticipation-deficit hypothesis. Another aspect ofverbal working memory, phonological memory, as-sessed for instance by oral repetition of long nonwords,was often reported to be related to language develop-ment (Montgomery, 2000) and future reading ability inchildren (Bishop, North, & Donlan, 1996).

In conclusion, the present data show evidence ofcommon cognitive components in phonological aware-ness and smooth pursuit eye movements. Other studiesshowed that phonological memory, perceptual memoryor processing of sequentially presented stimuli are re-lated to reading performance. Working memory ability,that is short term active storage and processing of visualor auditory information, and anticipation during thetracking of a visual or auditory stimulus related to fron-tal cortex, could account for all these associations. Thecognitive consequences of brain damage which disruptssmooth pursuit need further research.

Acknowledgments

We thank the medical doctors and nurses of NationalDepartment of Education, teachers, parents, and chil-dren of the community of Creusot-Montceau-les-Minesfor their participation. This study was supported byMinistere de l�Education Nationale and Communaute

224 D. Callu et al. / Brain and Cognition 58 (2005) 217–225

Urbaine de Creusot-Montceau-les-Mines. D.C was sup-ported by a grant from Fondation de France.

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