auditory processing disorder in children with reading - brain

Auditory processing disorder in children with readingdisabilities: effect of audiovisual trainingEvelyneVeuillet,1 Annie Magnan,2 Jean Ecalle,2 HungThai-Van1 and Lionel Collet1

1Universite¤ de Lyon, Lyon, F-69003, France, universite¤ Lyon 1, CNRS, UMR 5020, Lyon, F-60007, France, Ho“ pital EdouardHerriot, Pavillon U, Service d’Audiologie et d’Explorations Orofaciales, F-69003 Lyon, France, IFNL, Lyon, F-60003, Franceand 2Universite¤ de Lyon, Bron, F-69676, France, universite¤ Lyon 2, CNRS, EA 3082, Laboratoire EMC, Bron, F-69676, France

Correspondence to: EvelyneVeuillet, Ho“ pital Edouard Herriot, Pavillon U, Service d’Audiologie et d’Explorations Orofaciales,Place d’Arsonval, 69437 Lyon Cedex 03, FranceE-mail: [email protected]

Reading disability is associated with phonological problems which might originate in auditory processing disor-ders.The aim of the present study was 2-fold: first, the perceptual skills of average-reading children and childrenwith dyslexia were compared in a categorical perception task assessing the processing of a phonemic contrastbased on voice onset time (VOT).The medial olivocochlear (MOC) system, an inhibitory pathway functioningunder central control, was also explored. Secondly, we investigated whether audiovisual training focusing onvoicing contrast could modify VOT sensitivity and, in parallel, induce MOC system plasticity. The resultsshowed an altered voicing sensitivity in some children with dyslexia, and that the most severely impairedchildren presented the most severe reading difficulties. These deficits in VOT perception were sometimesaccompanied by MOC function abnormalities, in particular a reduction in or even absence of the asymmetryin favour of the right ear found in average-reading children. Audiovisual training significantly improved readingand shifted the categorical perception curve of certain children with dyslexia towards the average-readingchildren’s pattern of voicing sensitivity. Likewise, in certain children MOC functioning showed increased asym-metry in favour of the right ear following audiovisual training. The training-related improvements in readingscore were greatest in children presenting the greatest changes in MOC lateralization. Taken together, theseresults confirm the notion that some auditory system processing mechanisms are impaired in children withdyslexia and that audiovisual training can diminish these deficits.

Keywords: VOT; auditory efferent; lateralization; training; dyslexia

Abbreviations: MOC=medial olivocochlear; VOT=voice onset time

Received April 12, 2007. Revised September 4, 2007. Accepted September 5, 2007. Advance Access publication October 5, 2007

IntroductionFailure to acquire adequate reading skills (reading beingslower or less accurate than expected for age) is one ofthe most common neurobehavioural problems affectingchildren. Although there is some debate about the precisedefinition of the term ‘dyslexia’ (Frith, 1999), abundantresearch has demonstrated that one of its primary featuresis defective development of the phonetic skills necessary toidentify and properly use the constituent sounds of writtenwords. The concept of auditory processing disorder arguesthat a sensory temporal processing deficit affects thesensory input needed for the proper phonological codingcritically required for reading (Mody, 2003). Such a deficitcould prevent the learning of precise relations between

word sounds and letter sounds, leading to difficulties in

associating the printed letter (grapheme) with the appro-

priate speech sound (phoneme). This could arise in part

from left hemisphere dysfunctions, more particularly

located in the left perisylvian region (see Demonet et al.,

2005 for a review). These deficits are aggravated in the

presence of background noise, suggesting that a noisy

listening condition, such as often prevails in the classroom,

is more particularly deleterious for such children (Bellis,

1996; Chermak and Musiek, 1997; Bradlow et al., 2003;

Ziegler et al., 2005). Electrophysiological studies confirm

such vulnerability to noise. Cunningham et al. (2001)

observed abnormal cortical but also reduced brainstem

potentials in response to speech stimuli presented in noise

in children with reading-based learning disability. King

et al. (2002) reported that the noise selectively degrades

doi:10.1093/brain/awm235 Brain (2007), 130, 2915^2928

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cortical responses in learning-impaired children whopresent abnormalities in neural brainstem synchrony, andthat training could increase neural resistance to noise forthese children with abnormal brainstem processing. Ofparticular interest is that, after an auditory trainingprogram, cortical (Hayes et al., 2003; Warrier et al., 2004)and brainstem responses (Russo et al., 2005) became moreresistant to the deleterious effect of background noise.Assuming that evoked potentials, which reflect the responsepattern of neurons responsible for encoding the acousticcomplexities of speech, express neural synchrony, and giventhat noise is known to alter the timing of morphologicalfeatures of the waveform, it can be supposed that noiseexcessively desynchronizes auditory firing in learningdisabled children.The neural mechanisms underlying speech intelligibility-

in-noise have not yet been well identified, but the medialolivocochlear (MOC) system is a possible candidate.Previous animal studies have shown that efferent bundleactivation can improve hearing-in-noise by exerting anantimasking effect (Kawase and Liberman, 1993; Kawaseet al., 1993). In humans, weak MOC functioning iscorrelated with poor tone detection in background noise(Micheyl and Collet, 1996; Micheyl et al., 1997a, b) andreduced speech intelligibility-in-noise in both adults(Giraud et al., 1997) and children (Kumar and Vanaja,2004). The MOC inhibitory fibres originate from a part ofthe superior olivary complex and project onto the outerhair cells, forming the last step of a descending auditorypathway which originates in the cortex (Huffman andHenson, 1990). In humans, there are several lines offunctional evidence for cortical influence on the cochlearmicromechanical properties reflected by evoked otoacousticemissions, which are sounds thought to be generated by theouter hair cells (Kemp, 2002). This corticofugal modulationmay be mediated by the MOC fibres. Such an effect hasbeen demonstrated in cortically resected patients (Khalfaet al., 2001) and by electrical cortical stimulation inepileptic patients (Perrot et al., 2006). Moreover, theMOC fibres which originate from the ipsilateral superiorolivary complex (uncrossed MOC system) present a patternof functional asymmetry influenced by handedness (Khalfaet al., 1998)—a pattern found to be absent in schizophrenicpatients (Veuillet et al., 2001). It could thus be argued thatabnormal cortical functioning results in impaired corticalfeedback to the brainstem and cochlea and that dysfunctionin the MOC system, which is partly under auditory cortexcontrol, thus reflects cortical alterations. Finally, the MOCsystem has been shown to function more strongly inprofessional musicians (Micheyl et al., 1997a, b; Perrotet al., 1999; Brashears et al., 2003), suggesting the possibilitythat sound conditioning could strengthen these auditorydescending pathways.We therefore wondered whether the exacerbated deficits

under background noise found in children with learningproblems might stem from impaired MOC functioning.

In a previous experiment we had observed clearly andsignificantly impaired uncrossed MOC system functionalityin learning-impaired children selected for their academicdifficulties, in a context of multiple phonemic confusionbetween voiced/voiceless French phonemes (Veuillet et al.,1999). Fine sensitivity to voicing requires optimal phonolo-gical encoding of voice onset time (VOT) duration. In aprevious study, Giraud et al. (2005) found that dyslexic adultswith auditory discrimination deficits for voiced–unvoicedcontrasts presented specific time-coding impairment of thesuccessive components of the acoustic signal. VOT is atemporal component of speech and, as with the perception ofspeech in noise, the neurophysiological processes involvestimulus-locked synchronous firing. Probably the twoprocesses share the same mechanism, as shown by Wibbleet al. (2005) who observed that children with degradedbrainstem timing presented greater degradation of corticalresponses in noise. Banai et al. (2005) suggested that thiscould be the result of abnormal cortical feedback.

Motivated by these findings, the present study sought toclarify the nature of the auditory deficit in dyslexia byinvestigating MOC functioning, coupled with a quantitativeassessment of voicing sensitivity using a categorical percep-tion test. MOC functioning was easily and non-invasivelyexplored by an objective procedure. The first experiment wasconducted to test the hypothesis of an efferent feedbackdeficit and to study a categorical perception task assessingthe/ba/-/pa/VOT contrast. Coupling these measurementsenabled links to be sought between MOC functioning andboth voicing sensitivity and reading skills. In the secondexperiment, both of these parameters were measured beforeand after an audiovisual training program focused on voicingcontrast. It was hypothesized that, compared to average-reading children, children with dyslexia would presentabnormalities in MOC functioning which could be associatedwith an altered sensitivity to voicing and that audiovisualtraining of voicing could improve voicing sensitivity andMOC functioning. The impact of such training on theperformance of children with dyslexia in a word-reading testhaving been published elsewhere (Magnan et al., 2004), thepresent study reports only the links between the impactof training-induced changes on auditory parameters andreading skills.

Experiment 1Materials and methodsParticipantsA group of 46 school-aged children served as subjects.Twenty-three were formally classified as dyslexic on neuro-psychological and speech-therapy assessment. Thesechildren with dyslexia (mean age, 10yr 11m; range, 8yr4m to 13yr 11m; 11M, 12F) had a consistent history ofpersistent specific literacy difficulties, with reading levelsat least 18 months behind chronological age, but witha performance Intelligent Quotient above 80 on the

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Wechsler Intelligence Scale for Children – Revised(3rd Edition) (WISCIII-R). None of them presented anattention-deficit hyperactivity disorder. Twenty-threeaverage-reading children (mean age, 10yr 10m; range, 8yrto 14yr; 10M, 13F), all academically average or aboveaverage, having never had to repeat a grade, and withoutany signs of learning disability, were included as controls:they had normal-for-age reading skills on the French‘L’Alouette’ reading test, which evaluates reading level interms of both word and non-word decoding and readingspeed (Lefavrais, 1965); none had previously undergonespeech therapy. For practical reasons (availability of testmaterial and time limitations) non-verbal intelligence wasassessed by the Raven’s Progressive Matrices (PM38,Edition 98) (Raven et al., 1984) and not by WISCIII-R asfor the children with dyslexia.The children were all monolingual native French speak-

ers; none suffered from neurological, psychiatric oremotional disorder or were educationally disadvantaged.All had audiometric pure-tone thresholds not exceeding20 dBHL at octave frequencies in the 250–8000Hz rangeand normal middle-ear function, and none had hadsignificant middle-ear infection during infancy. Speechintelligibility in quiet was in all cases 100% between 80and 50 dBHL for both right and left ears. Handedness wasassessed on the short 10-item version of the EdinburghHandedness Inventory (Oldfield, 1971): all scored between+0.71 and +1, indicating a right-hand manual preference;mean laterality quotient did not differ significantly betweenthe two groups. Testing involved the clinical assessmentprocedures routinely carried out on children with learningproblems consulting in our hospital department. Theaverage-reading children and their parents gave theirwritten informed consent to participate in the research.Table 1 gives descriptive data of both group and test

statistics.

Behavioural and physiological measurementsCategorical perception test. Stimuli and instrumentation. Inthis task the children were asked to label token stimulifrom a phonemic continuum based on the bilabial stopconsonant [b:] plus the vowel [a:] in which only the

VOT differed. A categorical perception task was used because itis the most basic linguistic task focusing on phonemes,which are the smallest speech units that can change themeaning of a word (Scarborough and Brady, 2002). VOT,essential to stop-consonant discrimination, refers to the timebetween onset of ‘voice’ (laryngeal vibration) and its releasefrom the mouth closure. French speakers, produce vocal cordvibration during ‘voiced’ stops, explaining why the VOT forvoiced stops (normally perceived as/b/) has a long negativevalue while for voiceless stops (normally perceived as/p/) it hasa short positive value (whereas in English, initial voiced plosivesuch an/b/are only partially voiced). Stimuli were taken froma synthetically created natural-speech voiced-voiceless con-tinuum designed to range from/ba/to/pa/by step-wise deletionof most of the initial low-frequency segment of the voicedconsonant–vowel (CV) sequence/ba/pronounced by a femalenative French speaker (see more technical details in Laguittonet al., 2000). So that the test would not be excessively long, 16VOTs (ms) were selected: �110, �96, �73, �55, �26, �20,�14,�9,�3, +3, +11, +17, +23, +29, and +35. These 16 tokenstimuli were generated via a compact disc player connected toan AC40 audiometer, and were binaurally presented at 60dBHL at random. The continuum was presented 5 timesconsecutively.

Procedure. The child was seated at a table in a quietroom, wearing a pair of Telephonics TDH39P headphones.A single-interval, 2-alternative forced-choice identificationprocedure without feedback was adopted. The two possibleresponses (letters B and P) were printed on a white sheetstuck onto the table, and the stimulus was identified bypointing and giving an oral response. The experimenterrecorded the responses manually on a data sheet. For therare cases when the two responses (pointing and oral) werediscordant, the pointing response was recorded in order tobetter target the phoneme–grapheme association and avoidfalse responses due to problems of articulation. Prior tobeginning the test, children performed a short training trialwith feedback to familiarize them with the phonemiccontrast, and then the whole continuum from the longestto the shortest VOT was administered without mixing theCVs, in order to sensitize the child to the voicing fade-out.During the test, the VOT stimuli were presented randomlyto avoid order effect.

Table 1 Characteristics of the 23 participants of both groups in Experiment 1

Average-reading children Children with dyslexia t P (df = 44)

Age in months 130� 4 (96^168) 131�4 (100^167) �0.12 0.90Performance Intelligence Quotient 105 (95^25) 101 (84^114)Age reading in months 132�4 (97^159) 94� 4 (72^140) 7.07 0.001Reading difficulties (delay in months between

reading age and chronological age)�2.26�1 (�15 to 9) 36� 4 (18^76) �10.35 0.001

Mean range� SE (range). See text for the tests used.The reading retardation corresponds to the difference between the child’s age andreading age as measured with the ‘L’Alouette’ test. Concerning the children with dyslexia: 10 present mixte dyslexia and the other (n=13)phonological dyslexia.

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Data processing. The percentages of B and P answers perVOT were calculated and identification functions plottedfor each child by graphing the percentage/BA/and/PA/responses as a function of VOT (�110 through +35ms).These identification curves were fitted with the Matlab�

software using a sigmoid function (hyperbolic tangent).Two parameters characterizing each identification functionwere extracted from this mathematical model: (1) thephoneme boundary, calculated as the 50% point of thefitted labelling curve (maximum confusion point) and(2) the identification function gradient (slope).

MOC system functioning. Stimuli. The Otodynamics�

ILO92 apparatus (software V3.94L) was used for recordingthe cochlear responses (Kemp, 2002). Following the MOCsystem exploration protocol described in detail elsewhere(Collet et al., 1992; Veuillet et al., 2001), evoked otoacousticemissions were recorded monaurally at five stimulusintensities ranging from 57 to 69 dB SPL in 3 dB steps, inrandom presentation order, with and without contralateralacoustic stimulation consisting of 30 dBSL continuousbroadband noise (speech-like noise) produced by anaudiometer.

Procedure. The test was carried out in a soundproofroom with the children sitting quietly watching silentvideo cartoons of their own choosing or playing ona Gameboy with no sound. Both ears were tested inrandom order.

Data processing. The groups did not differ significantlyin emission amplitude in either right or left ear. Theamplitude reduction with contralateral acoustic stimulationwas quantified in terms of stimulus-equivalent attenuation,defined as the mean decrease in the ipsilateral stimulus(dB) which causes the same reduction in emission ampli-tude as does a 30 dBSL contralateral broadband noise(for more details, see Veuillet et al., 1999): the more negativethe equivalent attenuation, the more functional the MOCsystem. An asymmetry index quantifying the functionallateralisation of the MOC system was calculated as thedifference between right and left ear: the more negative theindex, the more MOC system functioning predominated inthe right ear, and the more positive, the more in the left.Statistical analysis was performed with SigmaStat� soft-

ware (SPSS). All data were expressed as mean (� SE). Thedata were evaluated by parametric t-tests, or by mixed-design repeated-measures analysis of variance (ANOVA)with group effect as between-subjects factor and stimuluscondition (VOT duration, Ear) as within-subject factors.The significant ANOVAs were followed up by post hocBonferroni-adjusted t-tests. Linear regression analyses wereconducted on the relationship between MOC functioningand VOT sensitivity. Although there was no significantdifference between groups for non-verbal performance orchronological age (Table 1), partial correlations were evenco-computed to control for these factors. The significancethreshold for all tests was set at P50.05.

ResultsComparisons between average-reading childrenand children with dyslexiaCategorical perception. Averaged category labelling func-tions for the VOT series (percentage identified as/ba/or/pa/,plotted as a function of VOT) are presented for each groupin Fig. 1a. Both average-reading and dyslexic childrenidentified stimuli along the VOT acoustic–phonetic con-tinuum in a categorical-like fashion with well-establishedplateaus at the extremes and steep gradients around thephoneme boundary. Significant differences between groupswere predominantly observed for the VOT around thephoneme boundary, where the function showed a right-ward shift in the children with dyslexia as compared to theaverage-reading group. The graph in Fig. 1 shows that thefunctions differed significantly between groups with respectto phoneme boundary [F(1,44) = 12.81; P50.001] but notto gradient [F(1,44) = 1.48; P= 0.23). In average-readingchildren, phoneme perception tipped over from ‘ba’ to ‘pa’earlier than in children with dyslexia. A two-way ANOVAfor repeated measures on one factor (duration) using thepercentage of ‘ba’ categorizations for each subject wassignificant for the VOT duration effect [(F(15,660) = 478.95;P50.001], for group [F(1,660) = 13.79; P50.011)], and forthe interaction [F(15,660) = 4.29; P50.001]. Post hocpairwise multiple comparison procedures (Bonferronit-test) indicated that, whichever the group, the percentageof ‘ba’ responses obtained with the �9ms VOT stimulusdiffered significantly from that with all other stimuli,but also revealed significant differences in percentage ‘ba’responses between average-reading and dyslexic children onboth sides of the phoneme boundary [�14, �9 and �3msVOT (P50.001) and �3, +3, +11ms VOT (P50.01)] andalso for the 35ms VOT (P50.05). For all these cues,average-reading children gave less ‘ba’ responses. Thus,the fall-off in ‘ba’ responses became significant as of the�14ms VOT in this group, but did not appear before the�9ms VOT in the group of children with dyslexia.

MOC system functioning. The mean equivalent attenua-tion values for groups and ears are presented in Fig. 1b.A contralateral suppression effect was present in bothgroups for both ears. To analyse the results, a two-wayANOVA for repeated measures on one factor (Ear) revealedno significant effect of the factor Ear, a tendency fora significant effect of Group [F(1,44) = 3.10; P= 0.08],but a significant interaction between Ear and Group[F(1,44) = 27.11; P50.001]. Post hoc comparisons(Bonferroni t-test) indicated that, in average-readingchildren, the MOC system was much more functional inthe right than the left ear (P50.001), but predominated inthe left ear in children with dyslexia (P50.01). Moreover, asignificant difference was observed between the two groupsin the right ear (P50.001), suggesting a deficit of MOCfunctioning in the right but not the left ear in children withdyslexia. These differences in MOC function lateralization


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between the groups are confirmed in Fig. 1c, plotting meanand individual asymmetry index values: a t-test revealed asignificant difference between the groups (t44df = 5.21,P50.001). In addition, one sample t-test showed that themean laterality score for average-reading children (�1.4)was significantly less than 0 (P50.001), indicating rightear predominance, whereas the mean score of childrenwith dyslexia (+1.07) was significantly greater than 0(P= 0.004), indicating a left ear advantage in MOCfunctioning. Analysis of individual data showed a rightear advantage in MOC functioning for only four childrenwith dyslexia, in contrast to 21 of the 23 average-readingchildren.

Relations between MOC functioning, categoricalperception and reading ability. Linear regressions betweenMOC functioning (for equivalent attenuation in right andleft ear and asymmetry index) and phoneme boundaries

were computed for each group separately. Significantcorrelations emerged exclusively for the group of childrenwith dyslexia, and concerned the three indices of MOCfunctioning (Fig. 2): the stronger the contralateral suppres-sion effect in the right and left ear, and the more stronglypositive the asymmetry index and more strongly negativethe phoneme boundary even after controlling for non-verbal performance [respectively: r= 0.43, r= 0.48 andr=�0.44 (P50.05)] and age (respectively r= 0.42,r= 0.48; r=�0.44 (P50.05)]. After the exclusion of twooutlying children presenting the most prolonged bound-aries, less MOC functioning and also the most severereading difficulties (reading levels at 67 and 76 monthsbehind chronological age), these significant correlationspersisted and were even strengthened for equivalentattenuation in left ear (r2 = 0.21; P= 0.03) and asymmetryindex (r2 = 0.25; P= 0.02).

Fig. 1 Comparison between groups of average-reading children l and children with dyslexia for categorical perception and MOC function-ing. (a) Mean percentage stimuli identified as ‘ba’ (solid lines) or ‘pa’ (dotted lines) as a function of VOT for the control (open squares) anddyslexic (filled squares) groups. Enclosed Fig.1a: Mean� SE and individual phoneme boundary values for the dyslexic (filled squares) and thecontrol (open squares) children. (b) Comparison between right ear (RE) and left ear (LE) evoked otoacoustic emission suppression(expressed as Equivalent Attenuation) for children with dyslexia (filled symbols) and average-reading children (open symbols). (c) Means andindividual values of the interaural difference in Equivalent Attenuation (EA): Asymmetry Index: EARE-EALE) in children with dyslexia (filledsquares) and average-reading children (open squares). Bars represent the standard error of the mean. (�P_0.05; ��P_0.01, ��P_0.001).


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For the group of children with dyslexia, a singlesignificant link was found between reading difficulties andphoneme boundary (r= 0.42; P= 0.04): the more severe theretardation, and more strongly positive the phonemeboundary even after controlling for non-verbal performanceand chronological age (respectively r= 0.42 and 0.45;P50.05).

DiscussionThese results show that some children with dyslexia havealtered voicing sensitivity which is sometimes associatedwith abnormal MOC functioning with more particularlyabnormalities in MOC system lateralization. Moreover,the children with the most severe reading problems(i.e. greatest reading difficulties) were those who were themost deficient in categorical perception.Categorical perception deficits have been widely reported

in children with dyslexia, who are generally describedas being ‘less categorical’ (for more recent studies,see Adlard and Hazan, 1998; Serniclaes et al., 2001, 2004)

or ‘less accurate’ (Manis et al., 1997; de Gelder andVroomen, 1998; Joanisse et al., 2000; Breier et al., 2001;Chiappe et al., 2001) than average-reading children inphonetic contrast identification tasks. In the present study,all children presented identification functions with a clearlyregular S-shape. The mean slopes of the boundary wereboth equally steep, suggesting that no difference existed inthe consistency of phoneme categorization between the twogroups. The mean phoneme boundaries, however, differedsignificantly, average-reading children labelling VOT signalsas/pa/which were still being identified as/ba/by the childrenwith dyslexia. These children were also less accurate thanthe average-reading children in identifying clear instancesof/p/at the end of the continuum. The two groups may thushave been using different criteria for VOT identification,children with dyslexia showing abnormal sensitivity tovoicing, which they continued to perceive even when it wasso short as to be no longer perceptible for the average-reading children, as if their neural encoding of voicing wasaltered leading to erroneous VOT perception. It could bedue to deficits in inhibitory processes or excessive noisingin the auditory pathways. This altered sensitivity could alsobe related to the higher degree of allophonic perceptionfound both in dyslexic children (Serniclaes et al., 2004) andin those with gap-detection deficits (Van Ingelghem et al.,2001; Hautus et al., 2003). Electrophysiological studies alsorevealed that learning-impaired children present abnormal-ities in response to speech syllables that originate specifi-cally in the brainstem (Cunningham et al., 2001; King et al.,2002; Wibble et al., 2004) and that dyslexic children processverbal stimuli in a different manner than normal-readingchildren at the cortical level (Kraus et al., 1995; Breier et al.,2003) with a link between these brainstem and corticalresponses (Wibble et al., 2005).

Altered MOC functioning in children with dyslexia is inagreement with our previous study (Veuillet et al., 1999)and also with an experiment conducted on learning-disabled children with auditory processing disorder(Muchnik et al., 2004). Such a deficit was not found inchildren with specific language impairment (Clarke et al.,2006) but was present in children with selective mutism,where abnormal MOC functioning in the right ear was alsofound (Bar-Haim et al., 2004). Functional studies, both inanimals subjected to electrical stimulation of the inferiorcolliculus (Zhang and Dolan, 2006) and in humansundergoing cortical stimulation (Perrot et al., 2006), nowsupport the assumption that the MOC system is undercentral control. Several previous studies argue for abnormalpatterns of cerebral activation in dyslexia more particularlyat the level of the auditory cortex: for example, diminishedleft temporoparietal cortex activation (for a recent review,see Demonet et al., 2005), reduced left temporoparietalcortex activation paired with increased temporoparietalactivity specifically during reading (Simos et al., 2000a, b),and altered M100 asymmetry pattern (Edgar et al., 2006).The MOC system is driven by cortical areas and thus the

Fig. 2 Scatter-grams showing the relation between phonemeboundary and left MOC functioning (a) and Asymmetry Index(b) in children with dyslexia (filled symbols) and average-readingchildren (open symbols). The lines represent the line of bestregression fit (solid for children with dyslexia and dashed foraverage-reading children). The two circled points (outliers) werenot included in the regression. �P_0.05.


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present study provides new arguments for the notion ofabnormal cerebral lateralization in dyslexia. The robust andsignificant link observed between voicing sensitivity andleft-ear MOC advantage in the group of children withdyslexia suggests that some such children may, perhapsthrough compensatory activation, develop right-hemispheredominance for speech consonants. The question which thenarises is whether such abnormal lateralization of MOCfunctioning is linked to deficits in mechanisms which arethe cause and/or consequence of reading impairment.Longitudinal and maturational studies will be necessary toexamine this. Probably the descending system linking brainand cochlea exerts ‘top-down influences’ (Davis andJohnsrude, 2007), important for the preservation of theneural encoding of auditory information, especially whentemporal processing is required as is the case with VOTperception. It has been suggested that there may be aninteraction between ascending and descending corticofugalauditory pathways (Suga et al., 2002), and perhaps thesignificant links found in our group of children withdyslexia between the phoneme-boundary VOT value andMOC functioning may be taken as indicating a role of theauditory efferent system in inhibiting extraneous auditorycues. However, a statistical relationship between twovariables does not necessarily entail an underlying causallink between them, and one must be very cautious ininterpreting correlation data.

Experiment 2Materials and methodsParticipantsEighteen children with dyslexia participated in this study,three of whom had been included in the first Experiment.The selection criteria were the same as for previousexperiment except for the performance IntelligentQuotient, which was never under 70. The children weredivided into two groups of equal size. One group (the‘Trained group’: mean age, 10yr 6m; range, 9yr 2m to 12yr8m; 7M, 2F) completed 5 weeks’ training, with pre- andpost-training assessment. The second group (the ‘Non-Trained group’: mean age, 10yr 4m; range, 9y to 11y 10m;4M, 5F) also received two assessments with a 5-week

interval, identical to those of the trained group. These twoassessments are referred to as ‘pre-test’ and ‘re-test’,respectively. Each child and their parents were fullyinformed on all study procedures and gave their writtenconsent.

Table 2 summarizes the results on inclusion tests andstatistical tests. None of the parameters differed between thegroups.

Training procedureThe training procedure consisted of an exercise embeddedin an audiovisual computer game (Play-On) designed byDanon-Boileau and Barbier (2000), played individually byeach child of the training group 4 times a week for 5 weeks.The goal was for each child to complete 20 trainingsessions, each lasting 30min. The training did not disrupttheir regular classroom lessons, and all the children,whichever the group, continued to receive their usualspecial education and written language therapy during thestudy period. The 10-h training module was based on analternative choice with feedback, and consisted in listeningto consonant-vowel (CV) syllables and choosing which oftwo printed letters, differing only in voicing, representedthe initial consonant. This training, practiced as a game-likeexercise, focused on the voicing opposition between twoitems in six pairs of phonemes:/b/-/p/;/t/-/d/;/k/-/g/;/f/-/v/;/s/-/z/and/ch/-/j/. After auditory presentation of the syllable(for example,/ba/), a basketball fell from the top of thescreen and the child pressed one of two keys to drop theball into the basket corresponding either to ba or to pa.This audiovisual game, discriminating the phonetic featureof voicing, provided training with ortho-phonological unitsand was expected 1/to help dyslexic children to specifyphonemic representations, and 2/to improve matchingbetween visuo-orthographic pattern (letter name) andphonological unit (letter sound), so that children wouldnot confuse phonetically close phonemes, which couldfacilitate their written-word processing.

Auditory and reading assessmentsTwo forms of auditory assessment were given to thechildren: a categorical perception test and an exploration

Table 2 Characteristics of the children with dyslexia in the Experiment 2

Trained children Non-trained children t P (df=16)

Age in months 126� 5 (110^152) 124� 4 (108^142) 0.27 0.79Performance Intelligence

Quotient90 (70^120) 100 (74^113) �1.58 0.14

Age reading in months 86�2 (77^92) 85�3 (73^106) 0.36 0.72Reading difficulties (delay in

months between reading ageand chronological age)

40� 4 (19^65) 40� 5 (18^63) 0.05 0.96

(N=9 in each group). Same legend as forTable 1. Concerning the children of the trained-group: five present phonological dyslexia, threewith mixed dyslexia and one with surface dyslexia. In the non-trained group: six with mixed dyslexia and three with phonological dyslexia.


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of MOC functioning. The tests were performed as describedearlier (Experiment 1), ahead of training (pre-test) andpost-training (re-test) for the trained group, or simply aftera 5-week interval for the non-trained group (re-test), to assesstraining-related changes. To evaluate the impact of trainingon reading ability, a word recognition test (Ecalle, 2003) wasalso administered but to only seven of the nine children, twobeing absent at the time of evaluation. It consisted in findingthe target word in a list of five items consisting of theorthographically correct word (e.g. bateau, meaning ‘boat’),and four pseudowords: namely, a homophone (bato), avisually similar item (baleau), an item sharing the same initialletters (batte) and an item containing an illegal letter-sequence (btaeu). A composite score (called ‘recoding score’)of the first two responses (i.e. target word and homophone)was calculated (max.: 36).Statistical analysis was performed as in Experiment 1 to

compare MOC functioning, VOT sensitivity and readingscores between the two sessions (pre- and re-test) for eachgroup (trained and non-trained).

Results

Categorical perceptionPre- and re-test identification performance for the trained(left panel) and non-trained (right panel) groups is shown inFig. 3a. No pre- to re-test change in identification was foundfor the non-trained dyslexic group; audiovisual training, onthe other hand, resulted in a clear and substantial shift ofthe identification function, more particularly in the regionaround the phoneme boundary. Repeated measures ANOVA,comparing the pre-test performance of the two groups,with group (trained or non-trained) as between-subjectsvariable and VOT duration as within-subject variable, foundno significant group difference but a main effect of VOTduration [F(15,240) = 113.48; P50.001] with no significantinteraction between group and VOT, indicating that bothgroups divided the continuum into/ba/and/pa/categoriesin a similar manner before training. Separate two-wayrepeated measures ANOVAs were conducted for each group(trained and non-trained), with test session (pre- and re-test)

Fig. 3 Effect of training on categorical perception. (a) Mean/b/-/p/identification functions of trained (circles) and non-trained (squares)children with dyslexia. (b) Mean pre-test and re-test phoneme boundary values for trained (circles) and non-trained (squares) children withdyslexia. Comparisons between pre-test (filled symbols) and re-test (open symbols). Bars indicate standard error of the mean. �P50.05,��P50.01, ��P50.001. (c) Individual subject changes in phoneme boundary between the pre- (before) and re-test (after) sessions forthe trained (circles) and non-trained (squares) children. Post-test changes are plotted relative to normalized pre-test session values.The diagonal hatched line denotes equal performance, so that points below the lines show individual improvement between the earlierand the later test. �P50.05.


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as the independent variable. For the trained group,this analysis revealed a main effect of test session[F(1,120) = 13.22; P= 0.007], a main effect of VOT duration[F(15,120) = 144.65; P50.001], and also a significant inter-action between test session and VOT [F(15,120) = 1.98;P= 0.02]. Post hoc Bonferroni t-test revealed significantdifferences between pre- and re-test values for three VOTstimuli located within the phoneme boundary (�9, �3 and+3ms VOT) but also for one located at the extremity of thecontinuum (+35ms). There were no significant test-sessiondifferences for any of the VOTs in the non-trained group,with a main effect of VOT [F(15,120) = 80.39; P50.001]but no significant interaction between test session andVOT—indicating that, for the non-trained children, meanidentification functions showed no difference in waveformmorphology between the two test sessions over an interval of5 weeks. A repeated measures ANOVA comparing re-testVOT identification between groups showed a significantgroup difference [F(1,240) = 6.68; P= 0.020], a main effect ofVOT [F(15,240) = 132.84; P50.001] and a significantGroup�VOT interaction [F(15,240) = 1.79; P= 0.04].This training effect also impacted mean phoneme

boundaries (Fig. 3b). (It is to be noted that, for one childin the non-trained group, the phoneme boundary was notmeasurable at any moment.) A repeated measures ANOVAwith test session (pre- and re-test) as within-subject factorand Group (trained or non-trained) as between-subjectsfactor produced no main effect of Group but a significanttest session effect [F(1,15) = 11.15; P= 0.004], and asignificant interaction [F(1,15) = 7.09; P= 0.018]. Post hocBonferroni t-test revealed that the phoneme boundaries,which were comparable between groups at the pre-testsession, were significantly modified from pre- to re-testonly in the trained group (P50.001): as shown in Fig. 3c,the correlation between pre- and re-test phoneme bound-aries was significant only in the non-trained group(P50.05). Individual subject analysis found that six ofthe nine trained-group subjects exhibited a substantialdecrease in phoneme boundary (more than 5ms) comparedto only one child in the non-trained group. All the otherchildren maintained constant phoneme boundaries overtime; this included three trained children, who wouldappear to have been ‘resistant’ to training, but two of these‘resistant’ children had no impaired categorical perceptionin the first place.

MOC system functioningContralateral suppression effects were present in boththe trained and non-trained groups for both ears on bothpre- and re-tests. Two-way ANOVAs with repeatedmeasures were separately conducted on the right and leftear to separate the effects of test-session (within subject)and group (between subjects). No significant main effectsfor these factors and no significant interaction were found.To further investigate a possible lateralized training-induced

effect on MOC functioning, asymmetry indexes werecompared between groups and across test sessions(Fig. 4a). They were positive for both the trained andnon-trained group in the pre-test session but reached�0.24� 0.56 on re-test for the trained children, indicatinga change in the asymmetry of MOC functioning. A two-wayrepeated measures ANOVA on one factor of repetitionrevealed no significant effect of group, a tendency for asignificant effect of test-session [F(1,16) = 3.53; P= 0.08]and a significant interaction [F(1,16) = 5.66; P= 0.03]. Posthoc Bonferroni t-test revealed a significant decrease inasymmetry index between pre- and re-test sessions onlyin the trained group (P= 0.008). Close analysis of theindividual asymmetry index data revealed that five of thenine trained children showed a decrease in this acousticparameter after training, with a particularly great change forone of the children, whereas no change was ever observedin the non-trained subjects. The individual changes inequivalent attenuation (right and left ear) from pre- tore-test for both groups are plotted in Fig. 4b. In the rightear, they were significantly correlated between the twosessions whichever the group, whereas the left-ear correla-tion was not significant in the trained group—suggestingthat training had the effect of attenuating the suppressioneffect in this ear.

Relationships between change in MOC functioningand shift in phoneme boundaryTo discover whether these training-induced modificationsin phoneme boundary and MOC functioning were related,linear regressions were calculated between the training-induced shifts in phoneme boundary and MOC function-ing; however, none reached significance. Closer analysis ofindividual results revealed that the asymmetry indexes offive of the six trained children who presented a clear shiftin phoneme boundary towards average-reader values andwho can be qualified of ‘dyslexic responder’ shifted towardsan RE advantage for MOC functioning. This decreaseinvolved improved MOC functioning in the right ear aftertraining in three children and/or decreased MOC function-ing in the left ear in five children. Those who associatedboth profiles tended to be those showing the largest shift inphoneme boundary. For the sixth ‘responder child’, MOCfunctioning increased in both ears but most especially inthe left. After training, this child no longer differed fromthe children with dyslexia in the previous experiment,who were characterized by normal phoneme boundariesand strong MOC inhibition in the left ear. For the three‘resistant’ children, no common profile for change in MOCfunctioning emerged.

Reading skills and relationships with auditoryprocessing changesThe audiovisual training had a beneficial effect on recodingscores, which significantly increased between the pre- and


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re-test sessions (respectively, 28.57� 2.29 and 32.71� 1.29;t6dl =�2.82, P= 0.03) with improvements being evident forthe five trained children present at the reading evaluation.A significant link existed between changes in training-induced scores and in asymmetry index. The moreasymmetric the MOC system became in favour of theright ear (asymmetry index decrease), the more the word-recognition score improved (Fig. 5). There was nosignificant correlation between the training-inducedchanges in phoneme boundary and in word recognitionscore. Analysis of individual data revealed that the readingimprovement observed in five children was accompanied bya shift to the left in the phoneme boundary in only threetrained children, the other two showing no change. One ofthe two children with no improvement in word-recognitionscore showed a decrease in phoneme boundary, and theother showed no change.

DiscussionAfter training, the patterns of voicing sensitivity and MOCsystem lateralization shifted towards average-reading valuesand the improvement in reading scores was as large as thechange in MOC functioning in favour of the right ear.

In the audiovisual training experiment, the identificationcurves of the non-trained children did not vary between testsessions, indicating that neither task repetition or on-goingspeech therapy were exerting significant effects. In thetrained group, the significant shifts in identificationfunction produced new phoneme boundaries which werecloser to those found in the group of average-readingchildren as tested in the first experiment. Thus, trainingwas effective in enhancing French listeners’ ability toperceive the/b–p/contrast, in agreement with previousbehavioural (for recent studies, see Bradlow et al., 1997;Bedoin, 2003) and neurophysiological (Kraus et al., 1995;

Fig. 4 Effect of training on Equivalent Attenuation results. (a) Mean Asymmetry Index for trained (circles) and non-trained (squares)subjects during the pre- and re-test sessions. Bars indicate standard errors of the mean. (b) Individual results. Comparisons of pre-test(before) and re-test (after) values for right ear and left ear. The diagonal hatched line denotes equal values, so that points above or belowthe line show individual changes between the earlier and the later test.


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Tremblay et al., 2002) studies. This training-inducedphoneme boundary shift suggests that audiovisual trainingenables a better perceptual representation of voicing to beconstructed in the auditory pathways. However, our experi-ment also confirmed that this rehabilitation strategy basedon improving the correspondence between speech contrastsand graphemes does not prove efficacious in all children(Bishop et al., 2005; Tijms and Hoeks, 2005) and indeedsometimes has no effect (Pokorni et al., 2004); the next stepwill be to understand why. MOC functioning did not differsignificantly between sessions, attesting to the good repro-ducibility of these measures. The significant decreases inasymmetry index, which tended to be greater in the trainedgroup, suggest an effect of training on the lateralization ofMOC system functioning, which tends to become morenegative, as in the average-reading children of the firstexperiment. This MOC lateralization change was shownto be significantly correlated with improvement in readingskills. Our sample size was relatively small, but thistraining-induced change appeared in seven of the ninetrained children. Using the same remediation technique asours, Santos et al. (2007) observed a beneficial effect onpitch discrimination deficit, supported by an increase inP300 amplitude. Other studies, conducted on learning-disabled children with different types of training, havereported functional brain changes along the auditorypathways from brainstem to cortex. At sub-cortical level,training was found to improve neural synchrony (Hayeset al., 2003; Russo et al., 2005). At cortical level, the readingimprovement induced by training was associated withincreased left-hemisphere involvement, corresponding to a‘normalisation’ of underactivated left-hemisphere regions(Simos et al., 2002; Aylward et al., 2003; Shaywitz et al.,2004). But as in the present study, these changes were notsystematically observed and when observed were notalways very large. The greater left auditory cortex plasticityreported in the above training studies may be in agreement

with the lateralized training effect observed in the presentstudy, especially as voicing is known to be preferentiallyprocessed in the left hemisphere and the MOC functioningadvantage in favour of the right ear is thought to reflectthe hemispheric dominance of the left auditory cortex inlanguage processing.

General discussionFirst, this study confirms the existence of deficits inauditory processes for some children with dyslexia, showinglinks between altered voicing sensitivity and readingdifficulties. Secondly, audiovisual training was found tomodify not only VOT categorization but also MOClateralization, this effect on descending auditory pathwaysbeing correlated with the training-induced effect on read-ing. Thus, these results argue for auditory deficits indyslexia with a positive effect of training.

However, it has been commonly underlined that anauditory deficit is neither a necessary nor a sufficientcondition for disturbed reading acquisition (Bailey andSnowling, 2002). This is well confirmed by the presentresults, where a large overlap in phoneme boundaries wasobserved between groups. Our children with dyslexia allhad considerable experience of prior speech-therapy whichmay well have had some effect on their voicing categoriza-tion even if it had failed to fully remedy their dyslexia.It must also be underlined that not all children withdyslexia have a categorical perception deficit (Manis et al.,1997). Our study shows that certain ‘average-reading’children performed no better than certain dyslexics onthis task, and yet were average readers—suggesting thatother factors must be involved which are able tocompensate any such deficit in phonemic perception.However, the children with dyslexia presenting the greatestalteration in VOT sensitivity were those who presented thegreatest reading difficulties. Manis et al. (1997) observedthat the children with lower phonemic awareness hadshallower phoneme identification than children with higherphonemic awareness, and our reading-impaired childrenmay have presented this pattern. At the individual level,however, some average-reading children are comparable tochildren with dyslexia in their categorical perception, evenif dyslexics are often ‘over-trained’, which indicates thatother abilities, doubtless involved in phoneme sensitivity,come into play, confirming the multidimensional natureof reading disorders.

During the MOC exploration, a greater differentiationbetween the two groups emerged. This reinforces theimportance of the use of this test as a biological marker forabnormal lateralized central processing in children withreading acquisition deficits in a context of normal hearing.MOC system investigation could be an easy complementaryand generally objective tool to pinpoint children andmonitor the effect of training. In the present experimentthe audiovisual training focused on the improving

Fig. 5 Scatter-grams showing the relation between training-induced changes in MOC functioning (Asymmetry Index) andrecoding score. The line represents the line of best regression fit.�P_0.05.


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correspondences between speech contrast and graphemes.The significant changes observed in VOT categorization andMOC system functional lateralization argue that both therepresentation of speech sound and MOC functioning areplastic, and that these changes may reflect processes ofnormalization in the neural activity which underlies speechrepresentation. Recently, Hayes et al. (2003) reported thatafter training the cortical response became more resistant tothe deleterious effect of noise. Such improved resistance tonoise may be related to the changes in MOC functioningobserved in the present study. This rehabilitation strategy,however, did not prove efficacious in all children withdyslexia and the co-variations between the training-inducedchanges in auditory parameters and reading scores differedfrom one child to another. This heterogeneous effect oftraining is imputable to the particular profile of each childwith dyslexia before training: two of them presented nodeficit in VOT sensitivity (perhaps because over-trained),another presented a maximal recoding score beforetraining, and two children showed an MOC systemlateralized in favour of the right ear. Thus, in spite of aselection which tried to be as rigorous as possible, anunwanted heterogeneity subsisted and was increased by thediverse type of dyslexia and the diverse forms ofrehabilitation that these children were following, and alsoprobably by maturational processes (Bishop and McArthur,2005)—even if the effect of age was controlled for in thepresent study.In conclusion, our results support the notion that

children with dyslexia present different degrees of MOCfunctioning deficit, which may in some cases be associatedwith an altered perception of voicing that is proportional totheir reading acquisition difficulties. Some of these auditoryabnormalities, however, are reversible by training. MOCsystem investigation could be an easy and objective tool tocharacterise children with dyslexia and monitor the neuralchanges induced by training, but further research is neededto better understand the involvement of the corticofugalsystem in auditory perception. Lastly, because of the greatheterogeneity of the learning-impaired population, probablyonly an individual approach will enable better specificationof a given child’s disability, opening up the possibility ofmore efficient rehabilitation tailored to the precise disorder,the ultimate challenge being an improvement in literacyskills among them the reading speed and fluency. Ahead ofany attempt at therapy, the pervasiveness of these auditorydeficits will need to be determined by assessing their formand extent.

AcknowledgementsWe thank Sophie Jery and Isabelle Comte-Gervais (respec-tively speech therapist and neuropsychologist) for helpcollecting the psycho-educational data; Dr Isabelle Soares-

Boucaud (child psychiatric) for allowing us to test thechildren with dyslexia and for giving us some helpful adviceduring the setting up of the training experimentation.We are very grateful to students and more particularlyNorbert Maionchi-Pino for help collecting the experimentaldata. Lastly, this study would not have been able to bemade without the children who always showed enthusiasmand motivation and we thank them infinitely.

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