Auditory event-related potentials in poor readers

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Ž . International Journal of Psychophysiology 36 2000 11]23 Auditory event-related potentials in poor readers Jorge Bernal a, U , Thalıa Harmony a , Mario Rodrıguez a , Alfonso Reyes a , ´ ´ Guillermina Yanez a , Thalıa Fernandez a , Lıdice Galan b , Juan Silva a , ´˜ ´ ´ ´ ´ Antonio Fernandez- Bouzas a , Hector Rodrıguez a , Vicente Guerrero a , ´ ´ ´ Erszebet Marosi a ` b Centro de Neurociencias, La Habana, Cuba a Lab. de Neurometrıa, Proy. de Neurociencias, ENEP Iztacala, UNAM, Manuel Fernando Soto No. 68, Col. Constitucion de ´ ´ la Republica, 07469 Mexico, Mexico ´ Received 19 December 1996; received in revised form 28 September 1999; accepted 28 September 1999 Abstract Ž . Although poor readers PR are considered the major group among reading-disabled children, there are not Ž . event-related potentials ERP studies reported of PR on the subject. In this study, attentional and memory processes were studied in an auditory oddball task in PR and normal controls. ERP to auditory stimuli were recorded Ž . Ž in 19 leads of the 10r20 system, using linked earlobes as references, in 20 normal children 10 female and 20 PR 10 . Ž . Ž . female of the same age 10 ] 12 years old . Two pure tones 1000 and 3000 Hz were used in an oddball paradigm. No significant differences were observed in the amplitudes and latencies of N100 between the groups. However, N200 to frequent stimuli and P200 to both frequent and infrequent stimuli were of higher amplitude in poor readers than in normal children. There were no differences between groups in the latency and amplitude of P300. The results suggest that PR use more attentional resources in the components occurring before P300 to both frequent and infrequent stimuli than the normal children, and this finding is particularly marked for PR girls. Q 2000 Elsevier Science B.V. All rights reserved. Keywords: P300; Auditory event-related potentials; Poor readers; Reading disabilities; Sex differences U Corresponding author. Ž . E-mail address: [email protected] J. Bernal 0167-8760r00r$ - see front matter Q 2000 Elsevier Science B.V. All rights reserved. Ž . PII: S 0 1 6 7 - 8 7 6 0 99 00092-6

Transcript of Auditory event-related potentials in poor readers

Ž .International Journal of Psychophysiology 36 2000 11]23

Auditory event-related potentials in poor readers

Jorge Bernala,U, Thalıa Harmony a, Mario Rodrıgueza, Alfonso Reyesa,´ ´Guillermina Yaneza, Thalıa Fernandeza, Lıdice Galanb, Juan Silvaa,´˜ ´ ´ ´ ´

Antonio Fernandez- Bouzasa, Hector Rodrıgueza, Vicente Guerreroa,´ ´ ´Erszebet Marosia`

bCentro de Neurociencias, La Habana, CubaaLab. de Neurometrıa, Proy. de Neurociencias, ENEP Iztacala, UNAM, Manuel Fernando Soto No. 68, Col. Constitucion de´ ´

la Republica, 07469 Mexico, Mexico´

Received 19 December 1996; received in revised form 28 September 1999; accepted 28 September 1999

Abstract

Ž .Although poor readers PR are considered the major group among reading-disabled children, there are notŽ .event-related potentials ERP studies reported of PR on the subject. In this study, attentional and memory

processes were studied in an auditory oddball task in PR and normal controls. ERP to auditory stimuli were recordedŽ . Žin 19 leads of the 10r20 system, using linked earlobes as references, in 20 normal children 10 female and 20 PR 10

. Ž . Ž .female of the same age 10]12 years old . Two pure tones 1000 and 3000 Hz were used in an oddball paradigm. Nosignificant differences were observed in the amplitudes and latencies of N100 between the groups. However, N200 tofrequent stimuli and P200 to both frequent and infrequent stimuli were of higher amplitude in poor readers than innormal children. There were no differences between groups in the latency and amplitude of P300. The results suggestthat PR use more attentional resources in the components occurring before P300 to both frequent and infrequentstimuli than the normal children, and this finding is particularly marked for PR girls. Q 2000 Elsevier Science B.V.All rights reserved.

Keywords: P300; Auditory event-related potentials; Poor readers; Reading disabilities; Sex differences

U Corresponding author.Ž .E-mail address: [email protected] J. Bernal

0167-8760r00r$ - see front matter Q 2000 Elsevier Science B.V. All rights reserved.Ž .PII: S 0 1 6 7 - 8 7 6 0 9 9 0 0 0 9 2 - 6

( )J. Bernal et al. r International Journal of Psychophysiology 36 2000 11]2312

1. Introduction

Ž .According to Rayner and Pollatsek 1989 , chil-dren with reading difficulties may be classified in

Ž . Ž .three groups: 1 ‘poor readers’ PR are thosewho score between 1 and 2 years below their

Ž .expected reading level and have normal IQ; 2‘dyslexic readers’ are those who score 2 or moreyears below their expected reading level, with

Ž .normal IQ, and 3 ‘backward readers’ are thosewho score below their expected reading level andhave IQ scores equal to 80 or less. PR maycorrespond with the ‘garden-variety poor readers’

Ž .as Gough and Tunmer 1986 have called them,and constitute 13% of school age children, whiledyslexic children constitute only a small part of

Ž . Žthe total school age subjects 2% Rayner and.Pollatsek, 1989 .

Neuropsychological studies on dyslexics, haddescribed deficits in auditory and visual process-

Ž .ing Boder, 1973; Tallal et al. 1993 , in phonologi-Ž .cal processing Torgesen, 1988 , in short-term me-

Ž .mory Mattis et al., 1975; Lyon, 1982 and inŽ .working memory Swanson, 1993 . Moreover,

Ž .Stanovich 1988 has proposed that in dyslexicsthe core of the reading difficulties is a deficit inphonological processing and that although gar-den-variety poor readers share the phonologicalproblems of dyslexics } perhaps in less severeform } they have also a wide variety of cognitivedeficits.

Reading difficulties of any type in children maybe related to working memory capacity. Just and

Ž .Carpenter 1992 have proposed that working me-mory plays a central role in language comprehen-sion, storing the intermediate, and final productsof a reader’s or listener’s computations, as she orhe constructs and integrates ideas from the streamof successive words in a text or spoken discourse.These authors have demonstrated that individualdifferences in working memory capacity for lan-guage can account for qualitative and quantitativedifferences among adults in several aspects oflanguage comprehension. Moreover, SwansonŽ .1994 studied the performance in several tasks ofshort-term and working memory in a group withlearning disabilities. These subjects were selectedbecause of primary problems in reading, but also

had low scores in mathematics. Lower scores forverbal working memory tasks, but not forvisual]spatial working memory tasks, and for averbal and a visual]spatial short-term memorytask were observed in these subjects when com-

Ž .pared to normal subjects. Swanson 1994 con-cluded that short-term and working memory doreflect different processes and both are importantin reading comprehension and mathematics.

Although the causes of dyslexia are not well-known, there are studies showing that this abnor-mality has neurobiological basis. Thus, it has beenproposed that dyslexic subjects have deficiencieswith temporal sequence processing probably dueto an anatomical disorganization of some cerebral

Žstructures Tallal et al., 1993; Galaburda and Liv-.ingstone, 1993 and several electrophysiological

alterations when compared with normal subjectsŽAhn et al., 1980; John et al., 1983; Taylor and

. ŽKeenan, 1990 . However, in PR as defined by.Rayner and Pollatsek, 1989 there are not explicit

hypothesis about biological causes of deficienciesin reading.

Actually, there is no accord if PR and dyslexicsare qualitatively different groups or if they sufferfrom the same deficiency but at different degrees.However, it is clear that in both groups thereexist deficiencies in the processing of some aspectrelated to reading.

( )2. Event-related potentials ERP in children

ERP is a non-invasive technique that can pro-vide data about the neural activity related tocognitive information processing.

Recent studies have used these potentials as amethod for assessing cognitive differences in chil-dren due to ERP provide unique insights into thenature of the reading disorders by highlightingquantitative andror qualitative differences in in-formation processing between normal and read-ing disabled children. Among the auditory ERPcomponents that have been studied we can find:N100, P200, N200 and P300; these componentshave been related to different phases of informa-tion processing.

N100 has a fronto-central topographic distribu-

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Ž .tion Iragui et al., 1993 . It is related to selectiveŽattention Loveless, 1983; Naatanen and Picton,¨¨ ¨

.1987; Elbert, 1992 , may be reflecting an earlyselective process: the comparison of the attendedstimulus with the model stored in memory, or }on the other hand } some active supervisingprocess, that evaluates the arriving information or

Žthe access to memory Loveless, 1983; Picton,.1988 . Longer latencies and reduced amplitudes

of N100 have been reported in children withŽ .reading difficulties Pinkerton et al., 1989 and

Žalso in children with attentional deficits Satter-.field and Bradley, 1977; Loiselle et al., 1980 .

P200 shows a topographic distribution with itsŽhighest peak at the central region Iragui et al.,

.1993 . Controversy exists about if P200 is anŽexogenous or endogenous component Shibasaki

. Ž .and Miyazaki, 1992 . Polich et al. 1990 inter-preted developmental changes in P200 as a re-flection of the maturation of the sensory functionrather than that of cognitive function. Also, Hill-

Ž .yard and Picton 1987 had proposed that P200 issensitive to the physical attributes of the stimulus.

Ž .However, Oken 1990 described it as en-Ž .dogenous. Johnson 1989 found that P200 is

modified by the attentional demands of the tasksŽ .performed and Holcomb et al. 1986 , reported

higher P200 amplitude at Cz to unexpected sti-muli, in reading disabled and in children sufferingattentional deficit with hyperactivity as comparedto controls and children with attentional deficitwithout hyperactivity.

N200 is an endogenous component whose topo-graphic distribution depends on the sensory

Ž .modality of the stimulus Donchin et al., 1978 ; incase of auditory stimulation, the highest ampli-tude is observed at vertex and in case of visual

Žstimulus, at the preoccipital region Simson et al.,.1977 . This component reflects a discriminative

process that responds to environmental changesin an automatic way and might participate in the

Žorientating response Naatanen and Michie, 1979¨¨ ¨.in Loveless, 1983 . N200 can also reflect the psy-

chological processes associated to target selectionŽ .Donchin et al., 1978 or stimulus discriminationŽ .Satterfield et al., 1990 . Strong relationships havebeen reported between N200 and task demandsŽ .Johnson, 1989; Duncan et al., 1994 and selective

Ž .attention Satterfield et al., 1990 . Iragui et al.Ž .1993 have proposed another hypothesis, suggest-ing that N200 reflects a categorization processwhen decisions are taken.

The psychological processes underlying P300have been widely studied. There is evidence sug-gesting that P300 reflects information processing

Ž . Ževents associated with: a attention Holcomb et. Ž . Žal., 1985 ; b memory operations McIsaac and

. Ž .Polich, 1992 ; and c developmental changes inŽthe memory capacity of children Polich et al.,

.1990 . At the moment, the most accepted theoret-ical interpretation of P300 is that it indexes activi-ties required in the maintenance of working me-mory, reflecting processes which are engaged

Ž .when the mental model or schema of the envi-Žronment is refreshed and updated Donchin et

.al., 1986 .ERP technique has been useful in investigating

the neurophysiological deficits of dyslexics. Firststudies frequently reported smaller amplitudeandror later latencies of N100, P200 and N200

Žcomponents Conners, 1971; Shields, 1973; Weberand Ommen, 1977; Preston et al., 1977; Brying

.and Jarvilehto, 1985; Pinkerton et al., 1989 .¨However, most recent studies reported resultswith endogenous components such as P300 andwith components that occur before 300 ms. Ingeneral, these studies have shown lower ampli-tudes andror larger latency of P300 component.

Ž .Thus, Taylor and Keenan 1990 reported smallerP300s and N200 with minor latency for languagestimuli in dyslexic children as compared to con-

Ž .trols. Holcomb et al. 1986 have found decreasedamplitude of auditory P300 but no significantdifferences in N100 and N200 between dyslexicand normal children; however, dyslexics showedgreater P200 to unexpected stimuli. In addition,

Ž .Erez and Pratt 1992 using pure tones and twononsense monosyllables, have reported decreasedamplitudes of P300 at midline leads in dyslexicsubjects compared to normal ones.

These results had been interpreted as reflectingeither decreased availability of attentional re-sources or the inability to allocate them appropri-

Ž .ately. Furthermore, Duncan et al. 1994 pro-posed that altered P300 is a reflection of theimmaturity of the brain that impairs those cogni-

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tive operations necessary for successful readingtake place.

Thus, it is clear that ERP provide very impor-tant information related to sensory and cognitiveprocessing in children. However, to our know-

Žledge, cognitive processing of poor readers as.defined above have not been studied with this

technique. For this reason, the aim of this workwas to study ERP characteristics of poor readersto explore electrophysiological signs that canguide to the biological basis of this disorder. Inthis study amplitudes and latencies of N100, P200,N200 and P300 components were evaluated.

The results will be discussed in terms of thefindings reported for dyslexics, in order to con-tribute to clarify the controversy about cognitivedifferences between dyslexics and poor readers.

3. Material and methods

3.1. Subjects

Forty right-handed children between 10 and 12Ž .years of age 20 male and 20 female were stud-

ied. All subjects were of middle socioeconomicclass with normal paediatric and neurological ex-amination. No subject was under medication atthe time of the study. They all came from a public

Ž .school. The average IQ was 120.3 S.D.s8.9 forŽ .the control group and 102.1 S.D.s10.5 for the

PR group, as assessed by the Weschler Intelli-Ž .gence Scale for Children Mexican Revision

Ž .WISC-RM . Although both groups had normalIQ values, ANOVA showed significant differ-

Ž .ences between them F s24.02, P-0.0001 .1,30ŽThe control group consisted of 20 children 10

.girls and 10 boys with good academic achieve-Žment. The PR group consisted of 20 subjects 10

.girls and 10 boys with low achievement in allacademical subjects; 70% of them had repeatedat least one grade and attended special psy-chopedagogical courses, in order to cope success-fully with normal educational requirements. How-ever, some subjects had not clear ERP compo-nents, so, the definitive number of the subjects inthe sample diminished to 17 children in the con-

Ž .trol group 10 boys and 7 girls and 15 childrenŽ .for the PR group 8 boys and 7 girls .

The division of the children in the control andPR groups was based upon performance in twobatteries for the assessment of reading: The Psy-

Ž .choeducative Battery Ostrosky et al., 1984 andŽthe Reading Disabilities Battery Regiosa et al.,

.1994 .The Psychoeducative Battery is a standardized

reading test for Mexican children, which includesspeed of reading and reading comprehension testsin both silent and out-loud reading.

The Reading Disabilities Battery was designedfor the computerized analysis of reading. This testis called ‘Baterıa para los Trastornos de Lectura´Ž .BTL ’ in Spanish and it includes eight differentsubtests: word reading, reading comprehension,ordering of words into syntactically correctphrases, completion of phrases, naming, phono-logical categorization of pictures and words andperception of visual features.

PR scored between one and two standard devi-ations below the scores of the normal readers inboth batteries. Table 1 shows the subtests of theBTL with significant differences between the twogroups. The performance of PR was significantlylower than the performance of controls in each

Ž .subtest Silva et al., 1995 .

3.2. Stimuli

Auditory stimuli were tones of 1000 and 3000ŽHz, presented at 70 dB SPL 10 ms riserfall and

Table 1Reading Disabilities Battery differences between groups

aŽ .MANOVA

Task P- Differences

Reading of words 0.0001 NR)PRComprehension of a text 0.0001 NR)PRNaming of pictures 0.0006 NR)PROrdering of sentences 0.0001 NR)PRCompletion of sentences 0.0001 NR)PRPhonological categorization of pictures 0.0001 NR)PRPhonological categorization of words 0.0001 NR)PRVisual perception 0.0038 NR)PR

a Ž .) means better performances less errors and faster RT ;Ž .NR, normal readers controls ; PR, poor readers.

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.50 ms plateau and an interstimulus interval of2]2.5 s. Stimuli were presented in three seriesthat consisted of 70, 80 and 110 tones each one.In each series, the probability of presentation was

Ž .of 80% for the frequent tone standard stimulusŽ .and 20% for the infrequent tone target stimulus .

Stimuli were presented randomly in a contra-Žbalanced way half of the experimental subjects of

both groups had the 1000-Hz tones as infrequentstimulus and the other half, the tones of 3000

.Hz .

3.3. Procedure

Subjects were familiarized with the laboratory,and then seated in a comfortable chair in anilluminated room. They were asked to count thetarget stimuli and, after each series, the childrenhad to say the number of target stimuli counted.

At the beginning of each session, the childrenwere taught to identify the target stimulus andrehearsed until they were able to execute thediscrimination task without errors.

3.4. Recording

The stimuli were presented binaurally throughearphones. Nineteen AgrAgCl electrodes wereplaced at FP1, FP2, F3, F4, C3, C4, P3, P4, O1,O2, F7, F8, T3, T4, T5, T6, Fz, Cz and Pz sites ofthe 10]20 International System, using linked ear-lobes as references. Recording and stimulationwere made using a Medicid-3M computer systemwith amplifiers of 0.5]30 Hz of band range. Eyemovements were monitored by bipolar electrodesattached to the right supraorbital region and outercantus. The electrode impedance was alwaysbelow 10 kV. The sampling period was of 4 msover a time epoch of 1024 ms with a 100-msprestimulus baseline. EEG segments were se-lected visually, off-line, eliminating segments withartifacts and with EEG activity higher than 40 mVat any channel. Averaging was done separatelyfor frequent and infrequent stimuli, adding thestimuli of the three series. A minimal of 15]20clean segments were used since Taylor and

Ž .Keenan 1990 have reported that 10]15 seg-ments are enough to obtain a reliable ERP inchildren.

4. Data analysis

4.1. Latency

The largest positive-going peak occurring afterthe N100]P200]N200 complex within a latency

Žwindow of 280]700 ms determined by examining.grand mean ERP at Pz was designated as P300

and its latency was measured at all derivations,for both standard and target stimuli. Latencies of

ŽN100, P200 and N200 components determined by.examining grand mean ERP at Cz were mea-

Žsured in all derivations at the largest peak also.for both types of stimuli within latency windows

of 60]150, 120]220, and 180]280 ms, respec-tively.

4.2. Amplitude

Mean amplitudes of N100, P200, and N200components relative to pre-stimulus baseline, forfrequent and infrequent stimuli, were calculatedat all leads within a latency window determinedby the peak latency of each component in the

Žgrand mean ERP at Cz as follows: N100 92]108. Ž . Ž .ms ; P200 152]184 ms and N200 224]256 ms. .

For P300, this measure was done within an inter-val of 266]366 ms also for all leads, consideringP300 peak latency at Pz.

4.3. Topography

Scalp topography analysis of the scaled baselineŽ .to peak amplitudes McCarthy and Wood, 1985

of each component in frequent and infrequentconditions were done when these componentsand conditions were statistically different betweengroups. Two types of analysis were done: thetopographic profile comparisons using only Fz, Czand Pz leads and hemispheric comparisons with-out considering these three electrodes.

( )J. Bernal et al. r International Journal of Psychophysiology 36 2000 11]2316

4.4. Statistical analysis

A four-factor ANCOVA was applied to ampli-tude measures of each component, for both sti-

Ž .mulus conditions target and standard separatelyŽin the following way: Group controls vs. poor

.readers = Sex = Anterior-to-posterior electrodeŽ .placements: frontal F7, F3, Fz, F4 and F8 leads ,

Ž .central T3, C3, Cz, C4 and T4 leads and parietalŽ .T5, P3, Pz, P4, and T6 leads =coronal electrode

Ž .placements: left lateral F7, T3, and T5 leads ,Ž . Žleft medial F3, C3 and P3 leads , medial Fz, Cz. Ž .and Pz leads , right medial F4, C4 and T4 leads

Ž .and right lateral F8, T4 and T6 leads . In thesecomparisons, repeated-measures ANOVAŽ .STATISTICA , with Greenhouse]Geiser epsiloncorrections were made and adjusted degrees offreedom were calculated and rounded down tothe nearest whole number. If the Group maineffect was significant, the remaining four elec-

Ž .trodes Fp1, Fp2, O1 and O2 were analysed. Forlatency measures, comparisons between groupswere done first at Cz for N100, P200 and N200and at Pz for P300 with two-factor ANCOVAŽ .Group=Sex . If significance between groups orGroup=Sex differences were found, then four-factor ANCOVA was carried out. In any othercase the analysis was finished. In all between-

Ž .group comparisons ANCOVA IQ was employedas covariable.

Behavioral tests: The responses for the Psy-choeducative Battery were analysed by Student’st-test, and those of the Reading Disabilities Bat-tery were analysed by means of MANOVA.

5. Results

5.1. Beha¨ioral results

The Psychoeducative Battery showed poorerperformances by the PR group considering both

Ž .reading speed ts2.25 P-0.05 and readingŽ .comprehension ts2.12 P-0.05 tests as com-

pared to the control group. The z-transformationof scores of the PR group showed that the meanscore of their reading speed was y1.7 S.D. valuesbelow that of the control group and their reading

comprehension score was y0.85 S.D. values belowthe control group’s mean score. These results arein accordance with Rayner and Pollatsek’s opera-tional definition of poor readers.

The Reading Disabilities Battery showed cleardifferences between groups. Table 1 illustratesthe MANOVA for the items of each task withtheir significance level. All tasks gave significantdifferences between groups; although another

Ž 2statistical analysis maximisation of R , correla-.tion matrix clearly showed that syntactic tasks

Že.g. ordering of words into syntactically correct.sentences and reading comprehension tasks dif-

ferentiated groups better than the other ones.Discriminant analysis with replication showed100% of hits in the classification of groups andthe discriminant function was composed of vari-ables of the syntactic and comprehension taskŽ .Silva et al., 1995 .

5.2. ERP results

For the odd ball paradigm, none of the groupshad errors in the task of counting infrequentstimuli.

5.3. Latency

Grand average waveforms elicited by infre-quent and frequent stimuli were morphologically

Žquite similar between control and PR groups Figs..1 and 2 . It can be observed that early compo-

nents N100, P200, N200 and late P300 had ap-proximately the same latency for both groupsconsidering the waveforms elicited by both typesof stimuli. The between-groups differences mea-sured at Cz were not significant: N100 occurred at103 ms in the control group and 101 ms in the PRgroup, this component was also observed at frontalŽ .except F7 and F8 , central, and parietal deriva-tions. P200 appeared at 170 and 174 ms for thecontrol and PR groups, respectively, and it was

Ž .observed at frontal except F7 and F8 , central,parietal and occipital regions. N200 was detectedat the same regions as P200 as well as at postero-temporal leads; although some between-groupdifferences were observed in N200 latency, they

Žwere not significant latency for controls was 244

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Fig. 1. ERPs to infrequent stimuli in both groups at 19 electrode locations. Cursors show stimulus onset and the arrow at Cz showsP200, with maximal amplitude at frontal, central, parietal and occipital regions. Asterisk marks P300.

.ms and 271 ms for PR . Finally, we can observe aP300 wave with maximal amplitude at Pz, thoughit was clearly distinguishable at central, parietal,temporal and occipital areas. Latencies at Pz were,for the control group 388 ms and for the PRgroup 360 ms. Again, this difference was notsignificant.

5.4. Amplitude

For N100 and P300 amplitudes, no between-group differences were found either to infrequentor frequent stimuli. However, amplitude differ-ences were observed in P200 and N200 compo-nents to infrequent and frequent stimuli respon-ses, but these differences were more important tothe infrequent ones.

5.4.1. P200The significant group effect showed greater

P200 amplitude for PR than the control group to

Ž .infrequent stimuli F s7.3, P-0.01 . Group1,27Ž=Sex interaction was also significant F s15,1,27

.P-0.0006 where PR girls had greater ampli-tudes that either boys or girls of the control groupŽP-0.04 and P-0.0007, respectively in post hoc

.analysis . Group = Antero-posterior electrodeŽsites interaction was also significant F s3.28,1,44

.P-0.05 . Post hoc analysis showed that P200amplitude at central and posterior sites were sig-

Žnificantly greater in PR than controls P-0.0001. Ž .and P-0.0004, respectively see Fig. 3 . Like-

wise, the next interactions were significant: GroupŽ .=Coronal sites F s3.9, P-0.03 , and Group1,42

Ž .=Sex=Coronal sites F s3.7, P-0.03 . In1,42the last interaction, post hoc analysis showed thatPR girls had greater P200 amplitudes than thePR boys at left medial, medial and right lateral

Želectrode sites P-0.003, 0.0002 and 0.03, re-.spectively , while in the control group there were

no significant sex differences. In addition, PRgirls showed greater P200 amplitudes than con-

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Ž .Fig. 2. ERPs to frequent stimuli in both groups control and poor readers at the 19 electrode locations. Cursors show stimulusonset and the arrow at Cz shows P200, with maximal amplitude at frontal, central, parietal and occipital regions.

trol girls at left medial, medial and right lateralŽelectrode sites significant level: P - 0.0007,

.0.0002 and 0.0002, respectively and than controlŽ .boys at medial electrodes P-0.0007 . The same

tendency was observed for FP1, FP2, O1 and O2,Žwhich showed a significant effect of Group F1,27

.s9.13, P-0.005 and Group=Sex interactionŽ .F s6.8, P-0.02 . In this manner, the PR1,27group had greater P200 amplitude than the con-

Ž .trol group means3.04 mV vs. y0.78 mV ; PRgirls had significant greater P200 amplitudes than

Žboys or girls of the control group means5.8 mVvs. 0.08 mV, P-0.03 and y1.06 mV P-0.004,

.respectively .Thus, it was obvious that differences between

groups were due to greater P200 amplitudes ofPR girls in almost all of the derivations.

Also between group differences were found inthe hemispheric asymmetry analysis. Group=Hemisphere effect was significant in the overall

Ž .ANOVA F s 6.1, P - 0.02 due to PR’s1,27greater P200 amplitudes over right hemisphere

Ž .respect to controls P-0.0002 . This last resultwas not observed when amplitude data were scaled

Ž .according to the McCarthy and Wood 1985transformation. No between group differenceswere observed in topographic profile analysis.

For frequent stimuli, the principal effect of thegroup was not significant, but Group=Sex inter-

Žaction was highly significant F s16.7, P-1,27.0.0004 . Post hoc analysis showed that PR girls

Žhad greater amplitude than PR boys means6.mV vs. y2 mV, P-0.002 , while in the control

group no significant sex difference could beobserved. In addition, PR girls showed greater

ŽP200 amplitude either than control girls means.5.8 mV vs. y2 mV, P-0.001 or control boys

Ž .means5.8 mV vs. 0.4 mV, P-0.04 . Group=Sex=Coronal sites interaction was also signifi-

Ž .cant F s4, P-0.02 . This result showed that2,67

( )J. Bernal et al. r International Journal of Psychophysiology 36 2000 11]23 19

Ž . Ž . Ž .Fig. 3. Topographic distribution of mean amplitude of P200 to infrequent stimuli, at left lateral LL , left medial LM , medial M ,Ž . Ž .right medial RM and right lateral RL electrodes at frontal central and parietal regions, for boys and girls from control and PR

groups. It can be observed that PR girls show higher P200 amplitude at most electrodes of frontal, central and parietal regions thanP200 of either control boys or girls, or PR boys.

PR girls had greater P200 amplitudes than PRboys at left medial, medial and right lateral sites

Ž .P-0.0002 , while in the control group no sig-nificant sex differences were found. Also, PR girls

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Ž .Fig. 4. Topographic distribution of mean amplitude of P200 to frequent stimuli at coronal regions: left lateral LL , left medialŽ . Ž . Ž . Ž .LM , medial M , right medial RM , and right lateral RL , for control and PR boys and girls. It can be observed that PR girlsshow higher P200 amplitude than control boys or girls or PR boys at LM, M and RM regions.

showed greater P200 amplitudes than girls orboys of the control group in the same regionsŽ . Ž .P-0.004 see Fig. 4 .

5.4.2. N200In case of N200 component the differences in

responses elicited by the infrequent stimuli, were

ŽFig. 5. Topographic distribution of N200 mean amplitude to infrequent stimuli at Anterior]posterior frontal, central and. Ž . Ž . Ž . Ž . Ž .parietal =Coronal interaction: left lateral LL , left medial LM , medial M , right medial RM , and right lateral RL , for control

and PR groups. It can be observed that the PR group shows higher amplitude than the control group mainly at right medialelectrodes at frontal, central and parietal regions.

( )J. Bernal et al. r International Journal of Psychophysiology 36 2000 11]23 21

significant only in Group=Antero-posterior=ŽCoronal interaction factors F s3.85, P-8,13

.0.015 . According to the post hoc test, this effectwas due to largest amplitudes in the control group

Žat frontal region: F3, F4, and F8 P-0.000025,.0.000025 and 0.05, respectively , at the central

Žregion: C4 and T4 P-0.000025 and 0.012, re-. Ž .spectively and at parietal sites: P4 P-0.00003

Ž .Fig. 5 . Moreover, the N200 component elicitedby the frequent stimuli showed a significant effectin the Group=Sex=Antero-posterior factor in-

Ž .teraction F s7.21, P-0.01 . This effect was1,36due to a greater amplitude in PR girls than PR

Ž .boys at central y5.34 mV vs. y1.01 mV andŽ .parietal y3.4 mV vs. 4.19 mV regions, while in

the control group there were no significant sexdifferences. In this component there were nodifferences in hemisphere or topographic profileanalysis in any frequent or infrequent responses.

6. Discussion

The objective of the current study was to anal-yse ERP characteristics of PR. The results showedthat the only differences between controls andPR were found in P200 and N200 components:PR had higher P200 amplitudes to both frequentand infrequent stimuli, higher N200 to frequentstimuli and lower N200 to infrequent stimuli ascompared to controls.

Though there are no clear conclusions aboutthe psychological processes that might be relatedto P200, some studies provide evidence that P200

Ž .is related to attention. Johnson 1989 hasobserved higher amplitude of auditory N100 andvisual P200 in a reaction time task compared tosimple counting task, suggesting that auditoryN100 and visual P200 are sensitive to tasks that,according to the difficulty level, require more

Ž .attention see also Stelmack et al., 1988 . More-over, higher P200 amplitudes have been associ-ated to phasic changes in attention. In the study

Ž .of Holcomb et al. 1986 , P200 amplitude at Czwas larger to a surprising sound in reading dis-abled and attentional-deficit with hyperactivitychildren compared to either controls or attentio-nal-deficit without hyperactivity children; that is,

P200 was larger to the stimuli that capture moreattention.

Therefore, PR’s higher P200 amplitude mayreflect that these children paid more attention toboth kinds of stimuli than normal group. Thisfact, together with normal P300 amplitude toboth frequent and infrequent stimuli in the PRgroup may indicate that these children displayedmore attentional effort than normals in compo-nents occurring before P300. Probably, the abovedescribed characteristics of PR are the psy-chophysiological expression of their deficienciesduring the attentional process. It suggests thatattentional resources were allocated in earlierstages of information processing, in contrast withnormal subjects who displayed properly more at-tentional resources in those stages that corre-

Ž .spond to evaluation of stimuli i.e. P300 .Although PR showed deficiencies in early stages

of information processing, they showed the sameor similar P300 as controls. It could be supposed

Žthat when PR accomplishes an easy task as in.the current study their deficiencies do not affect

information processing in later stages, but if thetask was more difficult then alterations in laterstages would be evident too.

This statement was particularly true in the caseof PR girls who showed differences with bothboys or girls of the control group. It is verydifficult to find a clear explanation for this find-ing, since no sexual differences were observed forIQ, or scores of the Reading Disabilities Battery.However, the results seem to support the hy-pothesis about that, although in the developmen-tal disorders of childhood, the boys are morefrequently affected, when these disorders affect

Žgirls, they are more afflicted than boys Eme.Robert, 1992 . It is necessary to carry out other

studies in order to analyse this point.Analysis of the N200 component showed that

N200 to infrequent stimuli obtained from thecontrol group was greater than that obtained fromthe PR group. Maybe, this result reflected con-trols’ more efficient effort to discriminate infre-quent stimuli, compared to PR. Probably, PRdisplayed smaller N200 amplitude than controlsbecause they allocate resources in stages before

Ž .N200 i.e. P200 .

( )J. Bernal et al. r International Journal of Psychophysiology 36 2000 11]2322

In relation to results with auditory stimuli fordyslexics, two studies have reported a smallerauditory P300 in dyslexics related to normal chil-

Ž .dren Holcomb et al., 1986; Erez and Pratt 1992 .In the first paper, other components were alsostudied but neither N200 nor N100 discriminated

Žbetween groups. In the current work that used a.similar paradigm to Holcomb’s differences in

P200 and N200 amplitude discriminated betweenPR and normal readers. Therefore, it can beconcluded that whereas dyslexics show alterationsin stages related to stimuli evaluation and me-

Ž .mory processing i.e. smaller P300 than controlsŽ .such as Taylor and Keenan 1990 had shown,

PR’s alterations occur in stages before P300 ap-pearance. For dyslexics, deficiencies on stimuli

Žprocessing in working memory manifested by al-.terations in P300 amplitude and latency could

explain their reading alterations since workingmemory plays a key role in several processesnecessary in reading. In contrast, the readingproblems of PR could be explained by their defi-ciencies in earlier stages of the information pro-cessing.

Acknowledgements

This work was supported by National CouncilŽ .of Science and Technology CONACYT of

Mexico. Grant No.27235-N.´

References

Ahn, H., Prichep, L., John, E.R., Baird, H., Trepetin, M.,Kaye, H., 1980. Developmental equations reflect brain dys-function. Science 210, 1259]1262.

Boder, E., 1973. Developmental dyslexia: A diagnostic ap-proach based on three atypical reading]spelling patterns.Dev. Med. Child Neurol. 15, 663]687.

Brying, R., Jarvilehto, T., 1985. Auditory and visual evoked¨potentials of schoolboys with spelling disabilities. Dev. Med.Child Neurol. 27, 141]148.

Conners, C.K., 1971. Cortical visual evoked response in chil-dren with learning disorders. Psychophysiology 7, 418]428.

Donchin, E., Ritter, W., McCallum, W.C., 1978. Cognitivepsychophysiology: The endogenous components of the ERP.

Ž .In: Calaway, E., Tueting, P., Koslow, S.H. Eds. , Event-related Brain Potentials in Man. Academic Press, NewYork, pp. 349]441.

Donchin, E., Karis, D., Bashore, T., Coles, M.G.H., 1986.Cognitive psychophysiology and human information pro-

Ž .cessing. In: Coles, M.G.H., Donchin, E., Porges, S.W. Eds. ,Psychophysiology: Systems, Processes and Applications.Guilford, New York, pp. 244]267.

Duncan, C., Rumsey, J., Wilkniss, S., Denckla, M., Ham-burger, S., Odou-Potkin, M., 1994. Developmental dyslexiaand attention dysfunction in adults: Brain potentials in-dices of information processing. Psychophysiology 31,386]401.

Elbert, T., 1992. A theoretical approach to the late compo-nents of the event-related brain potential. In: Aersten, A.,

Ž .Braintenberg, V. Eds. , Information Processing in the Cor-tex: Experiments and Theory. Springer-Verlag, Berlin.

Eme Robert, F., 1992. Selective female affliction in the devel-opmental disorders of childhood: A literature review. J.Clin. Psychol. 21, 354]364.

Erez, A., Pratt, H., 1992. Auditory event-related potentialsamong dyslexic and normal-reading children: 3 clet andmidline comparisons. Int. J. Neurosci. 63, 247]264.

Galaburda, A., Livingstone, M., 1993. Evidence for a magno-cellular defect in developmental dyslexia. In: Tallal, P.,

Ž .Galaburda, A.M., Llinas, R.R., Euler, C.V., Eds. . Tem-´poral Information Processing in the Nervous System: Spe-cial Reference to Dyslexia and Dysphasia. Ann. N.Y. Acad.Sci. 682, 70]82.

Gough, P.B., Tunmer, W.E., 1986. Decoding, reading andreading disability. Remedial Spec. Educ. 7, 6]10.

Hillyard, S.A., Picton, T.W., 1987. Electrophysiology of cogni-Ž .tion. In: Plum F., Ed. , Handbook of Physiology, American

Physiological Society. Washington, DC, pp. 519]584.Holcomb, P.J., Ackerman, P.T, Dykman, R.A., 1985. Cognitive

event-related brain potentials in children with attentionand reading deficits. Psychophysiology 22, 656]667.

Holcomb, P.J., Ackerman, P.T, Dykman, R.A., 1986. Auditoryevent-related potentials in attention and reading disabledboys. Int. J. Psychophysiol. 3, 263]273.

Iragui, V.J., Kutas, M., Mitchiner, M.R., Hillyard, S.A., 1993.Effects of aging on event-related brain potentials and reac-tion times in an auditory oddball task. Psychophysiology 30,10]22.

John, E.R., Prichep, L., Ahn, H., Easton, P., Friedman, J.,Kaye, H., 1983. Neurometric evaluation of cognitive dys-functions and neurological disorders in children. Prog.Neurobiol. 21, 239]290.

Johnson Jr., R., 1989. Developmental evidence for modalitydependent P300 generators: a normative study. Psychophys-iology 26, 651]667.

Just, M., Carpenter, P.A., 1992. A capacity theory of compre-hension: individual differences in working memory. Psy-chol. Rev. 99, 122]149.

Loiselle, R.A., Stamm, J.S., Maitincky, S., Whipple, S.C., 1980.Evoked potential and behavioral signs of attentive dysfunc-tion in hyperactive boys. Psychophysiology 17, 193]201.

Loveless, N.E., 1983. Event-related brain potentials and hu-

( )J. Bernal et al. r International Journal of Psychophysiology 36 2000 11]23 23

Ž .man performance. In: Gale, A., Edwards, J.A. Eds. , Physi-ological Correlates of Human Behavior, vol. 2. AcademicPress Inc, London.

Lyon, R., 1982. Subgroups of learning disabled readers: Clini-Ž .cal and empirical identification. In: Myklebust, H.R. Ed. ,

Progress in Learning Disabilities, vol. 5. Grune and Stra-ton, New York, pp. 103]133.

Mattis, S., French, J.H., Rapin, T., 1975. Dyslexia in childrenand adults: Three independent neuropsychological syn-dromes. Dev. Med. Child Neurol. 17, 150]163.

McCarthy, G., Wood, C.C., 1985. Scalp distributions of event-related potentials: an ambiguity associated with analysis ofvariance models. Electroencephalogr. Clin. Neurophysiol.62, 203]208.

McIsaac, H., Polich, J., 1992. Comparison of infant and adultP300 from auditory stimuli. J. Exp. Child Psychol. 53,115]128.

Naatanen, R., Picton, T., 1987. The N1 wave of the human¨¨ ¨electric and magnetic response to sound: a review andanalysis of the component structure. Psychophysiology 24,375]425.

Oken, B.S., 1990. Endogenous event-related potentials. In:Ž .Chiappa, K.H. Ed. , Evoked Potentials in Clinical

Medicine. Raven Press, New York, pp. 563]592.Ostrosky, F., Navarro, M.E., Canseco, E., Perez, R.y, Zarate,´ ´

A., 1984. La lectura y los perfiles cognoscitivos de unapoblacion escolar mexicana. Rev. Mex. Psicol. 1, 53]65.´

Picton, T.W., 1988. The endogenous evoked potentials. In:Ž .Basar, E. Ed. , Dynamics of Sensory and Cognitive Pro-

cessing by the Brain. Springer-Verlag, Berlin, Heidelberg,pp. 258]265.

Pinkerton, F., Watson, D.R., McClelland, R.J., 1989. A neuro-physiological study of children with reading, writing, andspelling difficulties. Dev. Med. Child. Neurol. 31, 569]581.

Polich, J., Ladish, C., Burns, T., 1990. Normal variation ofP300 in children: age, memory span, and head size. Int. J.Psychophysiol. 9, 237]248.

Preston, M.S., Guthrie, J.T., Kirsh, I., German, D., Childs, B.,1977. VERs in normal and disabled adult readers. Psy-chophysiology 14, 8]14.

Rayner, K., Pollatsek, A., 1989. The Psychology of Reading.Prentice Hall, Englewood Cliffs, NJ, pp. 529.

Regiosa, V., Perez, M.C., Manzano, M., Antelo, J.M., 1994.´Sistema automatizado para explorar la lectura en escolaresde habla hispana. Rev. Latina. Pensamiento Lenguaje 2,141]160.

Satterfield, J.H., Bradley, B.W., 1977. Evoked potentials andbrain maturation in hyperactive and normal children. Elec-

troencephalogr. Clin. Neurophysiol. 43, 43]51.Satterfield, J.H., Schell, A.M., Nicholas, T.W., Satterfield, B.T.,

Freese, T.E., 1990. Ontogeny of selective attention effectson event-related potentials in attention-deficit hyperactivitydisorder and normal boys. Biol. Psychiatry 28, 879]903.

Shibasaki, H., Miyazaki, M., 1992. Event-related potentialsstudies in infants and children. J. Clin. Neurophysiol. 9,408]418.

Shields, D.T., 1973. Brain responses to stimuli in disorders ofinformation processing. J. Learn. Disabil. 6, 37]41.

Silva, J., Harmony, T., Bernal, J. et al., 1995. Comparacion´entre las habilidades en la lectura de dos grupos condiferente desempeno academico. Rev. Latina Pensamiento˜ ´Lenguaje 3, 65]81.

Simson, R., Vaughan Jr., H.G., Ritter, W., 1977. The scalptopography of potentials in auditory and visual discrimina-tion tasks. Electroencephalogr. Clin. Neurophysiol. 42,528]535.

Stanovich, K.E., 1988. Explaining the differences between thedyslexic and the garden-variety poor reader: the phonologi-cal core variable-difference model. J. Learn. Disabil. 21,590]604.

Stelmack, R.M., Saxe, B.J., Noldy-Cullum, N., Campbell, K.B.,Armitage, R., 1988. Recognition memory for words andevent-related potentials: A comparison of normal and dis-abled readers. J. Clin. Exp. Neuropsychol. 10, 185]200.

Swanson, H.L., 1993. Working memory in learning disabilitysubgroups. J. Exp. Child Psychol. 56, 87]114.

Swanson, H.L., 1994. Short-term memory and working me-mory: do both contribute to our understanding of academicachievement in children and adults with learning disabili-ties? J. Learn. Disabil. 27, 34]50.

Tallal, P., Miller, S., Fitch, R.S., 1993. Neurobiological basis ofspeech: a case for the preeminence of temporal processing.In: Tallal, P., Galaburda, A.M., Llinas, R.R., von Euler, C.´Ž .Eds. , Temporal Information Processing in the NervousSystem: Special Reference to Dyslexia and Dysphasia. Ann.N.Y. Acad. Sci., New York, 682, 27]47.

Taylor, M.J., Keenan, N.K., 1990. Event-related potentials tovisual and language stimuli in normal and dyslexic children.Psychophysiology 27, 318]327.

Torgesen, J.K., 1988. The cognitive and behavioral character-istics of children with learning disabilities. J. Learn. Disabil.21, 587]589.

Weber, B., Ommen, G., 1977. Auditory and visual evokedresponses in children with familial reading disabilities. J.Learn. Disabil. 10, 32]37.