Poor saccadic control correlates with dyslexia

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Pergamon

PII] S9917Ð2821"86#99069ÐX

Neuropsycholo`ia\ Vol[ 25\ No[ 00\ pp[ 0078Ð0191\ 0887 Þ 0887 Elsevier Science Ltd[ All rights reserved Printed in Great Britain 9917Ð2821:87 ,08[99¦9[99

Poor saccadic control correlates with dyslexia MONICA BISCALDI\ STEFAN GEZECK and VOLKER STUHR Brain Research Unit\ Institute of Biophysics\ University of Freiburg\ Germany "Received 07 April 0886^ accepted 5 December 0886#

Abstract*A large group of subjects\ either average readers or reading:spelling disabled subjects "n  074^ age between 7Ð14 years^ M  0223 years#\ were tested in various standardized cognitive tasks including reading:spelling assessment and in non!cognitive saccadic eye movement tasks[ Dyslexics were separated into a subgroup "D0# with de_cits in the serial auditory short!term memory and a subgroup "D1# with an isolated low achievement in reading:writing[ Control subjects had no relevant cognitive de_cit of any type[ Saccadic eye movements were measured in a single target and in a sequential!target task[ A signi_cant correlation was found between abnormal saccadic control and reading disability[ The two dyslexic groups showed only slight di}erences[ As compared to the control group\ the mean values of the standard deviations of the saccadic reaction times "SRT# and the amount of late saccades "SRT × 699# were signi_cantly increased in both dyslexic groups and especially in group D0 who also showed an increased amount of anticipatory saccades[ The number of express saccades "SRT  79Ð023 ms# was increased\ but not signi_cantly\ in D1 dyslexics[ Both dyslexic groups produced signi_cantly more regressive saccades in the sequential!target task[ The correlation between saccadic variables and {{reading factor|| was 9[3[ Signi_cant deviations from normal performance of the saccadic variables were found in an estimated 49) of the dyslexics as compared to 19) of the control subjects[ In spite of their worse level in saccadic control\ dyslexics also developed with age in the eye movement performance as the control subjects did[ Yet\ the development was slower in group D0[ It is suggested that reading process and saccade system are both controlled by visuoÐspatial attention and _xation systems that maybe impaired or develop slowly in many dyslexic subjects[ Þ 0887 Elsevier Science Ltd[ All rights reserved[ Key Words] saccadic eye movement^ express saccade^ dyslexia^ reading^ _xation^ attention^ overlap task[

a small subgroup of reading disabled children with visuoÐ spatial problems ð44Ł "see also review of Evans and Drasdo ð19Ł#[ Among the hypotheses claiming for a visual or visuomotor impairment in dyslexia\ a di}erence in the oculomotor behaviour between normally reading and reading disabled subjects remains a controversial issue[ The abnormal eye movement patterns that dyslexic sub! jects show during reading of text appropriate for their ages have been alternatively interpreted as speci_c for their reading disability or rather as a consequence of their linguistic di.culties ð0\ 04Ł[ Recent work has shown that normally reading subjects\ as well as dyslexics\ make a higher number of saccades and in particular of regressions and longer _xation durations when they read text material with di.culty above their present achieve! ment level ð26Ł[ A possible solution of the controversy is to consider saccadic eye movements made in non!cognitive tasks[ Unfortunately\ neither the claim that dyslexics make more regressions than normal subjects when looking at light stimuli sequentially presented from one side to the other ð41\ 42Ł nor that they have prolonged mean saccadic reaction times "SRT# in single target tasks ð06Ł have found consensus among di}erent research groups ð0\ 6\ 49\ 60Ł[

Introduction A speci_c reading disability\ or dyslexia\ has been gen! erally de_ned as {{a circumscribed impairment in the achievement of reading skills which is not caused by reduced visual acuity or neurological and psychiatric dis! eases or by inadequate educational support|| "ICD09# ð52Ł[ {{It is normally accompanied by persistent spelling and writing problems also in those subjects whose reading has reached a su.cient level of competence after many years of practice|| ð08Ł[ The existence of a separate popu! lation of dyslexic subjects ð53Ł or rather of a continuum of reading and writing abilities with the dyslexics at one end of a normally distributed population is still a matter of discussion ð58Ł[ While the claim that most dyslexics show phonological dysfunctions as well as poor performance in many linguis! tic tasks ð40\ 63Ł is well accepted\ the role of visual impair! ments has either been refused ð63Ł or has been limited to  To whom all correspondence should be addressed[ Institute of Biophysics\ Brain Research Unit\ University of Freiburg\ Hansastr[ 8\ D!68093 Freiburg im Brsg\ Germany[ E!mail] biscaldiÝuni!freiburg[de\ www[brain[uni!freiburg

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M[ Biscaldi et al[:Poor saccadic control correlates with dyslexia

After all\ the existence of a basic oculomotor de_cit has been proposed only for a small subgroup of dyslexics as a consequence of their visuoÐspatial problems ð44Ł[ In 0889 Fischer and Weber ð16Ł described di}erent groups of reading disabled subjects characterized\ in sin! gle target tasks\ by SRT distributions being signi_cantly di}erent from those of normally reading children[ One subgroup exhibited a tail of very long latencies[ Two other subgroups had shorter SRT than the control sub! jects] they made either more\ or exclusively saccades with very short latencies peaking at about 099 ms\ which are called express saccades ð10Ł[ Express saccades "latencies between 69Ð099 ms in mon! key and between 79Ð024 ms in man# are known to be easily elicited if a time interval "gap# is introduced between _xation point o}set and target onset ð13Ł[ Their number increases with training ð15Ł and can be modulated by directed attention ð33\ 64Ł[ These experimental obser! vations and the results of electrophysiological and lesion studies in the monkey ð56Ł have supported the idea of a basic optomotor circuit through the primary visual cortex and the superior colliculus controlled by cortical neural substrates underlying decision\ attention and _xation processes ð10\ 14\ 17Ł[ It was suggested that an express saccade can be elicited when\ for example due to inter! ruption of active _xation\ the processes of decision and disengagement of attention ð45Ł have been already ter! minated at the time of target onset[ The increase in the number of express saccades and the tail of long latencies observed in the SRT distributions of dyslexic subjects were therefore interpreted as a di.culty in engaging or disengaging attention from the _xation point ð16Ł[ In more recent studies ð2\ 3\ 12Ł\ we applied single target tasks and various sequential target tasks "similar to those used by Pavlidis ð41Ł# to two subjects| groups of di}erent age "13 children] 8Ð00 years^ 13 adults] 11Ð44 years#[ The subjects were de_ned as control or dyslexic by a diagnostic psychometric test battery[ Signi_cant eye movement deviations were found in the number of sac! cades and mean _xation durations made in the sequential target tasks as well as in the standard deviation of the SRT\ in the number of corrective saccades and in the number of express saccades made in single target tasks[ Some dyslexic subjects even produced almost exclusively express saccades[ The unusual saccade performance of these subjects\ the so!called express!saccade makers who are more frequently found among dyslexics than among normally reading subjects ð4Ł\ was explained according to the notion of a _xation system gating the generation of saccades at the cortical and collicular level ð22\ 35\ 54Ł[ It was concluded that a defect in attentive _xation could be responsible for the oculomotor abnormalities of many dyslexic subjects[ The aims of the present study were] "0# to extend previous results about saccadic eye move! ments to a much larger group of subjects and de_ne the correlation between saccadic performance and reading disability[

"1# to take into account the development of the saccade system\ which is known to occur rapidly in normally reading children above age of 8Ð00 years ð11Ł[ "2# to study the most characteristic cognitive aspects of the population considered as they resulted from the psychometric testing and to relate them with the sub! jects| saccadic performance[ The results con_rm that dyslexics as a group perform di}erently in saccadic tasks than subjects without a read! ing:spelling disability[ Dyslexic subjects can be de_ned through di}erent cognitive pro_les that have some relationship with the type of saccadic abnormality observed[ The measurement of saccadic eye movements may be considered as an additional diagnostic tool whose usefulness is to identify subjects whose saccadic control is disrupted and not developing at the same rate as normally reading age!matched subjects[

Methods Subjects and psychometric tests Most of the 074 subjects "016 males\ 47 females\ age between 7Ð14 years# included in the statistical analysis were children and teenagers "M  012 years#[ They had been either recruited from local primary and secondary schools or introduced in our laboratory by teachers\ physicians and parents seeking diag! nostical assessment of dyslexia[ Many of the younger subjects already received special support or therapy to improve their reading and spelling problems[ None of the subjects su}ered from neurological or psychiatric illness[ Their visual acuity was normal or corrected to normal[ Peripheral auditive impairments in severe disphonetic subjects had been excluded by audiometric tests[ Twenty!four children and some adults had already par! ticipated in previous studies ð3\ 12Ł[ The following psychometric tests "widely employed in Germany for the diagnosis of dys! lexia# provided the aptitude and achievement pro_les of the subjects] "0# Handedness] tracing\ dotting\ tapping on squares for chil! dren up to 00 years ð61Ł[ Otherwise a check list from the {{British Assessment of Handedness|| was used[ "1# Evaluation of the intelligence level] Coloured Progressive Matrices "CPM# ð50Ł or Standard Progressive Matrices "SPM# ð48Ł or WISC:WISA ð65\ 66Ł or the Kaufmann K! ABC battery ð27Ł[ The global measurement of intelligence was entered as variable for the analysis[ "2# Attentional!concentration performance] Test d1 ð01Ł[ The subjects had to tick within a given time as many target letters embedded in a line of distractors as possible[ Result variables were velocity "number of recognized letters per line# and errors "number of ticked distractors#[ "3# Sequential digit recall after verbal presentation] ZFG from the Adaptive Intelligence Test ð39Ł[ The digits had to be repeated either in "a# forward or in "b# backward sequence and the result variable was the maximal number of digits that could be repeated in the same order without errors[ The {{digit recall|| is also a test included in the verbal intel! ligence scale of WISC and WISA and in the sequential processing scale of the K!ABC[ "4# Non!word recall with auditive phonological discrimination] Mottier test ð34Ł[ Recall of verbally presented non!words formed by a sequence of two or more consonant!vowel

M[ Biscaldi et al[:Poor saccadic control correlates with dyslexia syllables[ This test o}ers a valid screening for auditive phonological discrimination ability and short!term verbal memory[ The number of correctly repeated words was used for the analysis[ "5# Reading] Zurcher Lesetest\ Forderdia`nostik der Le`asthenie ð23Ł for children up to 01 years[ Teenagers and adults had to read a short story aloud[ Reading time and number of reading errors "number of words that were not correctly read# were the entered variables[ "6# WritingÐSpelling "writing critical words at dictation#] the standardized tests DRT 2 ð37Ł\ WRT 3:4 ð46Ł\ WRT 5¦ ð47Ł\ or RT {{Der Nichtraucher|| ð1Ł were applied for di}er! ent school grades and age levels[ The subjects performances were stored as standardized scores "each psychometric test supported the performance assessment in a representative population resulting in gaussian distributed values# with the exception of the Mottier!Test and of the reading test for subjects of age above 01 years[ In this case\ the reading velocity and number of reading errors were directly stan! dardized on the population tested[ The non!standardized scores resulting from the Mottier!Test were then transformed "Box! Cox transformation# to obtain normal distributed values whose sign was inverted in order to relate positive values to better performances[ Subjects with IQ lower than 80 were excluded from the study[ The diagnostic criteria and resulting sub! grouping are described in the Results section[

Saccade tasks and stimuli Saccadic eye movements were measured in two experimental sessions\ both using an overlap paradigm with _xation and saccade targets remaining visible once being presented[ We used an overlap paradigm since the generation of express saccades in this case seems to be dependent of the _xation ability of the subjects ð4Ł[ In the single target task\ the _xation point was presented 0[6 s before target onset and both stimuli were turned o} after 799 ms of target presentation[ The target appeared randomly at 3> eccentricity to the left or right of the _xation point[ The interval between trials varied randomly between 0 and 0[4 s[ The subjects had to _xate the _xation point accurately before they looked at the target as soon as it appeared[ They were not encouraged to react {{as fast as possible|| in order to avoid a bias toward {{guessing|| the side of target appearance[ In the sequential targets task\ the _rst _xation stimulus appeared at the left side of the screen for a period of 0[1 s and was followed by four targets appearing on the same horizontal line in sequence every second and 3> apart[ The subjects had to _xate the _rst stimulus and then to look at the next target when it appeared[ They were requested to avoid blinks until all targets had been scanned[ Subjects were given the opportunity of some trials for practice before each experimental session was started[ The single target task was always performed _rst[ One hundred and _fty trials\ 64 for each side\ were collected in the single target task and 24 trials were collected in the sequential target task[ The visual stimuli\ consisting in a red _xation square "9[0>×9[0># for the single target task and in white target squares "9[1>×9[1># for both the single and sequential targets task\ were generated by a personal computer and presented on an RGB colour monitor using a graphic interface "mirograph 400# with a resolution of 0913×599 Pixels[ Stimuli onset times were syn! chronized with the screen frame rate "79 Hz#\ also taking into account the constant time delay between the synchronization pulse and the horizontal level at which the stimuli were presented[ The luminance of the stimuli was well above thres! hold\ 00 cd:m1 and 26 cd:m1\ respectively\ for the red and the white squares[ The background luminance was 2 cd:m1[

0080

Eye movement recording and analysis The subjects sat on an adjustable chair 46 cm in front of an EIZO 8979i computer monitor with their heads stabilized by a chin rest[ Movements of the left eye were measured using an infrared!light re~exion method ð29Ł[ The device was mounted on a spectacle frame either directly _xed on the subjects| head or through a helmet "IRIS System of the SKALAR medical#[ The analogue signal from the horizontal eye movement was digitized and stored on a computer disk with 0 ms temporal and 9[0> spatial resolution[ Calibration was checked before each experimental session] the gain and o}set of the recording device were adjusted until a one!to!one spatial relationship was obtained between eye position signal and the position of a stimulus moving smoothly or jumping 7> to the left and right[ During the o}!line analysis the sampled values were di}er! entiated to compute eye velocity[ All saccades after stimulus onset were detected by an eye velocity criterion of 29> per s[ The start and the end of a saccade were de_ned as the time when eye velocity crossed 19> per s[ Saccade latency was measured as the time between target onset and start of the saccade[ Saccade size and duration were calculated from the di}erences in eye position and in time between the start and the end of the saccade[ In the o}!line data analysis\ all trials that were con! taminated by artefacts "mainly caused by blinks or head move! ments# were discarded[ The total fraction of rejections did not normally exceed 09) of all trials[ During o}!line analysis\ the online calibration was checked once again and\ in the case of small deviations\ calibration was corrected by setting the mean change in the _nal eye position to 23>[

Variables and statistical analysis For the analysis of the psychometric data we considered 7 psychometric variables] "0# "1# "2# "3# "4# "5# "6# "7#

General intelligence "Intell#\ Performance in the d1 concentration test "Att!Loading#\ Sequential digit recall forwards "Digit Recall!v#\ Sequential digit recall backwards "Digit Recall!b#\ Auditive syllable di}erentiation "Phonol#\ WritingÐspelling performance "Spelling#\ Reading performance as reading errors "Reading Err#\ Reading performance as reading time "Reading Time#[

Ten oculomotor variables were considered separately for right and left targets in the single target task ð09×1Ł and three variables in the sequential targets task[ Time variables from the single target task were] "0# The mean SRT\ "1# The standard deviation of the SRT "SRT!SD# which\ as independent variable\ o}ers an objective measure of the temporal consistency in triggering saccades[ Previous studies have shown that SRT distributions are not unimodal but tend "optimally after training# to build up discrete peaks that can be mathematically calculated ð21Ł and underlie the di}erent saccadic populations described in Fischer et al[ ð18Ł[ We applied to the SRT the latency ranges where these peaks had been identi_ed as] "2# Percentage of express saccades "Exp Sacc# with latency between 79 and 023 ms\ "3# Percentage of fast regular saccades "Fast Sacc# with latency 024Ð068 ms\ "4# Percentage of slow regular saccades "Slow Sacc# with lat! ency 079Ð288 ms[

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M[ Biscaldi et al[:Poor saccadic control correlates with dyslexia

In addition\ we considered as separate variables the percentages of] "5# Saccades with latencies beyond the discrete latency peaks described above "Late Sacc# with latency 399Ð588 ms[ "6# Anticipatory saccades "Antic Sacc ³79 ms# ð18\ 67Ł "7# Saccades with latency beyond the normal time processing for simple light targets "Too Late Sacc −699 ms# Since anticipatory saccades cannot be triggered by target onset "on the half they are direction errors# and too late saccades cannot be elicited by the target\ which has already disappeared\ their number was not included in the calculation of the mean SRT\ the SRT!SD and the relative amount of target!elicited express\ fast\ slow and late saccades[ Accuracy variables speci_ed the percentage of trials that were corrected by a second saccade] "8# In the same direction "Under# "09# in the opposite direction "Over#[ From the sequence TT\ we considered] "00# The mean number of saccades in the target direction "N Sacc!ri#\ "01# The mean number of regression saccades "N Sacc!le#\ "02# The amplitude of regression saccades "Ampl Sacc!le#[ A recent study has described a signi_cant age!dependence of many saccadic variables\ e[g[ of SRTs and voluntary saccade control ð11Ł[ Hence\ before we carried out the statistical analysis on the eye!movement data of the subjects of the present study\ their results were normalized by the saccadic means and stan! dard deviations of a standard population of the same age group[ The standard population consisted in about 299 subjects who had been recruited among friends\ people working at the uni! versity\ in schools and neighbourhood[ Most of these subjects had not been psychometrically assessed and had participated in the already mentioned study of the saccadic development ð11Ł[ In this study\ the subjects had been classi_ed into 5 age groups] 7 years "10 subjects#\ 8Ð09 years "67 subjects#\ 00Ð01 years "27 subjects#\ 02Ð04 years "35 subjects#\ 05Ð19 years "31 subjects# and 10Ð14 years "36 subjects#[ The values of the eye!movement variables of our 074 subjects were computed according to the standardized deviation from the mean of the corresponding age level[ For example\ a SRT of 0[4 would indicate that the mean SRT of a given child falls above the mean of an age!matched control group by 0[4 times the standard deviation in that group[ A factor analysis was applied to the eight psychometric vari! ables in order to study in detail the main cognitive pro_les arising from the population studied[ We chose the principal factor method ð24Ł[ The factor analysis assumes a linear model of the variables[ The weight of each single variable was _tted in order to obtain the best reproduction of the correlations between the eight psychometric variables[ An analysis of variance "ANOVA# tested the hypothesis of di}erent group mean values for the oculomotor variables[ We computed a linear regression between psychometric scores and selected oculomotor variables to de_ne how saccadic variables related to the reading problems of the subjects[ SPSS was employed as statistical program throughout^ a ¾ 9[94 was taken as minimal criterium for signi_cance and marked on the _gures with one asterisk "#[ Two asterisks "# indicate a signi_cance level ¾9[90[

Results Psychometric results Psychometric classi_cation of the subjects[ To decide for each subject whether he:she should be considered

belonging to a control or a dyslexic group we followed the general de_nition of speci_c reading disability or dyslexia according to the {{International Classi_cation of Dis! eases|| "ICD!09 ð52Ł# based on the discrepancy between actual reading achievement and expectancy from the gen! eral intellectual abilities[ The international classi_cation of diseases states also that {{persistent spelling and writing problems are normally found also in those subjects whose reading has reached a su.cient level of competence after many years of practice|| ð08Ł[ Following these statements\ a subject was classi_ed as dyslexic if he:she scored in the reading or in the spelling! writing test at least one standard deviation below the IQ! score obtained in the intelligence test[ A second criterion of low reading:spelling achievement with respect to an age!matched standard population was introduced so that the mentioned discrepancy criterion had to be accompanied by a reading or spelling performance below the 14) level relative to a standard population of the same school grade[ Overall\ only subjects with IQ × 89 were included in the study to avoid the presence of backward readers[ Ninety!three subjects "65 males\ 06 females^ M  0122 years# were classi_ed as dyslexic[ The remain! ing 81 subjects "40 males\ 30 females^ M  0223 years# were used as control subjects[ The psychometric testing provided\ along with achieve! ment level and general intelligence\ a subject performance in tasks measuring functions that are known to be often impaired in dyslexics\ i[e[ auditive phonological dis! crimination\ sequential memory and attentional!con! centration loading[ In the following we will consider two groups of dyslexics] D0 dyslexics "34 males\ 01 females^ M  0022 years# whose sum of the performances avail! able from the phonological "Mottier#\ attentional!loading "d1#\ and digit recall "ZFG# tests was below the mean of the entire population in these tests^ D1 dyslexics "20 males\ 4 females\ M  0222 years#\ in the opposite case "sum of the performances above the population mean#[ This subgrouping corresponds to earlier subgrouping based on a clinical de_nition ð3Ł[ The type of classi_cation chosen allowed the separation of a group of {{pure|| dys! lexics with isolated reading:spelling problems "D1# and very good cognitive performances from dyslexics whose reading:spelling di.culties are associated with speci_c cognitive!attentional impairments ð60Ł[ Intriguing was the hypothesis of a stronger association of oculomotor abnormalities with {{pure|| "D1# dyslexics\ since they apparently do not present any other problem that could shed light on their poor reading and spelling achievement[ Table 1 lists the mean raw scores "as values of cumu! lative gaussian distributed variables# of the whole popu! lation and of the control\ D0\ and D1 groups in the psychometric tests[ The results of the ANOVA in Table 1 refer to the gaussian distributed variables[ Group D0 had a slightly lower mean intelligence!value "but yet well on the average# relative to the other two groups as well as slightly lower scores in the spelling and reading tests

M[ Biscaldi et al[:Poor saccadic control correlates with dyslexia

Fig[ 0[ Distributions of subjects| age in the control\ D0 and D1 groups[ The three curves are superimposed to allow a direct comparison[ The slight di}erence in the distributions "more children of age ³ 02 years and less teenagers in the D0 group# was statistically not signi_cant[

than group D1[ The age distribution of the subjects was slightly di}erent in the three de_ned psychometric groups "Fig[ 0# but this was far from signi_cance level at the ANOVA "F"071\1#  2[9\ P × 9[94#[ Main effects in the psychometric variables[[ The next analysis looked for main e}ects and speci_c cognitive pro_les arising from the psychometric variables[ The fac! tor analysis "principal factor method# extracted two fac! tors after computing the correlation matrix of all eight psychometric variables[ The loadings of the single vari! ables are shown in Table 0[ Factor 0 carried the largest variance between the subjects and was de_ned as {{Read! ing Factor||\ since the reading variables had the highest loading[ The largest loading on Factor 1 was yielded by the short!term memory\ sequential processing "forward digit recall# ability[ Therefore\ we called Factor 1 {{Sequ! encing Factor||[ Inserting the individual psychometric values into the two linear functions "Factor 0 and 1# resulted in estimated individual scores for each subject "plotted in Fig[ 1^ _lled circles\ empty squares\ and stars indicate D0\ D1\ and control subjects\ respectively#[ Since the highest loading

Table 0[ Loadings of the di}erent psychometric variables on the two factors resulting from the factor analysis according to the principal factor method Psych variables Intell Att!loading Digit recall!v Digit recall!b Phonol "Mottier# Spelling Reading error Reading time

Factor 0

Factor 1

−9[94 −9[94 −9[06 9[993 −9[94 9[02 9[43 9[31

9[04 9[04 9[48 9[98 9[06 9[09 −9[96 −9[03

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for Factor 0 was carried by the reading performance\ one can conclude that the reading performance and less the spelling performance\ characterized the di}erence between control and dyslexic subjects[ The overlap between the dyslexic groups and the controls along the ascissa suggests "as already implied in the standardization of the psychometric tests# that reading achievement builds up a continuum of performances[ Yet\ since in both factors the loading of the intelligence was very small\ Fig[ 1 does not carry any information about the dis! crepancy between actual reading and {{expected|| achieve! ment level[ So\ the question whether dyslexics forms a separate population or not remains open[ The fact that the second relevant factor arising from the analysis well separated D0 and D1 dyslexics gives support to the idea of a subgrouping based on cognitive performances[ The signs before the loadings for the di}erent variables in Factor 1 "and also in Factor 0# underline the opposite e}ect of reading compared to other cognitive performances[ In particular\ the D1 dys! lexics with good performances "high values# in the digit span and bad performances "low values# in reading reached high scores in Factor 1[ Many control subjects with normal digit span scores but very good reading performance could not achieve very high scores of Factor 1 and therefore also overlapped with the D0 dyslexics "see Table 1] the mean value of the digit span in group D0 lays one standard deviation below the mean value for the control group#[

Oculomotor results Differences in the eye movement performance of the psychometric groups[ The raw mean values and standard deviations of all the 12 saccadic variables for the whole population and for the three psychometric groups are illustrated in Tables 2 and 3 along with the results of the ANOVA "applied on the gaussian distributed variables that had been normalized according to age#[ All three variables from the sequential targets task "number of saccades to the right and regressions#\ four variables from the single target task for the left target "SRT!SD\ fast\ slow and too late saccades# and three variables for the right target "SRT!SD\ anticipatory and too late saccades# signi_cantly di}erentiated between the psychometric groups[ Since the dyslexic groups contained a higher pro! portion of males as compared to the control group\ an ANOVA tested the e}ect of group di}erences by gender with the signi_cant eye movement variables as dependent variables[ The e}ect for all variables was far from sig! ni_cance[ Figures 2 and 3 display examples of SRT distributions in the single target task and of raw data in the sequential targets task from two control subjects and four age!mat! ched D0\ D1 subjects who showed eye movement patterns representative for their group[ Con_rming the results of

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M[ Biscaldi et al[:Poor saccadic control correlates with dyslexia

Table 1[ Normal distributed values of the psychometric variables with the exception of the scores in the Mottier!test which were transformed before statistical analysis[ The F!values refer to the results of the ANOVA with the three groups of control "CON#\ D0\ and D1 subjects as factor

Psychometric tests

ALL "016 male\ 47 female# CON D0 D1 mean2SD "40 male\ 30 female# "34 male\ 01 female# "20 male\ 4 female#

Intell Att!loading Digit recall!v Digit recall!b Phonol Spelling Reading error Reading time

4626 4227 49209 40200 06209 35202 34200 35200

4526 4227 44200 43201 0226 4228 4127 4227

4326 3725 3227 3528 12209 2426 2326 2626

4824 4726 4026 4127 0923 2627 2825 3926

F"1^003# 2[7 02[0 08[9 00[2 21[2 61[6 52[6 46[5

  P ³ 4)\   P ³ 0)[

Fig[ 1[ Results of the factor analysis with the principal factor method[ The symbols indicate the subjects| classi_cation after psychometric grouping according to discrepancy criteria "described in the Method section#[ Factor 0 mainly described the reading performance of the subjects and indicated the best separation between dyslexic and control subjects[ Factor 0 was de_ned as {{Reading Factor|| "whose individual scores cal! culated for all the 074 subjects are plotted on the x!axis#[ D0 and D1 subjects are separated along the y!axis\ which represent Factor 1 mainly describing the sequencing processing ability of the subjects[ D1 dyslexics had been de_ned as subjects with the best cognitive performances in spite of low achievement in reading and spelling[

previous studies ð3\ 12Ł\ D0 subjects are characterized by an increased scatter of the SRTs "larger SRT!SD\ which is paralleled by an increase of anticipatory\ late and too late saccades\ see Fig[ 2 and Table 2#[ The control subjects\ in the middle panel\ exhibit regular SRT dis! tributions with discrete peaks in typical latency ranges "modes or saccadic populations# that\ by contrast\ are virtually absent in D0 subjects[ The D1 subjects "bottom panel# exhibited a signi_cant larger scattering of the SRT too "left panel of Fig[ 2 and Table 2#[ Also\ many subjects of the D1 group produced a clear saccadic mode around 099 ms consisting of a considerable number of express saccades "more than 29)\ right panel of Fig[ 2#\ which

is unusual for an overlap single target task[ The increased number of express saccades in this group "Table 2# did not reach the signi_cance level yet\ because of the large variability within subjects in eliciting express saccades[ The examples of raw data from the sequential targets task in Fig[ 3 show an irregular timing in triggering sac! cades in D0 subjects and short!latency "express# saccades elicited after the target onsets in D1 subjects[ In both D0 and D1 groups the number of regressive saccades was increased as compared with the control group "Table 3#[ Also\ regressive saccades had larger amplitude in group D0[ Reproduction of the individual {{Readin` Factor|| by the saccadic eye movement variables[ The ANOVA\ con! sidering the group mean values\ found signi_cant di}er! ences between the oculomotor behavior of normally reading and two de_ned groups of dyslexic subjects[ Now\ the question arose how the oculomotor behavior correlated with the grade of reading impairment of the individual subjects[ The grade of reading impairment was expressed by the {{Reading Factor|| or Factor 0 from the factor analysis on the psychometric tests "Fig[ 1#[ We tried to reproduce the single scores of the {{Reading Factor|| using a _tting procedure on a chosen pool of thirteen oculomotor variables[ The variables were selec! ted among those signi_cantly di}erentiating between the groups "Tables 2 and 3# and other variables as SRT\ undershoots\ overshoots "right target# and late saccades "left target# that did not turn out signi_cant but showed poor intercorrelation[ The _t parameters "weights of the thirteen eye move! ment variables# were optimized on 26 selected subjects "01 control\ 01 D0\ and 02 D1 subjects#\ whose oculomotor behaviour was particularly representative for their group[ A linear model underlying the relationship between the {{Reading Factor|| and the 02 eye movement variables was assumed to reproduce the {{reading scores|| of these test subjects by their individual eye movement data[ Within the linear model the weights of the 02 eye move! ment variables were _tted in order to minimize the di}er!

M[ Biscaldi et al[:Poor saccadic control correlates with dyslexia

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Table 2[ Raw values of the saccadic eye movements variables in the overlap single target task[ The F!values refer to the results of the ANOVA on the standardized variables "see text# with the three groups of control\ D0\ and D1 subjects as factor Variables

ALL means2SD

CON

D0

D1

F"1\071# 9[20 1[16

SRT ðmsŁ

le ri

121238 129234

121237 114232

122236 126233

114231 109228

SRT!SD ðmsŁ

le ri

68227 70223

61222 63220

74223 78222

71227 71218

5[04 3[96

Exp Sacc ð)Ł

le ri

01204 02205

00206 00204

01200 01201

05205 10210

9[56 1[62

Fast Sacc ð)Ł

le ri

19203 12204

07203 13204

12202 08202

19200 13201

2[33 0[31

Slow Sacc ð)Ł

le ri

48211 45210

51212 47210

43208 47206

44212 37211

2[14 1[74

Late Sacc ð)Ł

le ri

8201 828

8200 728

00202 00209

8201 626

0[15 9[75

Too Late Sacc ð)Ł

le ri

9[229[3 9[129[1

9[129[1 9[129[1

9[429[3 9[429[2

9[429[3 9[929[0

3[22 3[94

Antic Sacc ð)Ł

le ri

524 524

424 423

623 724

424 523

1[89 5[02

Under ð)Ł

le ri

28210 28210

27213 26211

30206 28207

31208 35210

9[31 0[66

Over ð)Ł

le ri

526 527

426 528

325 224

526 628

0[31 1[95

  P ³ 4)\   P ³ 0)[

Table 3[ Variables of the saccadic eye movements in the overlap sequential task[ See Table 2 Variables

ALL means2SD

CON

D0

D1

F"1\071#

Ampl Sacc ð>Ł

le

0[229[5

0[129[5

0[529[6

0[029[3

6[99

N Sacc

le ri

9[629[4 5[520[1

9[529[4 5[720[1

9[729[3 5[220[0

9[729[4 5[620[0

3[81 2[12

ence between the actual {{Reading Scores|| and their reproduction by the eye movement data[ The model function resulting from this analysis was applied to reproduce the individual loadings of the {{Reading Factor|| for all subjects of the study "Fig[ 4#[ Negative scores of the {{Reading Factor|| on the hori! zontal axis of Fig[ 4 correlates with a {{bad|| oculomotor performance on the vertical axis[ A signi_cant correlation between the two factors was found "correlation index  9[3#[ If one takes 0 SD below the mean value of the ocu! lomotor score as cut!o} point between a normal and a {{deviant|| oculomotor behavior\ 43) of the D1 subjects\

37) of the D0 but only 19) of the control subjects fall in the {{deviant|| region[ In a last step\ the weights of the 02 oculomotor variables were _tted by linear regression to reproduce the individual values of the eight psychometric tests[ This way tried to investigate a possible relation between saccadic eye move! ments and psychometric variables[ Interestingly\ the vari! able intelligence was not related to the oculomotor performance at all "P  9[14# whereas the other psycho! metric variables show some dependency with the saccadic variables "P!values between 4) and 09)#[ The highest relationship was found for the reading and writing!spelling performances "P ³ 9[9990 and P ³ 9[90\ respectively#[

0085

M[ Biscaldi et al[:Poor saccadic control correlates with dyslexia

Fig[ 2[ Examples of SRT distributions obtained from single subjects of the three psychometric groups in the single target task[ The thin and thick lines represent distributions for the left and right target\ respectively[ Latencies are plotted on the x!axis and the probability with which a saccade fell in a latency bin width of 0 ms is plotted on the y!axis "the data are smoothed using the kernal method^ the gaussian kernal had a bandwith of 0[4 ms#[ The distributions of the control subjects exhibit more or less clearly two peaks that correspond to the peaks of fast and slow regular saccades described in the literature[ The distributions of the dyslexic subjects are more scattered "some of them fall beyond the 499 ms limit of the diagrams#[ In addition\ the D1 subjects show a clear peak with short latencies in the range of 79Ð023 ms "somewhat shifted to the right in subject AM#[ In the SRT!distributions of the D0 subjects one can no longer di}erentiate between discrete peaks of latencies[

M[ Biscaldi et al[:Poor saccadic control correlates with dyslexia

0086

Fig[ 3[ Examples of saccadic eye movements obtained in the sequential target task in the three groups[ Time is plotted on the x!axis and the vertical lines indicate the onset of the targets[ At the top of each graph the dots in the raster plots represent single saccades] the upper section is for the right!directed saccades\ the section below is for the left!directed saccades "regressions#[ Consecutive trials are shown one below the other[ In the middle\ the cumulative frequency distributions of the saccades are depicted and\ at the bottom\ the mean eye position averaged across trials is traced[ The D1 subjects show more saccades with smaller amplitude than the control subjects and the _rst distribution lays in the express!saccade latency range[ In the D0 subjects\ saccades were elicited with relatively slow\ scattering latencies[ In both dyslexic groups the number of regressions was increased as compared to the control subjects[

Cognitive and saccadic development of dyslexic subjects As one would expect from standardized tests\ no cor! relation was found between age and psychometric vari! ables for the control group[ This indicates that even for the not completely standardized reading and Mottier tests

the estimation of the developmental course was satis! factory[ The dyslexics groups\ however\ showed a di}erent developmental course as expected[ In the D1 group\ a signi_cant positive correlation was found between age and reading time "r  9[41\ P  9[990# and a negative

0087

M[ Biscaldi et al[:Poor saccadic control correlates with dyslexia

Fig[ 4[ Reproduction of the {{reading scores|| by 02 selected saccadic eye movements variables[ The single subjects and their psychometric classi_cation are indicated by the symbols[ Circled symbols mark 26 test subjects whose data were _tted in order to _nd out an optimal model function "see text for methodological details#[ Negative scores mean poor reading performances on the x! axis and a {{deviant|| oculomotor performance on the y!axis[ A signi_cant correlation between the two scores was found[

one for the spellin` performance "r  −9[33\ P  9[996#[ In the D0 group\ there was a clear negative correlation of backward!digit recall "r  −9[24\ P  9[91#[ This means that D1 subjects tend to improve their reading time "but not their reading errors;# with age faster than control subjects whereas their writing!spelling performance develops slower[ Hence\ the discrepancy between the writing performances of normally reading and dyslexic subjects of older age turns out to be higher than that of younger subjects[ Finally\ we computed the correlations between age and the 02 selected saccadic variables to look for deviant oculomotor age!dependent development in the dyslexic groups[ The saccadic performance of group D1 developed normally although it never reached the level of the control subjects[ This was also true in group D0 for the variables from the sequential targets task[ By contrast\ in group D0 the variables SRT\ SRT!SD\ and amount of anticipatory saccades from the single target task were not only deviant with respect to the control group but they also seemed to develop more slowly than in the control subjects[

Discussion A factor analysis on various psychometric variables indi! cated a continuous distribution of reading:spelling abilities and of cognitive abilities[ The cut point between control and dyslexics was therefore based on criteria of low achieve! ment and of a de_ned amount of discrepancy from intel! ligence level[ Moreover\ we isolated two dyslexic subtypes mainly characterized by the quality of their performance in tasks requiring short!term memory and sequential process! ing[ It has been discussed whether or not abnormalities of sequential processing functions can be considered typical for dyslexic subjects ð57\ 27Ł[ In our study these anomalies were associated with a larger subgroup of dyslexics who

consist of a mixture of subjects with either clear phono! logical!linguistic de_cits or mild visuoÐspatial disorders ð7\ 32\ 43\ 60Ł[ The other subgroup D1 did not show any sequencing or other linguistic or visuoÐspatial problems at least according to the psychometric testing applied[ This group seems to match another subgroup of dyslexics de_ned by Satz and Morris on the basis of a cluster analysis carried on the results of a large neuropsychological test battery ð55Ł[ The authors considered that group {{unexpected|| because the subjects performed on the average\ or above\ in language and perceptual tests[ Yet\ we do not know whether more speci_c kinds of neuropsychological or psychophysical test! ing "for example of rapid sequential temporal processing ð62Ł# could reveal more subtle impairments in these subjects[ The separation of the subjects in {{pure|| dyslexics and dyslexics with other cognitive disorders was just partially reproduced by di}erent types of oculomotor deviations[ Indeed both dyslexic groups tended to generate saccades with an irregular time triggering but\ in addition\ D1 showed an increased tendency to generate re~exive fast saccades[ In previous studies\ the deviant oculomotor behaviour of reading disabled subjects has been explained by a de_cit of control functions "attentional and _xation processes# on the saccadic system ð3\ 16Ł[ Neuro! physiological data con_rm the existence of a spread system of _xation neurons at di}erent cortical and sub! cortical levels probably modulated by selective attention] neurons responsible for attentive _xation were found in the frontal eye _eld and parietal cortex ð22\ 54Ł and recently also in the deeper layers of the rostral part of the superior colliculus[ After chemical deactivation of these cells\ monkeys are no longer able to maintain _xation when a peripheral target appears in a memory!guided task[ This leads to irrepressible re~exive saccades to the target while\ in this case\ saccades should be triggered by _xation point o}set ð36Ł[ We know that subjects\ who make an excessive number of express saccades in an over!

M[ Biscaldi et al[:Poor saccadic control correlates with dyslexia

lap task\ have also di.culties in memory!guided and anti saccade tasks "in the latter case the subjects have to look in the direction opposite to the side where the target appeared# ð4\ 03Ł[ The _xation neurons together with build!up neurons in the build!up layers set the time for releasing a saccade "after visual or motor impulse# ð02\ 05\ 69Ł[ If the visual input in the burst layers is strong enough and the _xation neurons are deactivated\ then a saccade with express latency will be generated[ On the contrary\ activated _xation neurons together with a weak visual response will completely block saccade generation or favor the second motor response resulting in the gen! eration of fast or slow regular saccades[ In this case\ there will be enough time to complete voluntary decision processes\ e[g[ in the FEF[ An impairment of the collicular _xation neurons have been thought to be responsible for the increase of short! latency saccades "express saccades# in both dyslexic of type D1 and normally reading express makers ð4\ 03Ł[ Actually\ the present study has clearly shown that express saccades alone are not a marker for dyslexia[ An increase of the SRT!SD and of anticipatory saccades sometimes paralleled by an increase of express saccades can be con! sidered as a strong indication of reading problems and suggest that cortical levels of the _xation system are as well involved ð2\ 3\ 16Ł[ Since the ability to suppress sac! cades to the stimulus in an anti saccade task seems to be impaired in many dyslexic subjects independent of the number of express saccades generated ð5Ł\ the functional de_cit could extend for example to frontal structures that control the generation of voluntary eye movements[ Another possible explanation for the di}erences in sac! cadic performance found between dyslexic and control subjects points to the neural substrates that control selec! tive spatial attention[ Indeed\ attentional selection pro! cesses seem to modulate the grade of engagement of the _xation system ð02Ł and surely play an important role in the anti saccade task[ According to the model of saccade generation mentioned above\ a de_cit in the modulation function of selective attention on the _xation system "for example a de_cit in attentional processes of stimulus selection resulting in a de_cit of _xation disengagement# will result in an increased generation of late saccades and in irregular saccade triggering[ Attentional problems have already been discussed in dyslexia research ð28Ł[ Many studies suggest problems in the focusing of visual attention ð20\ 50Ł[ Some dyslexics seem to have di.culties in the foveal processing of words[ They have poor lateral masking and perform visual dis! crimination more e.ciently with the peripheral retina ð20Ł[ Accordingly\ dyslexics have problems in utilizing a peripheral or parafoveal cue to direct their attention across the visual _eld ð8Ł[ As pointed above\ the possibility that problems in directing attentional resources can a}ect saccadic behavior and generate the abnormalities observed in dyslexics should be taken into account for future work in this _eld[ Recently\ a correlation between poor _xation control

0088

and reading problems has been stated by Eden et al[ ð07Ł[ In particular\ they stressed instability in eye vergence and poor pursuit _xation and related their results to the _ndings of a de_cit in the magnocellular transient system in many dyslexics ð30\ 31Ł[ Along with the knowledge that the M!pathway projects up to the parietal cortex\ it has been speculated that a right parietal dysfunction could be responsible for the oculomotor as well as the visual abnormalities ð09Ł[ Eden et al[ also found a relationship between poor vergence control and lack of phonological awareness[ In the frame of the magnocellular theory\ the association of visual and phonological de_cits in dyslexic subjects has been explained with the postulated existence of a transient system also for rapid temporal processing of auditive stimuli ð00\ 62Ł[ Eden et al[ considered another type of linkage between eye movements abnormalities and a magnocellular de_! cit[ They claimed that saccadic intrusion and poor _x! ation control could be a consequence of the insu.cient inhibition of sustained activity from the transient system[ Children would generate irregular eye movements to increase activity in their transient system ð07Ł[ In the present study\ however\ this explanation could account for the increase of anticipatory but not of late saccades[ As in Eden et al[ we also found a signi_cant correlation between reading performance and oculomotor variables\ although we looked mainly at the SRT distributions of the subjects[ This could in any case be an indication that reading process and saccade system share common control mechanisms[ Attentional control mechanisms\ for example\ seem to play a central role in driving sac! cades during reading ð25\ 51Ł and reading quality is a}ec! ted by the landing position within the word ð38Ł[ It remains open\ however\ whether or not poor saccadic and _xation control could directly in~uence reading per! formance\ at least in some subjects[ A last important point is the observation that saccadic eye movement control rapidly develop from child to adult ð11Ł[ We found that a similar development "although probably slower for group D0 of the dyslexics# occurs in dyslexic subjects as an indication that saccadic eye movements are not de_nitively impaired but rather a}ec! ted from some kind of maturational lag ð3Ł[ In conclusion\ the present study con_rms that visual and visuo!motor problems strongly correlate with sub! types of speci_c reading disability[ Psychophysical tasks and proper methods of measuring saccadic eye move! ments in di}erent non!cognitive tasks can be helpful in understanding the multifactorial etiology of reading problems and in thinking about new methods of treat! ment[

Acknowled`ements*This research was supported by the Deutsche Forschungsgemeinschaft[ The critical comments of Prof[ Burkhart Fischer were very helpful[ We also thank Dipl[ Phys[ Klaus Hartnegg for his technical support and Christine Aumeier!Fritz and Kerstin Dor~inger for their support in the psychometric measuring[

0199

M[ Biscaldi et al[:Poor saccadic control correlates with dyslexia

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M[ Biscaldi et al[:Poor saccadic control correlates with dyslexia

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33[

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37[ 38[

49[ 40[

41[ 42[

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M[ Biscaldi et al[:Poor saccadic control correlates with dyslexia

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