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Evidence for impaired visuo-perceptual organization in developmental dyslexics and its relation to temporal processes

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An analysis of normal and dyslexic readers’ reaction-time (RT) performance in a standard visual-detection task (Experiment A) and in temporally-primed visual detection (Experiment B) reveals a tendency for significantly longer search and detection
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  COGNITIVE NEUROPSYCHOLOGY,2005,22 (5),499–522 E VIDENCE FOR IMPAIRED VISUOPERCEPTUALORGANISATION IN DEVELOPMENTAL DYSLEXICS AND ITS RELATION TO TEMPORAL PROCESSES Cordula Becker and Mark A.Elliott  University ofLeipzig and Ludwig-Maximilians-University,Munich,Germany  Thomas Lachmann University ofLeipzig,Germany and Brain Science Institute,RIKEN,Wako-shi,Japan An analysis of normal and dyslexic readers’reaction-time (RT) performance in a standard visual-detection task (Experiment A) and in temporally primed visual detection (Experiment B) reveals atendency for significantly longer search and detection RTs for dyslexic relative to the performance of normal readers.Consistent with previous studies,the RTs of normal readers and fast dyslexic respon-ders exhibited target-specific priming effects.In contrast,in addition to increased but statistically insignificant target priming,a set of slower dyslexic responders showed strong negative priming ontarget-absent trials.In spite of the longer detection latencies produced by these dyslexic participants,no evidence was found to suggest that negative priming occurred as a general function of increasingdifficulty in task performance (Experiment C).The enhanced positive and the negative primingeffects are both interpreted in the context of the possible deployment of attentional mechanisms tothe priming stimulus.The extent to which this strategy is characteristic of dyslexic performance as a whole may relate to the degree to which the dyslexic responder concerned experiences some generaltemporal processing impairment:Attentional deployment in this instance serving to compensate alack of the requisite temporal resolution required for coding the spatiotemporal structure of theprime. © 2005 Psychology Press Ltd 499 http://www.tandf.co.uk/journals/pp/02643294.htmlDOI:10.1080/02643290442000086Correspondence should be addressed to Mark A.Elliott,Ludwig-Maximilians-Universität München,Department Psychologie,Leopoldstr.13,D-80802 München/Munich,Germany (Email:elliott@psy.uni-muenchen.de). The authors would like to express their thanks to Ray Klein,David Plaut,and two anonymous reviewers for helpful suggestionsconcerning the research described in this manuscript.The authors are also indebted to Daniela Buschmann for her assistanceduring data collection.C.Becker was supported by Deutsche Forschungsgemeinschaft project grant EL 248/2.This study wassupported by project grant EL 248/1 to M.A.Elliott and grant No.22231608 from Barmer Ersatzkasse and the BeriSoftCooperation to T.Lachmann. INTRODUCTIONControversies on the aetiology of dyslexia  According to the International Classification of Diseases (World Health Organisation,1992),developmental dyslexia is defined as a specific dis-ability in learning to read and to spell despite atleast normal intelligence,adequate instruction,sociocultural opportunity,and the absence of sen-sory defects in vision and hearing.By this defini-tion,instead of aetiologically grounded criteria,the diagnosis of dyslexia rests upon a criterion of discrepancy between the reading performanceexpected from measures of general intelligence  and the observed reading performance,or in other words the discrepancy between how a child isexpected to learn to read and how,in fact,it does.However,the existence of partially contradictingexperimental work suggests that dyslexia may bebest considered a polyaetiological syndrome that isinfluenced by structural and functional character-istics of the central nervous system in interaction with exogenous factors.Reading is understood as a complex cognitivetechnique requiring the coordination of a series of subfunctions,including visual functions such asthe analyses of configural (feature) and ortho-graphic forms,as well as language-related func-tions,such as phonological,semantic,andsyntactic coding and decoding (e.g.,Friederici & Lachmann,2002).In this context,current modelsof dyslexia may be roughly divided into thoseassuming language-related deficits (which repre-sent the majority view;e.g.,Snowling,2000,2001;Vellutino,1987) and those assuming visual deficitsas an important determinant of reading disability (see,e.g.,Habib,2000).Visual impairments areoften (but controversially) related to the transient visual subsystem.Typically,it is assumed that the visual processing of normal and dyslexic individu-als undertakes a coarse decomposition of the visual scene into low and high spatial frequenciesthat are processed by independent channels,thesebeing the transient and sustained subsystems,respectively (Breitmeyer & Ganz,1976).Thetransient subsystem is believed to be most sensi-tive to low spatial and high temporal frequencies while the sustained visual subsystem is proposedto be most sensitive to high spatial and low tem-poral frequencies.Evidence of a functional deficitin transient subsystem activity is claimed fordyslexic readers on the basis of evidence indicat-ing that magnocellular layers of dyslexic brains aredisordered while the magnocells are significantly smaller in dyslexic readers than in normal readers(Livingstone,Rosen,Drislane,& Galaburda,1991).Psychophysical studies have also showndyslexic readers to demonstrate a general slowingof visual processing relative to normal readers:Related to the transient subsystem some studieshave shown longer visualpersistence to accompany  BECKER,ELLIOTT,LACHMANN 500 COGNITIVE NEUROPSYCHOLOGY,2005,22 (5) low spatial frequency stimuli (Lovegrove,Bowling,Badcock,& Blackwood,1980a;Lovegrove,Heddle,& Slaghuis,1980b;see also Slaghuis & Ryan,1999),while it has also been shown thatdyslexic readers experience slower flicker fusionrates (Martin & Lovegrove,1987).There is alsoevidence for overall slowed responding to config-ural visual information,which is independent of spatial frequency (Keen & Lovegrove,2000),although this finding has been considered in termsof a reduced capacity to process rapidly presentedstimuli and has thus been related to problems withsaccadic suppression,which,by extension,relatesto the transient subsystem (see,e.g.,Breitmeyer,1980).Evidence for a transient subsystem deficithas also been claimed from electroencephalo-graphic (EEG) data in which dyslexic readers’exhibit diminished visually evoked potentials tomotion signals (Livingstone et al.,1991).In addi-tion,functional magnetic resonance imaging(fMRI) studies have shown reduced activity inbrain areas receiving strong magnocellular inputsuch as areas of primary visual cortex (V1/V5) andthe secondary cortical visual area MT  (Demb,Boynton,& Heeger,1997,1998;Eden et al.,1996). The ascription of abnormal visual processing indyslexic readers to impaired transient subsystemfunction has been questioned (see,Johannes,Kussmaul,Munte,& Mangun,1996) and beensubject to counter-claims (see Greatrex & Drasdo,1995,for a general analysis of the issues).ThefMRI data recorded by Eden,Van Meter,Rumsey,Maisog,Woods,and Zeffiro (1996) has beenargued to lack control for responses to motionstimuli evoking a response in the sustained subsys-tem,for example colour-global dot motion.Therehave also been a number of failures to replicatesome psychophysical findings ascribed to impairedmagnocellular processing in dyslexia (see,e.g.,Hayduk,Bruck,& Cavanagh,1996;Hulme,1988;Skottun,2000),in particular,studies such as thatof Spinelli,Angelelli,De Luca,Di Pace,Judica,and Zoccolotti (1997),who investigated contrastsensitivity thresholds,found no evidence that theperformance of dyslexic participants could bespecifically ascribed to abnormalities in transient  subsystem function.Concerns of a methodologicalnature,such as those expressed by Chase and Stein(2003;see also Skottun,2000) refer to the validity of specific measures of contrast sensitivity ormotion perception as effective indicators of mag-nocellular function,suggesting that a transientsubsystem deficit may not emerge in all measuresof contrast sensitivity and may in fact be based onthe technical characteristics of the measures them-selves,where measurement noise obscures milddeficits. While weaknesses in the hypothesis of deficitsin the transient subsystem have lead to the pro-posal that dyslexic reading performance should beascribed to impairments in the functioning of thesustained processing channels (see Skottun,2000),there is also a more general view that dyslexicreaders experience a generalised difficulty in pro-cessing sensory information that is brief or thatchanges rapidly over time.Generalised is heretaken to indicate that dyslexia should be charac-terised in terms of a “temporal integration”deficitthat is not specific to a given visual processing sub-system and may be neither specific to the visual(DiLollo,Hanson,& McIntyre,1983;Talcott,Hansen,Assoku,& Stein,2000) nor the auditory domain (Kujala,2002;Tallal,1984),but which hasbeen argued to influence processing in bothdomains (Farmer & Klein,1995;Habib,2000;Klein,2002;Lachmann,2002;Stein & Walsh,1997;although see also Studdert-Kennedy & Mody,1995,for a critical review of the case forauditory deficits in dyslexia).Alternative proposalssuggest that visual impairments should be betterconsidered in terms of disturbed attentionalmechanisms (Hari & Renvall,2001;Stuart,McAnally,& Castles,2001). Particular temporal aspects of  visuoperceptual organisation If activation of the transient (magnocellular)system inhibits activation of the sustained (parvo-cellular) system (Breitmeyer,1980;also Burr,Morrone,& Ross,1994),simple logic would statethat this pattern of interaction occurs only undercircumstances when both transient and sustained VISUOPERCEPTUAL ORGANISATION IN DYSLEXIA COGNITIVE NEUROPSYCHOLOGY,2005,22 (5) 501 channels are concurrently engaged in stimulusprocessing,with the necessary implication thatactivity in each channel is functionally connectedand thus share some common mechanism of coactivation.Candidate mechanisms for linkingtransient and sustained channels are inhibitory interneuron networks:In early visual processing,inhibitory thalamic connections are known to beresponsible for the generation of oscillatory neu-ronal activity serving as a carrier for neuronal syn-chronisation.An emergent structure of oscillationscoupled with the cross-correlation (synchronisa-tion) of oscillatory neuronal activity has beenfound in the responses of cells engaged in pro-cessing the parallel trajectories of separate (andlinked) moving contours.This pattern of oscilla-tory synchronisation is interpreted in terms of thecoding of spatio-temporal relations between (i.e.,the common fate motion of) the moving stimuli,suggesting that oscillatory synchronisation is onemeans by which spatial and temporal informationcan combine to form a unitary perceptual experi-ence (see Singer,1999,for a recent review of theliterature on this topic).A relationship between inhibitory interneuronnetworks and the coding of stimulus synchrony has been suggested in an experiment conducted by Elliott,Becker,Boucart,and Müller (2000).Inthis task,observers were required to produce areaction-time (RT) response to the presence orabsence of a target grouping of four corner junctions (a Kanizsa-type square) presented in aregular 5  5 matrix of distracter junctions.Pre-sentation of this target matrix was preceded by thepresentation of a flickering premask matrix com-prising 25 crosses divided across four asynchro-nously presented image frames and organizedspatially in the same 5  5 arrangement as thetarget matrix.On 50% of trials,the premask matrix included an embedded target-prime,whichcomprised four simultaneously presented crosses(a synchronous premask),repeatedly shown below detection threshold at the location of the subse-quently presented target.This “synchronous”pre-mask condition contrasted with a random premask condition in which four crosses were presentedsimultaneously but in pseudorandomised spatial  BECKER,ELLIOTT,LACHMANN 502 COGNITIVE NEUROPSYCHOLOGY,2005,22 (5) configuration (i.e.,which did not correspond to asquare),while for both conditions,the remainingpremask matrix elements were pseudorandomly divided across the remaining three premask matrixframes (see Figure 1 and Methods and Elliott & Müller,1998,for further details of the paradigm).Elliott et al.(2000) discovered that responsesto target (but not nontarget) presentation weresignificantly expedited for healthy volunteers when targets followed synchronous-premask pre-sentation;these target “priming”effects weresubstantially amplified when experimental partici-pants had been administered Lorazepam,aGABA A ergic agonist known to influence the tem-poral response of interneuron networks.This find-ing was consistent with earlier findings thatsuggested priming to be sensitive to the precisetemporal characteristics of premask matrix presen-tation:Elliott and Müller (1998,2000) discoveredpriming effects to be specific to premask matricesthat flickered at 40Hz,which is in the range of those frequencies accompanying neuronal syn-chronisation. Investigation of a temporal processing deficit in dyslexic readers Based upon relations between the findings of Elliott and colleagues and those of physiologistsinterested in the temporal organisation of neu-ronal mechanisms engaged in visual processing, we considered the outcomes of synchrony primingas potentially revealing with respects to the regu-larity and temporal structure of synchronised neu-ral responses to visual stimulus presentation.Onthis basis,our specific aim was to further explorethe idea of visual temporal processing deficits indyslexic readers on the assumption that reading,asa task requiring the organisation of graphemicinformation,may be related to the temporalorganisation of visual-coding processes.We wereparticularly interested in the extent to which thecoding of stimulus synchrony and,with closeanalogy,neuronal synchronisation,may beimpaired in dyslexic relative to normal readersand,consequently,the extent to which evidenceexists to suggest that difficulties in the precisionof (neuronal) temporal organisation may be ageneral characteristic of dyslexia.Using both a standard target detection task (i.e.,a target detection task without priming,Experiment A) and target detection supported by the premask paradigm developed by Elliott andMüller (in Experiment B),we recorded responsetime and response accuracy during target detec-tion performance for both dyslexic and normalreaders.By employing the premask paradigm of Elliott and colleagues we investigated the extent to which the dyslexic and normal readers may be dif-ferentially susceptible to synchronous premask presentation.Given that successful primingappears to be highly dependent upon the precisefrequency of premask matrix presentation,we con-sidered that impaired magnocellular or transientsubsystem responses and/or a prolongation of  visual persistence might be responsible for reduc-ing the temporal fidelity of the neural response topremask matrix presentation.However,on the evi-dence of Elliott and Müller (2001),who discov-ered no reduction in priming as a consequence of the introduction of apparent-motion signals attarget matrix onset (these signals were induced by  varying the size of the target elements relative tothe size of the premask crosses),it seemed morelikely that variations in priming would relate to variations in the structure of prime persistence, which has been shown to match,with highfidelity,the 40-Hz structure of premask matrixpresentation (see Elliott & Müller,2000).On thisbasis,we expected priming effects to be reduced orabsent and an overall elevation in target and non-target detection RTs.Furthermore,if target search were influenced by prolonged and temporally ill-defined premask matrix persistence,a furtherexpectation was of slightly slower RTs to targetmatrices presented after premask matrix presenta-tion (Experiment B) relative to those presented inExperiment A.In the present experiments,premask crossesand target elements were presented in 5  5 ele-ment matrices and in two inducer specificationconditions.Variations in inducer specificationrefers to variations in the premask cross–cross ortarget junction–junction continuances,which were  VISUOPERCEPTUAL ORGANISATION IN DYSLEXIA COGNITIVE NEUROPSYCHOLOGY,2005,22 (5) 503 specified by two luminous contours covering inequal measures either 40% (2  20%) or 60%(2  30%) of the overall distance between the junction or cross vertices.On the basis of similarmanipulations made by Elliott and Müller (2001), variations in inducer specification were expectedto result in 60%-specified targets being faster todetect than targets specified to 40%,indicating variation in inducer specification to be analogous with variation in the “figural goodness”of the tar-get.Consequently,this variation was intended as ameans of examining whether or not target detec-tion was differentially influenced as a function of figural goodness for the dyslexic relative to normalreaders in Experiment A,while in Experiment B,the extent to which priming interacted with fig-ural goodness could be examined with a view toassessing the extent to which synchrony primingsupports figural processing if the speed of targetdetection is otherwise compromised relative to theperformance of normal readers. METHODSParticipants A total of 23 students,11 male dyslexic readersand 12 normal readers (11 male),participated inExperiments A and B.For Experiment C,11adult volunteers (4 male,mean age 25.73 years) were recruited from the undergraduate populationof the University of Leipzig.The groups inExperiments A and B (dyslexic–nondyslexic) were matched according to age and intelligence(see Table 1 for details).For each participant,thelevel of general intelligence was measured by means of the Raven Standard ProgressiveMatrices (Heller,Kratzmeier,& Lengfelder,1998) on the same day the experiment was per-formed.Each of the participants was found tohave at least normal intelligence;no significantdifferences in age or intelligence were foundbetween the groups. The dyslexic participants were recruited from aspecial school for language-disabled children inLeipzig (seven students) and from a vocationaleducation centre for language-disabled adoles-cents in Borna,Saxony (four students).The stu-dents comprising the control group were obtainedfrom a junior high school ( Realschule  ) in Leipzig.All participants had normal or corrected-to-normal vision.The regional supervisory schoolauthority as well as the students and their parentsgave their informed consent to the participation of the children in the present study.All studentsreceived € 10.00 and a reimbursement for trans-portation costs for their participation.The adult volunteers were paid at a standard rate of  € 8.00per hour. Diagnostics A diagnosis of dyslexia was given to all partici-pants of the dyslexia group according to the dis-crepancy definition of the diagnostic manualICD9/ICD10 (World Health Organisation,1992) by a team of professional examiners some5–12 years before the study.All dyslexic readersconformed to the definition of developmentaldyslexia as opposed to acquired dyslexia.Theexamination team consisted of one psychologist,two specialist teachers for dyslexic children,andone specialist teacher for language impaired chil-dren.As required by federal law,the diagnosis hadto be given during the second class of primary school using the test battery by Weigt (1980;seealso Kossakowski,1961) in order to send the chil-dren on a 2-year special training programme fordyslexic students during grade 3.The test battery included tests of reading and spelling for bothcontextualised and isolated letters and words,tests  Table 1. Comparison ofage and intelligence level betweennormal and dyslexic readers a  Normal readersDyslexic readers Mean(Min,max)Mean(Min,max)tp Age14.75(13,17)16.09(13,20)–2.058.052IQ97.17(80,127)91.82(74,106)1.070.297 a Homogeneity of variances assumed following a Levene-test.Intelligence level was measured with the Raven StandardProgressive Matrices.
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