Auditory Processing Deficits in Dyslexia:Task or Stimulus Related?Karen Banai1,3and Merav Ahissar21Department of Neurobiolo...
Waber and others 2000; Amitay, Ahissar, and Nelken 2002;Ramus and others 2003) and electrophysiological (Baldewegand other...
a larger initial frequency difference, 800 Hz. Participants respondedto the stimuli in each trial orally, by telling their...
vocabulary, and block design (Woerner and Overstreet 1999)did not significantly differ between D-LDs and control II.Process...
the D-LD participants in the Hi/Lo (left), but not in the S/D task(right), was significantly correlated with both their ver...
Taken together, these data show that D-LDs have difficultiesin tasks that require explicit retention and comparison of seri...
subjects were only asked to repeat a single bisyllabic pseudo-word. The minimal signal level needed to achieve 80% correct...
What could be the specific operations that are impairedamong D-LDs? Although our set of paradigms can refute thegeneral cog...
cortex. Thus, Nagarajan and others (1999) recorded deficits inauditory cortical responses to tones presented with briefinte...
reading disability: comparisons of discrepancy and low achievementdefinitions. J Educ Psychol 86:6--23.France SJ, Rosner BS...
Waber DP, Wolff PH, Forbes PW, Weiler MD. 2000. Rapid automatizednaming in children referred for evaluation of heterogeneo...
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Pac en dislexia

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Pac en dislexia

  1. 1. Auditory Processing Deficits in Dyslexia:Task or Stimulus Related?Karen Banai1,3and Merav Ahissar21Department of Neurobiology and 2Department of Psychologyand Interdisciplinary Center for Neural Computation, HebrewUniversity of Jerusalem, Jerusalem 91904, Israel 3Currentaddress: Department of Communication Sciences andDisorders, Northwestern University,Evanston, IL 60208, USAThe nature of the fundamental deficit underlying reading disability isthe subject of a long-standing debate. We previously found thatdyslexics with additional learning difficulties (D-LDs) performpoorly in simple auditory tasks. We now tried to determine whetherthese deficits relate to stimulus or task complexity. We found thatthe degree of impairment was dependent on task rather thanstimulus complexity. D-LDs could adequately detect and identifymild frequency changes in simple pure tones and minimal phonemicchanges in complex speech sounds when task required only simplesame--different discriminations. However, when task required theidentification of the direction of frequency change or the ordinalposition of a repeated tonal or speech stimulus, D-LDs’ performancesubstantially deteriorated. This behavioral pattern suggests thatD-LDs suffer from a similar type of deficits when processingspeech and nonspeech sounds. In both cases, the extent of diffi-culties is determined by the structure of the task rather than bystimulus composition or complexity.Keywords: auditory processing, dyslexia, frequency discrimination,perceptual memory, perceptual processing, working memoryIntroductionDyslexics are individuals with substantial and continuousreading difficulties in spite of adequate general intelligenceand education. They comprise ~10% of school children (Lyon1995; Shaywitz 1998; Snow and others 1998). Though a sub-population of dyslexics has particularly high general cognitiveabilities, enabling them to compensate for their poor reading,most dyslexics have additional learning difficulties (Fletcher andothers 1994).Most dyslexics, with and without additional learning difficul-ties, suffer from poor phonological processing (Snowling 2000).They have difficulties ‘‘hearing’’ words that are composed ofsmaller speech segments and in ‘‘manipulating’’ speech sounds.These impairments are directly linked to their reading difficultybecause decoding of the alphabetical script requires mappingvisual symbols to basic speech sounds (Snowling 2000).Another typical characteristic of dyslexia is poor verbalworking memory (Siegel and Ryan 1989; Swanson 1993; Vargoand others 1995). Working memory is the ability to retain a set ofstimuliwhileperformingadditional cognitive operationsonthem(Baddeley 1986). Basic tasks, like decoding unfamiliar words andsimple arithmetic calculations, require holding parts (speechsegments or digits) while manipulating other parts of the inputstream. Consequently, poor working memory may impede theperformance in a broad range of academic tasks including, butnot specific to, reading (Gathercole and Pickering 2000).A 3rd set of observations relates to dyslexics’ performance insimple psychoacoustic tasks. Many studies (e.g., Tallal 1980; seereview by Wright and others 2000) reported dyslexics’ poorperformance in such tasks, though both the prevalence and thefunctional role of these deficits have been heatedly debated(Rosen 1999).Recently, we found that poor psychoacoustic performance ischaracteristic of a specific, large, subpopulation of dyslexicswith additional learning difficulties (D-LDs). These individualsalso suffer from particularly poor verbal working memory,the extent of which is correlated with the degree of theirpsychoacoustic and reading deficits (Amitay, Ben-Yehudah,and others 2002; Banai and Ahissar 2004). Though D-LDsperform standard problem-solving tasks within the normalrange of the general population, they have severe difficultiesperforming tasks with heavy working memory load, and theyoften need special academic support to graduate high school(Banai and Ahissar 2004).The relationships between D-LDs’ phonological, psycho-acoustic, and working memory deficits are not clear. Becausehuman working memory has mostly been studied with phono-logical material, it is hard to decipher whether the difficulty inmanipulating speech sounds stems from poor processing ofsounds—that is, a stimulus-specific deficit—or from a generaldifficulty in interstimulus retention and manipulation—that is,a task-specific deficit. Similarly, because adequate performanceon any psychoacoustic discrimination task requires both en-coding of the specific stimuli to be discriminated and the dis-crimination process itself, that is, the need to serially retain andcompare stimuli, when discrimination is impaired, it is hard todissociate whether poor performance results from a stimulus-specific deficit (encoding auditory stimuli) or from a deficitrelated to the discrimination task at hand (retention, compar-ison, decision).In the current study, we asked whether D-LDs’ deficits arestimulus or task specific using both pure tones and complexspeech sounds. Specifically, we compared the predictions of2 types of hypotheses regarding the mechanisms underlyingD-LDs’ poor performance on auditory discrimination tasks.1. D-LDs have poor representations of auditory stimuli. Hence,they will have difficulties discriminating between similarauditory stimuli, regardless of task complexity. The extent oftheir difficulties will therefore increase with the subtlety ofthe required stimulus discrimination. This bottom-up hy-pothesis is parsimonious and consistent with many previousfindings, most notably by Tallal (1980) and the followingbehavioral (De Weirdt 1988; Reed 1989; Nicolson and others1995; Hari and Kiesila 1996; Kraus and others 1996;McAnally and Stein 1996; Adlard and Hazan 1998; Wittonand others 1998; Hari and others 1999; Heath and others1999; Talcott and others 1999; Ahissar and others 2000;Cerebral Cortex December 2006;16:1718--1728doi:10.1093/cercor/bhj107Advance Access publication January 11, 2006Ó The Author 2006. Published by Oxford University Press. All rights reserved.For permissions, please e-mail: journals.permissions@oxfordjournals.orgbyguestonJune29,2011cercor.oxfordjournals.orgDownloadedfrom
  2. 2. Waber and others 2000; Amitay, Ahissar, and Nelken 2002;Ramus and others 2003) and electrophysiological (Baldewegand others 1999; Nagarajan and others 1999; Ahissar andothers 2001; Kujala and others 2003; Maurer and others2003; Renvall and Hari 2003) studies. It predicts that D-LDs’performance will be poor when confronted with a percep-tual challenge, that is, when either high-resolution auditorydiscriminations or complex auditory processing are required,regardless of the behavioral task used.2. D-LDs’ ability to perform auditory discriminations is limitedby task requirements (i.e., protocol of stimulus presentationand required manipulations). Thus, the same type of stimuli(speech or nonspeech) will induce more severe difficultieswhen task complexity is increased (i.e., by increasingmemory load). Although quite a few previous studies as-sessed psychoacoustic abilities in related populations, theytypically used a single behavioral paradigm (e.g., Ahissar andothers 2000; Amitay, Ahissar, and Nelken 2002; Ramus andothers 2003) and hence could not dissociate whether dif-ficulties related to basic stimulus processing or to the re-quired manipulations (though see France and others 2002).To compare the predictions of these 2 hypotheses, we used 3frequency discrimination tasks, using the same stimuli withdifferent degrees of task complexity, and 2 speech perceptiontasks, again using the same speech tokens with 2 differentprocedures.Materials and MethodsParticipantsThe study was conducted in 2 test populations. The 1st was composedof 57 8th grade students (all female, aged 14.2 ± 0.4) from 2 classes, 32from a regular public school, and 25 from a private school for studentswith mild learning disabilities (LDs). The control (regular) school waschosen based on the similar demographic characteristics of the studentsin the 2 schools. Two paradigms of frequency discrimination as well asreading, memory, and cognitive measures were administered to thispopulation. Five students had to be removed from data analysis after allassessments were completed: One from the LD class had generally poorcognitive abilities, as measured by standard tests. For 1 control par-ticipant, we could not measure a reliable threshold for any of the psy-chophysical tasks, and we thus removed her data from furtheranalysis as well. Two other students in the control class were found tobe reading disabled, and their data were therefore also removed. Data ofanother student from the control class were removed because ofa hearing impairment. We thus report the results of 24 students fromthe special school and 28 normal learning control students.The 2nd population comprised 35 7th grade students (all female, aged13.1 ± 0.4) from the same school for mildly learning-impaired individ-uals, who participated in this study as a part of a larger research programin which they took part. Data of 1 student suspected of a hearing losswere removed from the analysis, and thus, data of 34 7th grade studentsare reported.The parents of all participating students gave their consent afterreceiving letters with information regarding the study. All participantscompleted all tasks, unless otherwise noted in the text.Group ClassificationNone of the students from the regular school had a history of learningproblems, and they were thus defined as a normal-learning controlgroup (control I). Students from the LD school all had a history of LD,reading related or otherwise. For the purpose of the current study, theywere divided to 2 groups: one with dyslexia (D-LD) and the other withnormal reading and phonological abilities, which served as a same-classroom control group (control II). Classification was based on 2measures that should be impaired among dyslexics based on currentdefinitions stressing the significance of phonological deficits to thediagnosis of dyslexia (Lyon 1995; Snowling 2000): reading of pseu-dowords and phonological awareness (see task descriptions sub-sequently). Based on these 2 measures, we calculated a combinedphonological score with respect to normal-learning controls (control Iaverage without the 2 individuals with reading disability). LDs whosephonological score was lower than the controls’ average by 1.5 standarddeviation or more were defined as dyslexics (n = 15 in the 8th grade and22 in the 7th grade). The rest, whose phonological abilities were withinthe range of the controls, were defined as same-classroom controls(control II; n = 9 in the 8th grade and 12 in the 7th grade).Cognitive PerformanceUnlike discrepancy-based definitions of dyslexia, current diagnosticcriteria, which were used in this study (Siegel 1992; Waber and others2000), do not require a discrepancy between reading abilities andintelligence quotient (IQ) scores but rather within the normal IQ ( >80).Although we could not conduct a full IQ test during the study, allstudents in the special school were administered a detailed psycho-educational assessment before being admitted to the school to ensurethat they have the potential to graduate with a full high school diplomaby the end of the 12th grade. This testing rules out the possibility ofIQ < 80 among the students (except for 1 student, whose data wereexcluded, as explained earlier). In addition, the Raven standard pro-gressive matrices scores (Raven and others 2000) of all these studentswere >35, which excludes the lower 25% of the population.MaterialsPsychophysical TasksAll stimuli were presented to both ears through Sennheiser HD-265linear headphones and a TDT system III signal generator (Tucker DavisTechnologies, Alachua, FL) controlled by a PC in a quiet room in eachschool.Auditory frequency discrimination. Participants made frequencydiscriminations in 3 conditions. The frequency of the test (higher)tone was always changed in a 2 down/1 up staircase procedure (stepsize was 40 Hz for the first 5 reversals and 5 Hz thereafter) converging ata performance level of 70.7% (Levitt 1971). The frequency of thereference tone was fixed, 1000 Hz. A pleasant visual feedback wasprovided for correct responses.1. High--low discrimination (Hi/Lo): Two 50-ms tones with 1000-msinterstimulus interval (ISI) were presented in each trial. Thestudents had to indicate which tone was higher (1st or 2nd).Assessment terminated after 50 trials or 10 reversals. Thresholdswere measured twice in the 8th grade, at the beginning and at theend of the 1st session, and the average just noticeable difference(JND) was used in the statistical analysis. Due to the high correlationbetween the two, only 1 assessment was conducted in the 7th grade.2. Same--different discrimination (2-tone S/D): Two 50-ms tones (with1000-ms ISI) were presented in each trial. The listener had toindicate whether they were same or different. Same and differenttrials had an equal probability of appearance. Assessment terminatedafter 100 trials or 10 reversals (based only on trials with differentstimuli). Threshold was measured once in the 2nd testing session.3. Same--different discrimination with 3 tones (3-tone S/D): a fixedreference tone was followed by a 1500-ms silent interval and then by2 other tones (with 950-ms interval between them), one of whichwas a repetition of the reference and the other was different.Participants had to indicate which tone (2nd or 3rd) was the same asthe reference.Participants were given a practice block of 15 trials (with a frequencydifference of 1000 Hz between the tones) to familiarize them with thetask prior to assessment. Initial frequency difference in the test blockswas 500 Hz. If they had 2 errors or more, they were given anotherpractice block. If they still had 2 errors or more, testing begun but withCerebral Cortex December 2006, V 16 N 12 1719byguestonJune29,2011cercor.oxfordjournals.orgDownloadedfrom
  3. 3. a larger initial frequency difference, 800 Hz. Participants respondedto the stimuli in each trial orally, by telling their answer to theexperimenter who immediately entered it to the computer to continuethe procedure. This mode of response was chosen to minimize errorsdue to sensory-motor confusions. This interactive mode further ensuredthat all participants were maximally alert throughout the assessmentprocedure. However, because it introduced an intervening oral re-sponses (within the sequence of pure tones) and somewhat prolongedthe assessment process, it may have elevated the estimated discrimina-tion thresholds.Calculation of frequency discrimination thresholds. Frequency JNDs,that is, the minimal frequency difference reliably discriminated, wereused as indices of discrimination. For each participant, JNDs were cal-culated based on the average of her last 5 reversals. Hi/Lo JNDs wereobtained for 54 8th grade and all 7th grade students (an equipmentfailure occurred during the assessment of one of the LD students). Twocontrol students failed to achieve a reliable JND in the 1st assessment(they had no reversals in the last 20 trials), and we thus used only their2nd thresholds. Given the high correlation between the 2 Hi/Lomeasurements (r = 0.79, P < 0.001), we used the average JND for therest of the students in the 8th grade. S/D JNDs were obtained for 51 8thgrade (28 Controls I, 8 Controls II, and 15 D-LDs) and all 7th gradeparticipants.Auditory duration discrimination. Seventh grade participants heard 2tones and had to indicate which one was longer, the 1st or the 2nd.Fixed reference duration was 100 ms in 1 condition and 400 ms in theother. Step sizes were 40, 25, and 5 ms in the 100-ms condition and 40,25, and 5 ms in the 400-ms condition. Step size changed after 3 reversals.All other aspects of the task were identical to the Hi/Lo frequencydiscrimination task.Speech discrimination and identification. Eighth grade participantswere required to discriminate minimal phonemic pairs. The stimuliwere pairs of 2-syllable pseudowords differing in 1 consonant andidentical otherwise. The following consonant pairs were used: /d/-/t/,/b/-/d/, /b/-/p/, /v/-/f/, /m/-/n/, and /s/-/z/, appearing either at thebeginning or at the end of the word. Between trials, 4 different syllableswere used (/a/, /e/, /i/, and /u/). All stimuli were produced by a nativefemale Hebrew speaker. Twenty-four different pairs were used.The task had 2 conditions with 48 trials in each. 1) Two-word S/Dcondition in which the 24 different pairs were supplemented with 24same pairs. 2) Three-word S/D condition in which the participant firstheard a pair of pseudowords. After a 2-s interval, one of the pseudo-words was repeated, and the task was to indicate which word itwas—the 1st or the 2nd. Each pair was repeated twice, each time witha different repeated word.Speech perception in noise. Minimal intensity level for accurate speechperception in noisy background (narrow-band amplitude--modulatednoise) was tested using the same set of 2-syllable pseudowords de-scribed earlier, normalized for intensity and duration. Total noise RMSwas 83-dB SPL (for fuller description, see Putter-Katz and others 2005).On each trial, a single pseudoword was played and participants wereasked to accurately repeat it. The intensity of the pseudowords wasadapted in a 3 down/1 up staircase procedure (converging on ~80%correct) while noise level remained fixed. The assessment terminatedafter 85 trials or 15 reversals. Identification threshold was the arithmeticmean of the last 10 reversals. This assessment was conducted in the7th grade.ReadingOral reading of pointed Hebrew words and pointed nonwords wasassessed using a list of 24 pseudowords followed by a list of 24 words(see Ben-Yehudah and others 2001). The pseudowords were designedto mimic the real Hebrew words in the word list. These reading tests,designed by A. Deutsch (for details, see Deutsch and Bentin 1996), werepreviously found to be reliable indicators of reading difficulties. Subjectshad to read aloud, as accurate and as fast as possible from the printedlists presented to them. Both accuracy and speed were recorded.Phonological AwarenessPhonological awareness was assessed using the Hebrew version of thespoonerism task (developed by Peleg and Ben Dror, unpublished testmaterials), consisting of phoneme deletion and replacement. Listenerswere orally presented with a word pair and were asked to swap the 1stphonemes of the 2 words (e.g., white pig / pite wig). In the process ofintroducing the task, all participants successfully performed its simplesubsteps (phoneme deletion/replacement). Twenty word pairs werepresented.Memory TestsVerbal memory was assessed using Digit Span, a subtest of Wechslerintelligence scale for children (WISC–R95 Wechsler 1998). This testcontains 2 parts. In the 1st part, participants are asked to repeat a list oforally presented digits in the order they were presented. The maximallength of successfully reproduced sequences characterizes the capacityor span of verbal memory. In the 2nd part, subjects are asked to repeatthe sequence of digits in the reverse order. The 2nd part is morecomplex and measures the combined effect of capacity and manipula-tion in verbal working memory. This test was scored using the Wechslerscaled score.A Hebrew version of the ‘‘sentence span’’ task adapted by Ben Drorand Shani (1998) from the reading span task originally developed byDaneman and Carpenter (1980) was used to assess retention of wordsthrough interfering stimuli and task switching. Seventh grade partic-ipants were asked to listen to a series of orally presented short sentenceswith a missing last word, complete the last word of each sentence, andrecall all the last words in the order of completion at the end of theseries. Series length increases from 2 to 6 sentences. Scoring emphasizesboth the number and the order of correctly recalled words.Nonverbal Cognitive AbilitiesBlock design (WISC-R95, Israeli version) was used as a measure ofgeneral cognitive abilities. Administration and scoring followed thestandard procedure described in the Administration and Scoring manualof the test.ResultsPopulation ProfileTable 1 shows the average scores of the 3 groups of 8th gradeparticipants: control I, control II, and D-LDs in reading andreading-related tests and in standard cognitive tasks. Table 2shows reading, reading-related, and standard cognitive scores ofthe 7th grade participants. As expected, D-LDs’ performancewas particularly impaired in the reading and phonological taskscompared with both control groups.General Cognitive AbilitiesThe 2 control groups did not differ significantly on any of thereading or cognitive measures administered. Thus, nondyslexicLDs (control II) are similar to normal-learning students ingeneral cognitive abilities and yet form a more adequate controlgroup to D-LDs in terms of having the same educationalbackground and school experience. D-LDs scored lower thancontrol I on block design, a standard measure of generalcognitive ability. However, their scores were not significantlylower than those of control II (for 8th graders: t = 1.2, P > 0.22,not corrected, to allow minimum chance of retaining the nullhypothesis that the groups do not differ cognitive tasks; for the7th grade, see Table 2), whose scores were intermediate.Moreover, D-LDs’ scores on this task were well within thenormal range. Table 2 further shows that scores in the 2 tasksthat often serve as a short version for measuring general IQ,1720 Auditory Deficits in Dyslexia: Task or Stimulus dBanai and AhissarbyguestonJune29,2011cercor.oxfordjournals.orgDownloadedfrom
  4. 4. vocabulary, and block design (Woerner and Overstreet 1999)did not significantly differ between D-LDs and control II.Processing Nonspeech StimuliFrequency DiscriminationFigure 1 shows average discrimination thresholds (JNDs) of the3 subject groups on the S/D and the Hi/Lo (1st and 2ndassessments) frequency discrimination tasks. A clear differencein thresholds is evident. The Hi/Lo task yielded higher JNDsthan the S/D task (Ftask = 19.2, P < 0.001). However, thisdifference was the result of D-LDs having huge difficulties withthe Hi/Lo task (in both assessments) compared with the 2 othergroups. The 2 control groups, on the other hand, did not differfrom each other. The average of the 2 measurements was 22 ±18%, 16 ± 10%, and 52 ± 28% in the control I, control II, andD-LD groups, respectively, with significant group (F = 9.7,P < 0.001) and interaction (F = 6.9, P = 0.002) effects; the 2post hoc comparisons between D-LDs and the other groupswere significant at P < 0.005, whereas those between the 2control groups were not significant. Percent success aroundthese thresholds did not differ significantly between the 3groups (81 ± 10%, 83 ± 6%, and 74 ± 17% in the control, LD, andD-LD groups, respectively; F = 1.7, P > 0.18), indicating thatgroup differences do not stem from measuring different levelsof performance accuracy.On the other hand, on the S/D task, neither performance level(F = 0.38, P = 0.687) nor performance accuracy (average percentcorrect was 84 ±6, 84 ±4 and 82 ±6 for Controls I, Controls II andD-LDs, respectively) significantly differed between the 3 groups.Comparing performance in these 2 frequency discriminationtasks on a subject by subject basis, we found no correlationbetween thresholds (r = 0.09, P > 0.5 in the entire 8th gradegroup), indicating that different bottlenecks may limit perfor-mance in these 2 tasks. Figure 2 illustrates that performance ofTable 2Group means (SD) in reading-related and standard tasks: 7th gradeControl II (n 5 12) D-LD (n 5 22) taPReading AccuracybNonwords 91.3 (7) 57.6 (14) 7.6 0.001Words 97.2 (3) 86.2 (7) 5.1 0.001Reading speedcNonwords 48 (11) 35 (12) 3.2 0.003Words 100 (29) 74 (26) 2.6 0.013PhonologySpoonerismb83 (16) 52 (23) 3.7 0.001Standard scoresdBlock design 11.1 (2) 9.5 (3) 1.7 0.092Digit span 10.2 (2) 7.7 (2) 3.8 0.001Vocabulary 7.6 (2) 7.3 (2) 0.5 0.633Sentence spane32 (5) 31 (4) 0.59 0.562at and P based on t-test between D-LDs and LDs.bPercent correct.cWords/min.dWechsler scaled scores.eScore.Hi/Lo1 Hi/Lo2 2-tone S/D010203040506070JND(%)Figure 1. Frequency discrimination—Hi/Lo versus S/D. Frequency JNDs of D-LD(filled bars), control II (empty bars with thick lines), and control I (empty bars with thinlines) participants on the Hi/Lo (2 left sets of bars) and S/D (right bar set) tasks. Hi/Lo1and Hi/Lo2 denote the 1st and 2nd assessments of this condition, respectively. Asexplained in the text, average of the 2 measurements was used for statistical analysis.Data are from 8th grade participants. Error bars denote ± 1 standard error of the mean.0 25 50 75 1000 25 50 75 1000481204812VerbalSpan0 25 50 75 10002550751000255075100Hi/Lo JND (%)PhonAwareness(%corr)0 25 50 75 100S/D JND (%)Figure 2. Frequency discrimination versus verbal memory and phonologicalawareness among D-LDs. Hi/Lo JNDs (average of the 2 assessments, left panels)are significantly correlated with both verbal memory (measured with digit span) andphonological awareness (measured with spoonerism) scores; 2-tone S/D JNDs (rightpanels) are not. Data are shown from the 8th grade.Table 1Group means (SD) in reading-related and standard tasks: 8th gradeControl I(n 5 28)Control II(n 5 9)D-LD(n 5 15)FaPReading accuracybNonwords 89.5 (10)*** 84.7 (11)*** 52.8 (15) 48.6 0.001Words 98.1 (3)*** 97.7 (4)*** 83.6 (11) 27.7 0.001Reading SpeedcNonwords 51 (14) 47 (12)* 38 (16) 4.1 0.02Words 90 (27) 96 (28) 78 (25) 1.6 0.22PhonologySpoonerismb88 (11)*** 85 (19)*** 50 (30) 18.7 0.001Standard scoresdBlock design 11.7 (2)** 10.7 (3) 8.8 (3) 6.3 0.004Digit span 10.2 (3)** 10.3 (2)* 7.7 (2) 8.1 0.001aF and P are the results of a 1-way analysis of variance between the 3 groups.bPercent correct.cWords/min.dWechsler scaled scores.*P 0.05, **P 0.01, ***P 0.001 on a post hoc test between D-LDs and each ofthe other groups.Cerebral Cortex December 2006, V 16 N 12 1721byguestonJune29,2011cercor.oxfordjournals.orgDownloadedfrom
  5. 5. the D-LD participants in the Hi/Lo (left), but not in the S/D task(right), was significantly correlated with both their verbalmemory (i.e., digit span: r = 0.68, P = 0.005) and phonologicalawareness scores (i.e., spoonerism: r = 0.82, P < 0.001), 2measures known to be causally linked with reading skills. Asimilar correlation pattern was observed among LDs (notshown), though it was only marginally significant due to thesmaller size of this group (r = 0.72 and 0.55, P = 0.04 and 0.15,respectively, for digit span and spoonerism). Note that S/D JNDsare not correlated with these measures even though they arequite scattered (the range of S/D JNDs among controls is0.5--40%, i.e., there is no floor effect).Duration DiscriminationA plausible explanation for D-LDs’ difficulties in the Hi/Lo taskrelates to the explicit analogy between pitch and height, whichis required by this task (participants were asked ‘‘which tonewas higher?’’) and could be particularly difficult for D-LDs. Inthat case, their impaired performance may stem from thespecific requirement embedded in frequency discriminationsrather than from the general requirement of stimulus evalua-tion. To assess whether this is indeed the case, we designedanother task, using the same behavioral paradigm as in theHi/Lo discrimination task; however, comparisons referred to anorthogonal dimension—stimulus duration. Stimulus durationdiscrimination may be a more attention-demanding task interms of requiring continuous monitoring throughout stimuluspresentation and, thus, perhaps requires more complex neuralcircuitry (Leon and Shadlen 2003). Yet, duration discrimination(which tone is longer?) is an intuitive and straightforwardevaluation, which was immediately understood by all partic-ipants, and was not susceptible to an interpretation that D-LDsmight not have fully understood the task.We administered the 2 duration discrimination conditions tothe 7th grade test group (who showed the same behavioral pat-tern on the Hi/Lo task as shown below). As shown in Figure 3,D-LDs (n = 19), who had difficulties in performing Hi/Lofrequency discrimination, had similar difficulties in performinglong/short duration discriminations around both durations,compared with the control II group (n = 9), with no difficultiesin Hi/Lo discriminations (t = 2.9, P = 0.007 for 400-ms reference;t = 2.5, P = 0.016 for the 100-ms reference). Performanceaccuracy did not differ between the groups in either condition(percent correct in the control II and D-LD groups were 76 ± 4%and 75 ± 4% with 100-ms reference and 73 ± 4% and 73 ± 6%with the 400-ms reference, respectively), indicating that differ-ences in thresholds did not stem from measuring different levelsof performance accuracy.Taken together, we have shown that the difficulties of ourdyslexic participants are not specific to the compared di-mension. When subjects had to estimate the direction ofchange, whether higher or longer, D-LDs had difficulties.Order JudgmentsParticipants could adequately perform the S/D task by identi-fying repetition of the stimulus without having to associatestimulus position (1st or 2nd) with the stimulus type (higher orlower). Though this task clearly requires some form of memorytrace, such a trace may be implicit and result from stimulus-specific adaptation mechanisms. These mechanisms yieldsmaller responses to previously presented stimuli and therebya greater response to novel stimuli, regardless of ‘‘how’’ they arenovel. These perceptual mechanisms thus signal novelty but arenot sufficient for determining its nature as required in the Hi/Lotask. An example for such a mechanism at the level of theauditory cortex is the mismatch negativity (MMN) response,which signals change in a repetitive sequence of auditorystimuli (see, e.g., Naatanen and others 2001).Under S/D conditions, D-LDs had no difficulties, whereas inthe Hi/Lo task, they had substantial difficulties. The differencebetween these tasks may thus stem from the Hi/Lo task beinggenerally more taxing for explicit memory mechanisms orperhaps from its more specific requirement to assess the natureof the difference between the stimuli. To resolve this question,we administered an extended S/D task, using 3 stimuli. In thistask, a repetition always occurs, and the listener needs toidentify the ordinal position of the repeated stimulus. Moreover,it requires retention through interfering stimuli and often forlonger durations (though duration per se is probably notovertaxing for D-LDs, Ben-Yehudah and others 2004). Thus,from a general working memory perspective, it is a taxing task,yet no parametric evaluations are required. Therefore, if D-LDs’difficulties stem from the requirement for parametric stimulusevaluations of the Hi/Lo task, then they are not expected tohave difficulties with this task, even though it is demandingfrom a working memory perspective.We administered all 3 frequency discrimination tasks to the7th grade group described earlier. In therepeated tasks (Figure 4,2 left bars), we replicated our findings (illustrated in Fig. 1) thatD-LDs were impaired in Hi/Lo (their average was 37 ± 26%compared with 10 ± 11% in the control II group; t = 4.8,P < 0.001) but not in S/D frequency discrimination (10 ± 10%vs. 8 ± 7%, respectively; t = 1, P > 0.3). In the novel 3-tone S/Dtask, D-LDs were significantly poorer than LDs (19 ± 15% vs.8 ± 10%, respectively; t = 3.1, P = 0.004; Fig. 4, rightmost bars),indicating that even S/D comparisons are difficult for themwhen accurate retention and comparison of previous stimuli isrequired through subsequent intervening stimuli.100 ms 400 ms020406080100Reference DurationJND(%)Figure 3. Duration discrimination. Average duration JNDs of D-LDs (filled bars) andcontrols II (open bars) with 100-ms (left) and 400-ms (right) reference tones (data arefrom the 7th grade).1722 Auditory Deficits in Dyslexia: Task or Stimulus dBanai and AhissarbyguestonJune29,2011cercor.oxfordjournals.orgDownloadedfrom
  6. 6. Taken together, these data show that D-LDs have difficultiesin tasks that require explicit retention and comparison of seriesof simple tones.Processing Speech ElementsComparing Speech SoundsWe now asked whether a similar pattern of difficulties wouldcharacterize D-LDs’ performance in analogous tasks that usecomplex speech sounds rather than simple tones as test stimuli.Two conditions of a speech discrimination task (describedearlier) were administered to the 8th grade D-LD and control IIparticipants: simple 2-stimuli S/D task (15 D-LDs and 9 controlsII completed this condition) and 3-stimuli order judgmentS/D condition (14 D-LDs and 7 controls II completed thistask), similar to the 3-tone S/D frequency discrimination task.Figure 5A shows average scores in these 2 tasks, illustrating thatD-LDs were significantly poorer than their peers in discrimi-nating phonological components when the task requiredjudging the ordinal position of the pseudowords but not inthe simple 2-stimuli S/D condition (Ftask = 9.6, P = 0.006; Fgroup =5.2, P = 0.05; the interaction term approached significanceFinteraction = 3.5, P = 0.078).Similar to the findings with pure tones, the degree of deficit inprocessing complex speech sounds was thus also dependent onthe task: Impairment was revealed only when a 3rd stimulus wasintroduced. Furthermore, as shown in Figure 6, D-LDs’ perfor-mance in the 3-pseudoword speech task, but not in the 2-pseudoword task (not shown), was highly correlated with theirHi/Lo frequency JNDs (r = 0.72, P = 0.003). These findingssuggest that the nature of D-LDs’ deficits may be similar forcomplex speech components and simple pure tones.Speech Perception In NoiseOur findings that S/D comparisons of speech components werenot difficult for D-LD individuals suggest that they do not havesevere difficulties in speech perception. Yet, given that thesestimuli were not very difficult (natural speech presented ata comfortable rate in quiet) and most subjects got most pairsright, more subtle speech perception deficits may have beenoverlooked due to a ceiling effect. In order to ensure that it wasnot the relative simplicity of the stimuli we used, we adminis-tered an adaptive test of speech perception in noise (with thesame pseudowords used for the discrimination tasks but withsuperimposed noise). In this task (originally described byPutter-Katz and others 2005), the stimuli were very complex,but the memory and cognitive loads were very low becauseHi/Lo 2-tone S/D 3-tone S/D01020304050JND(%)Figure 4. Frequency discrimination (7th grade). From left—Hi/Lo, 2-tone S/D, and3-tone S/D frequency JNDs of D-LDs (filled bars) and controls II (open bars).3-word SD 2-word SD707580859095100%correctspeech in noise10203040506070Identificationthreshold(dB-SPL)A BFigure 5. (A) Comparison of speech elements. Average performance of D-LDs (filledbars) and controls II (open bars) on a 3-pseudoword S/D task (left) and on a2-pseudoword S/D task (right). A significant intergroup difference is found only for the3-element tasks. Data are from 8th grade participants. (B) Speech perception innoise. Minimal intensity levels of D-LDs and LDs for speech perception in noise. Dataare from 7th grade participants.0 25 50 75 100708090100Hi/Lo JND (%)3-wordS/D(%corr)Figure 6. Verbal versus nonverbal performance of D-LDs. JNDs in the Hi/Lo frequencytask and scores (percent correct) in the 3-pseudoword S/D task are highly correlated(data are from the 8th grade students).Cerebral Cortex December 2006, V 16 N 12 1723byguestonJune29,2011cercor.oxfordjournals.orgDownloadedfrom
  7. 7. subjects were only asked to repeat a single bisyllabic pseudo-word. The minimal signal level needed to achieve 80% correctrepetition does not significantly differ between control II and D-LDs (t = 1.7, P > 0.10), as shown in Figure 5B. The finding thatincreasing signal complexity does not increase D-LD’s difficul-ties indicates that basic perceptual mechanisms underlyingimmediate auditory perception are adequate in these individu-als. Moreover, speech identification thresholds were not corre-lated with Hi/Lo JNDs among either D-LDs or control II (r = 0.03and 0.14, respectively, P > 0.59), suggesting that differentmechanisms affect performance in these 2 tasks.Do D-LDs Suffer from a Generalized Cognitive Deficit?Because it was not possible to fully match D-LDs and the othergroups on measures of cognitive ability, it may be claimed thatD-LDs’ deficits in performing complex discriminations (Hi/Lo,short/long, and 3-stimuli S/D comparisons) arise simply becausethese tasks have a generally greater cognitive load than thosethey performed adequately (2-stimuli S/D, a single pseudowordrepetition). Thus, their deficit may reflect a general cognitivedeficit rather than a task-specific one and is therefore notsurprising. For several reasons addressed subsequently, wewould like to suggest that this is not the case.First, where the group differences on Hi/Lo frequencydiscrimination related to group differences in IQ, we wouldexpect a correlation between block design and Hi/Lo frequencyJNDs. This was not the case. No significant correlations be-tween block design and Hi/Lo frequency discrimination wereobserved in either group (r = 0.2, 0.002, and 0.1 for control I[n = 29], control II [n = 19], and D-LDs [n = 37], respectively,P > 0.29; data pooled from 7th and 8th grades). Furthermore,repeating the statistical analysis of the Hi/Lo and S/D frequencydiscrimination tasks with block design scores as a covariate didnot change any of our findings, as expected from the lack ofcorrelation between block design and frequency discrimina-tion: Main effects for group (F = 9.5, P < 0.001), task (Hi/Lo vs. S/D: F = 5.33, P = 0.02), and a significant task 3 group interaction(F = 3.88, P = 0.028) were observed, whereas the block design 3task interaction (F = 1.43, P > 0.25) was not significant,suggesting that the findings cannot be fully attributed to IQscores.Second, as shown in Table 2, D-LDs could perform complexcognitive tasks like sentence span adequately. We chose thistask because it is cognitively demanding in similar ways to ourprevious tasks, that is, it requires information retention throughinterfering stimuli, and taxes attention and memory in terms ofdouble load of sentence completion as well as retention. Yet, itdoes not require stimulus manipulation, and retention can beenhanced using the semantic content of the words andsentences.Taken together, we conclude that D-LDs’ unique pattern ofdeficits in handling auditory stimuli is not a consequence ofa general factor limiting their performance in all cognitivelydemanding tasks (for further discussion, see Banai and Ahissar2004, 2005).DiscussionSummary of ResultsIn this study, we found that D-LDs’ performance was adequatein tasks that require identification or simple S/D discriminationof either pure tones or complex speech sounds. On the otherhand, given exactly the same physical stimuli, D-LDs hadsubstantial difficulties in tasks that required either parametriccomparisons (Hi/Lo and long/short) or judging the ordinalposition of the repeated stimulus (whether a tone or a pseu-doword). Moreover, high correlations were found between thedegree of difficulty in performance of complex tasks usingsimple tones and speech components. These findings suggestthat the mechanisms underlying D-LDs’ impaired ability toperform these demanding tasks are common to the 2 types ofstimuli. This common impairment is not in reasoning or generalcognitive abilities, as indicated by adequate performance ona cognitively demanding, yet largely semantic based, task. Wethus propose that D-LDs’ deficits involve mechanisms ofoperating on perceptual aspects of recently processed stimuli,broadly termed working memory mechanisms.Sex Differences in DyslexiaAll our participants were females because our study wasconducted in an all-female school. Thus, although our resultsare ‘‘clean’’ in the sense that we report within-gender perfor-mance and variability (see Liederman and others 2005), wecannot directly generalize our findings to the male population.The issue of prevalence of perceptual impairments among maleversus female dyslexics had not been systematically studied.Moreover, its assessment would be complex because it shouldalso address related issues of reasoning abilities, languageimpairments, and attentional deficits. At present, even therelative prevalence of dyslexia among males and females is stilldisputed (Shaywitz and others 1990; Share and Silva 2003).An informal examination of our own accumulated data (~200dyslexic and ~200 control participants) suggests no consistentgender-related perceptual differences.The Underlying Auditory Deficit of D-LD Individuals:Accuracy of Representation or Stimulus Manipulation?What is it that differentiates the tasks that posed particulardifficulties to D-LDs from those that did not? Tasks that posea great challenge for D-LDs could, in principle, be tasks thatrequire more refined auditory representations. Alternatively,they might be generally more demanding tasks, requiring betterreasoning or decision-making abilities. Third, these tasks maypound on specific stimulus operations that are selectivelyimpaired among D-LDs. We argue for the 3rd alternative, eventhough the range of tasks that we applied is not sufficient foraccurate characterization of these operations.The 1st interpretation can be refuted because increasingstimulus complexity and hence processing requirements tospeech stimuli (with and without noise) did not specificallyhamper D-LDs’ performance. The ‘‘difficulty’’ interpretation canbe refuted for the following 3 reasons. First, levels of difficulty,as measured by performance accuracy, were equated acrosstasks and conditions by applying an adaptive procedure thatconverged to the same relative level of performance. Second, asshown in Figures 1 and 4, in both control groups, thresholds didnot differ between the Hi/Lo and the same--different conditions.These tasks were just not more difficult for them. Third,difficulty per se was not a sufficient impediment to D-LDs, asshown by their adequate performance of the cognitivelydemanding task of sentence span.1724 Auditory Deficits in Dyslexia: Task or Stimulus dBanai and AhissarbyguestonJune29,2011cercor.oxfordjournals.orgDownloadedfrom
  8. 8. What could be the specific operations that are impairedamong D-LDs? Although our set of paradigms can refute thegeneral cognitive or the perceptual difficulty hypotheses, theyleave many alternatives unresolved. One is that some aspects ofworking memory mechanisms are impaired among D-LDsbecause the tasks that were specifically impaired among D-LDs put a heavier load on working memory. Our previousstudies refuted a retention deficit, that is, faster decay ofmemory trace interpretation, because manipulating ISIs didnot affect D-LDs’ deficits (Ben-Yehudah and others 2004). Yet,whether it is the buildup of stimulus-specific memory traces orthe operation of stimulus comparison that is impaired is beyondthe scope of this study. Both may be more taxing in the tasksthat posed greater difficulties to D-LDs.Our finding that the behavioral paradigm used for assessmentis crucial to the degree of deficits revealed by dyslexics isconsistent with reports of previous studies both in the auditory(e.g., Heath and others 1999; France and others 2002) and in thevisual domain (Ben-Yehudah and others 2001). However, moststudies applied only a single behavioral paradigm for evaluatingthresholds, and thus, the substantial interstudy variability wasmainly interpreted in terms of different population samplesrather than different behavioral tasks (see Discussion in Banaiand Ahissar 2004). An important lesson from our study is thatin order to decipher whether it is the task or stimuli thattaxes individuals, one needs to assess performance using atleast 2 behavioral tasks that greatly differ in their workingmemory load.Task-Specific Difficulties and Theories of DyslexiaAccording to the dominant ‘‘core phonological deficit hypoth-esis’’ of dyslexia (Snowling 2000; Vellutino and others 2004),reading disability is a result of a specific deficit in phonologicalprocessing. By this account, phonological deficits contributeto the reading deficits, whereas deficits in the processing ofnonverbal stimuli stem from a separate source and are irrelevantto reading. Data from the current study does not providesupport for a speech-specific deficit. Rather, our findings,coupled with recent findings from imaging studies (LoCastoand others 2004; Burton and others 2005; Luo and others 2005),suggest that processing of both speech and nonspeech stimulishares at least some common processing that is impaired amongD-LDs. Thus, although deficits in nonverbal auditory processingmay not be directly relevant to reading, it is part of the sameunderlying deficit contributing to the phonological processingdeficit and consequently poor reading.The current finding that the degree of discrimination deficitamong D-LDs is task dependent and that D-LDs do not havedifficulties detecting speech in noise suggests that their auditoryprocessing is not impaired under all circumstances. However,whether we define the deficits we found as ‘‘perceptual’’ (Tallaland others 1993) or ‘‘postperceptual’’ depends on our terminol-ogy of perception. We believe that the ‘‘auditory experience’’(i.e., what one perceives) is different for D-LDs under someconditions, depending on stimulus protocol and behavioral task.Thus, an integrative view of perception as a dynamic, large-scaleprocess, which underlies this experience (Hochstein andAhissar 2002), attributes these deficits to perceptual processes.This means that somewhere in the circuitry underlying ourimmediate explicit perception, D-LDs’ processing is impaired.However, the cortical circuitry underlying these processes isbroad and includes, among others, frontal areas, which are majorcontributors to the retention and comparison aspects requiredfor adequate performance in most tasks.Relation to Previous Imaging and ElectrophysiologicalStudiesBased on the strong dependence of D-LDs’ manifested deficitson stimulus protocol and on task demands, we suggest that theirfundamental deficit does not reside in auditory cortex. Thissuggestion is based on both lesion and imaging results. Neuro-psychological studies suggest that a pervasive lesion of theprimary auditory cortex impairs S/D discriminations for bothsimple tones and speech sounds (Tramo and others 2002), incontrast to our findings in D-LDs. Recent findings from imagingstudies have shown that activation patterns in auditory cortexwere more related to the nature of the stimulus, whereaspatterns of activity in frontal area were more related to taskdemands (Luo and others 2005). In frontal areas, task character-istics, for example, same--different versus rhyming rather thanthe stimulus processed (words vs. pseudowords or tones,LoCasto and others 2004; Burton and others 2005), were foundto affect activation patterns. Burton and others (2005) sug-gested that the task-related differences in activation are relatedto differences in working memory load.The behavioral impairments we measured are thus consistentwith each of the following 2 interpretations.1. D-LDs’ deficits may be related to impaired transfer ofinformation between posterior, modality-specific storesand the frontal areas carrying out specific working memoryoperations (for review, see Curtis and D’Esposito 2003).Such interpretation is consistent with the suggestion thatdyslexia is a ‘‘disconnection syndrome’’ in which communi-cation is impaired between different cortical regions(Paulesu and others 1996). In particular, Klingberg andothers (2000) have shown an abnormality of white mattertracks in temporoparietal regions in dyslexics, which maycarry information from temporal to frontal regions.2. Deficits may stem from impaired function of frontal areas.Thus, information is properly transferred but is not properlyoperated upon. Studies of executive functions in dyslexiareported that subgroups of the dyslexic population areimpaired in tasks considered as reliable correlates of pre-frontal function, such as the Wisconsin Card Sorting Test(Helland and Asbjornsen 2000; Brosnan and others 2002).Functional imaging studies also report abnormal patterns ofactivation in prefrontal areas of dyslexic subjects (Backesand others 2002; Shaywitz and others 2003). Furthermore,the most notable change in activation pattern following aneffective auditory behavioral training (which improvedreading ability) was observed in prefrontal areas (Templeand others 2003). The typical interpretation of thesefindings is that dyslexics fail to utilize brain areas that arenormally involved in language processing. Language andworking memory are, however, hard to disentangle whenusing verbal tasks. Although the amount of improvement inlanguage abilities in the study of Temple and others (2003)was correlated with the magnitude of increase in activationin the temporoparietal cortex, it could be that both are anoutcome of the prefrontal change.The above ‘‘higher level’’ interpretations seem at odds withpreviously reported findings of impaired activity of the auditoryCerebral Cortex December 2006, V 16 N 12 1725byguestonJune29,2011cercor.oxfordjournals.orgDownloadedfrom
  9. 9. cortex. Thus, Nagarajan and others (1999) recorded deficits inauditory cortical responses to tones presented with briefintervals. Moreover, abnormal MMN responses to frequency orphonemic oddballs were found among dyslexics (Kraus andothers 1996; Baldeweg and others 1999; Kujala and others 2003;Maurer and others 2003; Renvall and Hari 2003; Lachmann andothers 2005). This apparent discrepancy probably results fromthe following 2 reasons. First, the MMN response has multiplegenerators, including frontal ones (e.g., Rinne and others 2000).Impairment in the frontal generators seems to underlie thedeficits revealed in some of these studies, which reported anabnormality in the later portion of the MMN response amongchildren at risk of dyslexia (e.g., Maurer and others 2003).Second, other groups of dyslexics, who were not sampled in thecurrent study (which was focused on D-LDs), may havea different, possibly ‘‘lower level’’ source of impairment. Pre-liminary evidence that this may be the case was recentlyreported by Banai and others (2005). They found that a sub-group with a presumably early source of deficit (impairedbrainstem responses) had impaired MMNs. Interestingly, theoverall LD profile of this group was much milder (e.g., havingmuch better verbal memory) than that of D-LDs.Analogies to Animal StudiesConsistent with the suggestion of a frontal source of impair-ment, the pattern of D-LDs’ deficits with simple psychoacoustictasks resembles findings of studies characterizing dorsolateralprefrontal cortex (DLPFC) functions in monkeys. These studiesreport a similar dissociation between unimpaired perceptualabilities and particularly poor working memory skills. Thus,monkeys with bilateral lesions to DLPFC are impaired in a 3-item task that requires them to remember which items they hadalready chosen compared with monkeys with bilateral percep-tual IT lesions (Petrides 2000). In this task, the same 3 elementswere presented in each of the 3 trial stages, though not in thesame positions. Monkeys had to touch only an item that they didnot choose in a previous stage of the trial. When reduced to a 2-item task, which could be performed as a sequential S/D task,monkeys with bilateral DLPFC lesion could reasonably performthe task. We interpret this ability as reflecting a change-detection strategy, which, unlike interstimulus comparisons,can be subserved by low-level sensory circuitry (of inferotem-poral (IT) cortex in this case). Interestingly, retention per seseems to depend on the functioning of IT while comparisonswere contingent upon intact prefrontal cortex.Parametric stimulus comparisons probably also involve pre-frontal functions (Romo and Salinas 2003). Thus, neurons inprefrontal cortex have been found active during the delayperiod of a tactile frequency discrimination task similar to theHi/Lo task we used (Romo and others 1999; Romo and Salinas2003), where this activity retained parameters of the 1ststimulus. Though involvement of prefrontal cortex in auditoryworking memory was not intensively studied, imaging studies inhumans (Belin and others 1998; Zatorre and others 1999) andphysiological (Romanski and Goldman-Rakic 2002) and anatom-ical (Kaas and others 1999; Poremba and others 2003) findingsfrom nonhuman primates show that the prefrontal cortex is partof the cortical network dedicated to the analysis of sound.Taken together, these analogies suggest that the pattern of D-LDs’ behavioral deficits is consistent with a mild dorsolateralprefrontal deficit.NotesWe thank Ehud Ahissar, Shabtai Barash, Eli Nelken, Udi Zohary, andRanulfo Romo for helpful comments on the manuscript. 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