Artigo Original
Juliana Casseb Oliveira1 Cristina Ferraz Borges Murphy1 Eliane Schochat1
Descritores
Dislexia Percepção auditiva Eletrofisiologia Leitura Testes auditivos
Keywords
Dyslexia Auditory perception Electrophysiology Reading Hearing tests
Correspondence address: Eliane Schochat
R. Cipotânea, 51, Cidade Universitária, São Paulo (SP), Brasil, CEP: 05360-000. E-mail: eschocha@usp.br
Received: 2/27/2012
Accepted: 8/14/2012
Study developed at the Department of Physical Therapy, Speech-Language Pathology and Audiology, and Occupational Therapy, School of Medicine, Universidade de São Paulo – USP – São Paulo (SP), Brazil. (1) Department of Physical Therapy, Speech-Language Pathology and Audiology, and Occupational Therapy, School of Medicine, Universidade de São Paulo – USP – São Paulo (SP), Brazil.
Conflict of interests: None
electrophysiological and behavior evaluation
Processamento auditivo (central) em crianças com dislexia:
avaliação comportamental e eletrofisiológica
ABSTRACT
Purpose: To compare the performances of children with dyslexia and a control group in behavioral tests of (Central) Auditory Processing and Long Latency Auditory Evoked Potentials (P300). Methods: Participants were 22 individuals with dyslexia (study group) and 16 individuals with typical development (control group). All individuals underwent behavioral and electrophysiological assessment of (Central) Auditory Processing (Frequency Pattern Test, Dichotic Digit Test, Speech-in-Noise Test, and P300). Results: Concerning the behavioral tests, there was difference between groups for the Frequency Pattern Test and for the left ear in the Dichotic Digit Test, with worse performance observed in the study group. Considering the P300, there was difference between groups regarding amplitude and latency absolute values, but this finding was not statisti-cally significant. Conclusion: The findings suggest that individuals with dyslexia present temporal auditory processing and figure-ground alterations, which was evidenced by behavioral auditory processing tests. There was no difference between the performance of both groups for the P300 test.
RESUMO
INTRODUCTION
Dyslexia may be defined as a specific learning disability that is neurological in origin characterized by a difficulty with accu-rate reading fluency and poor decoding and spelling, resulting from a deficit in the phonological component of language(1).
Theories based on anatomical, physiological and behavioral disorders try to explain the etiology of dyslexia, and two of them are more broadly discussed(2-4). The first and oldest one affirms
that difficulties are phonological in origin and comprise a purely linguistic deficit, that is, difficulties concern specifically one aspect of the language processing(2,3). The second one, which
will be studied in this research, concerns perceptual sensory disorders found in people with dyslexia. It is suggested that the phonological processing disorder derives from a temporal auditory processing(4). A disorder in this ability would affect
the perception of speech sounds and, consequently, the phono-logical awareness causing further reading problems(4).
Despite the several researches corroborating the tempo-ral processing theory(5-9), there are controversies about these
findings due to the difficulty in establishing a causal relation between the phonological processing and the auditory tem-poral processing(10,11), besides the great individual variation
in children’s performance for this kind of auditory test(4,12,13).
Furthermore, there is the difficulty to evidence these disorders only by behavioral tests(14).
The P300 is a Long Latency Auditory Evoked Potential (LLAEP) which reflects mainly the thalamus and the cortex ac-tivity; these structures involve sound discrimination, integration and attention. Therefore, it is used to detect neural disorders of the sequential processing of information, immediate memory and/or decision taking(15). According to literature, children with
reading disorder present poor performance in the behavioral assessment of (central) auditory processing (AP), longer reac-tion time, and increased latency for P300(16).
In Brazil, there are a few studies relating dyslexia, beha-vioral processing and electrophysiological tests. Thus, the aim of this study is to compare the performance of children with dyslexia (study group) and of children with typical develop-ment (control group) in auditory processing tests and P300. We hope that results will contribute to a better understanding of the etiology of dyslexia, aiming, consequently, at a better assessment and rehabilitation of this disorder.
METHODS
The present study was analyzed and approved by the Ethics Committee of the School of Medicine of Universidade de São Paulo (USP), under protocol number 853/08. Furthermore, all subjects’ parents/tutors signed the Informed Consent Term before the beginning of the assessments.
Thirty eight individuals, ranging in age from 9 to 12 years old, took part in this study. Among them, 22 (six female and 16 male) composed the study group, and 16 composed the control group (seven male and nine female). Both groups were paired regarding age, allowing a similar mean age between them (Table 1).
Inclusion criteria for the study group were: diagnosis of severe dyslexia concluded by the Brazilian Association of Dyslexia (ABD); absence of cognitive, psychological or neurological disorders; pure tone, speech audiometry and im-mittance measures within normal range; Brainstem Auditory Evoked Potentials (BAEP) within normal range; absence of ophthalmological disorders or, when present, corrected by correction lenses.
Control group was composed by children from local com-munity where the research was carried out. Children should present normal hearing thresholds, assured by the same proce-dures applied in the study group (hearing assessment and ABR), absence of reading complaints or learning difficulties verified by the patient’s background during family interview, absence of previous psychological or neurological disorder also verified by family interview. Individuals from both groups underwent a series of procedures in a two-day evaluation. In the first day, the clinical history of patients was taken, and a full audiological assessment was performed composed by meatus inspection, immittance measures, pure tone and speech audiometry, and ABR. Children who didn’t match the inclusion criteria were excluded and, when necessary, they were referred to a specia-list. In the second day, reading tests, behavioral assessment of auditory processing and P300 were performed, as follows.
Isolated words reading test/reduced version(17)
It is a test with 30 words varying in regularity (regular and irregular words), in lexicality (real and pseudo-words), in ex-tension (short and long stimuli), and in familiarity (frequent and not frequent words). Words and non-words were presented in cards. Participants were instructed to pronounce, in loud voice, all stimuli right after their appearance even not being sure of the answer, and even not knowing the meaning of the word, since many of them were non-words. Readings was recorded and transcribed, and the totality of mistakes computed in the end of the test. Each word read correctly corresponded to one score (total=30 scores).
Text reading test/adaptation(17)
Children were instructed to silently read the story “A Coisa”, with 211 words extension, and then answer the ques-tions about the text. Ten quesques-tions were asked by the examiner after the child’s reading in order to assess the memory for events and characters described in the story, and the inferential understanding. Each question answered correctly corresponded to one score that were summed up (total=10 scores).
Table 1. Characteristics of both groups regarding age and gender
Variables Study group Control group Age (mean±SD) 11.13±0.94 10.75±1.18 Gender (%)
Male Female
45.4 54.5
43.7 56.2
Behavioral assessment of (central) auditory processing
Three tests were used to assess the (central) auditory pro-cessing: Speech-in-noise, that analyzes the selective attention and auditory closure skills; Dichotic digit, that analyses figure--ground skills to verbal sounds and the binaural integration(18);
and the Auditec(19) Frequency pattern test – adult version (from
9 years old) – to assess the temporal processing skill.
P300
P300 was obtained using the Bio-logicâ NavegatorPro equipment. Parameters used were: monaural stimulus (tone burst with 20 ms plateau and 5 msrise/fall), frequent stimu-lus was presented at 500 Hz and the rare stimustimu-lus at 750 Hz, intensity of both stimuli was70 dBHL, analysis time was 800 ms, filter of 0.5 to 30 Hz, sensibility of 100 µV, stimulus rate was 1,1 stimulus/second. Test ended when 50 rare stimuli were presented, varying the amount of frequent stimuli from one test to another, and totalizing around 300 stimuli. The ratio was 80% frequent to 20% rare stimuli. Stimuli were presented randomly (oddball paradigm). Surface electrodes were placed in the forehead (Fpz=ground electrode), in the vertex (Cz= active electrode) and in the mastoids (A1= reference electrode of left ear; and A2= reference electrode of right ear). Before the placement of electrodes, skin was cleaned and scrubbed to reduce electrical impedance between skin and electrode to less than 5 ohms.
After the recording of frequent and rare stimuli tracings, one was subtracted from the other and P300 was marked in the final tracing; it is identified as a positive wave with a post-stimulus latency of about 300 ms. P300 latencies and amplitudes were analyzed. In the statistical analysis, the following tests were used: the Friedman and Mann-Whitney non-parametric test and the parametric t-Student test. The significance level was 5%.
RESULTS
Table 2 shows the comparison between the performances of both groups for the reading tests applied. There was a group effect, that is, a significant difference between the averages ob-tained in each group for both, the word reading test (p<0.001), and the reading comprehension test (p=0.024) with a worse performance observed in the study group in both tests.
Table 3 presents the performances of both groups in the three behavioral tests of (central) auditory processing. For the Frequency pattern test, a group effect was observed (p<0.001) with a worse performance presented by the study group. In the Speech-in-noise test, there was not a group effect for the ears tested (RE: p=0.335; LE: p=0.889). Nevertheless, there was an ear effect for the study group (p<0.001), with a worse performance observed in the RE. For the Dichotic digit test a group effect only for the left ear (RE: p=0.068; LE: p=0.002) was observed, with a worse performance presented by the study group, and the ear effect was not observed in each group (study group: p=0.139; control group: p=0.499).
Table 4 presents the comparison of both groups regarding
the values of P300. It can be observed that one subject from the study group presented absence of P300. It was considered the values of 500 ms for the latency and 0 µv for the amplitude of this subject. The value of 500 ms was adopted due to the maximum latency value found in previous studies with subjects of similar age(20-22).
Considering the latency, there was not a group effect for both ears (RE: p=0.440; LE: p=0.223), as well as there was not an ear effect in each group (study group: p=0.893; control group: p=0.697). Considering the amplitude, results were similar; there was no group effect for both ears (RE: p=0.399; LE: p=0.393), nor ear effect (study group: p=0.154; control group: p=0.255).
Table 2. Comparison of the performances between groups for reading tests
Reading test Study group (n=22)
Control group (n=16)
Text comprehension
Mean 6.73 8.88
SD 3.02 1.14
Group effect 0.024*
Word reading
Mean 24.45 29.13
SD 6.27 1.02
Group effect <0.001*
* Significant values (p≤0.05) – Student’s t test
Note: SD = standard deviation
Table 3. Comparison of groups’ performances in the behavioral as-sessment of AP
AP assessment Study group (n=22)
Control group (n=16)
Frequency pattern (%) RE/LE RE/LE
Mean 53.35 89.16
SD 18.35 5.579
Group effect <0.001*
Speech-in-noise (%) RE LE RE LE
Mean 81.82 86.91 84.5 86.5
SD 7.48 9.25 9.45 8.24
Ear effect <0.001 0.216 Group effect RE=0.335; LE=0.889
Digits (%) RE LE RE LE
Mean 94.57 92.41 97.69 97.19
SD 5.33 5.56 2.32 2.86
Ear effect 0.139 0.499
Group effect RE=0.068; LE=0.002*
* Significant values (p≤0.05) – Student’s t test
DISCUSSION
This research aimed to compare the performances of chil-dren with dyslexia with a control group in AP tests and P300. Previously to these tests, reading tests were applied in order to prove the difference in the performance of this ability in both groups. As shown in Table 2, both reading tests (of words and text comprehension) evidenced significant differences between the groups, with a worse performance observed in the study group. Therefore, these results confirm the presence (in the study group) of the main complaint observed in children with dyslexia, that is, reading skills difficulties(1-4). As demonstrated
by several studies(1-3), the probable cause for these difficulties
is related to the phonological processing. The great question still would be what is behind this phonological difficulty, which was investigated through the auditory tests.
The (central) AP was analyzed by the tests: Speech-in-noise, Dichotic digit and Frequency pattern (Table 3). Tests were cho-sen because of their easy application and because they assess different auditory skills without relying on reading skills. There was a group effect for the Frequency pattern test, with a worse performance observed in the study group, and for the left ear in the Dichotic digit test, also with a worse performance observed in the study group. In the Speech-in-noise-test, there was no difference between the groups; there was only an ear effect in the study group with a worse performance for the right ear. Maybe this result is related to the learning effect since the same list was used for both ears and the right was the first one tested. The poor performance of the study group for the temporal processing corroborates another research that also investigated the temporal processing in individuals with dyslexia compa-red to a control group of subjects with typical development(6).
Individuals were assessed through behavioral auditory proces-sing tests (gap-in-noise detection). The authors found signifi-cant differences for the assessment of temporal (central) AP between the groups, and a correlation between the test perfor-mance and words and non-words reading skills. Similar results
were also found in other two studies that investigated temporal AP in children with dyslexia and in a control group(4,23). The
studies concluded that a deficit in the AP for short sounds may affect the perception of speech sounds an lead to a phonological awareness deficit and further reading problems.
Another study showed significant correlations between the performance of temporal tasks and reading and writing skills(24).
The hypothesis considered by the authors is that such difficulty in the temporal processing in individuals with dyslexia may be specified by the lack of neural specialization of the auditory system for the processing of temporal clues. In the present study, we observed a coexistence of sound frequency resolution disorder and reading difficulty, since the statistical analysis of data was significant. We believe that the hypothesis of the previous study(24) may also justify the disorders of children with
dyslexia of the present study because of the low performance in reading tasks combined with the fact that all of them presented altered results in the Frequency pattern test.
Another issue observed in the Frequency pattern test was the high standard deviation of the study group (Table 3) when compared to the control group, evidencing that performances of children with dyslexia varied a lot in this test. This finding suggests the existence of different impairment levels of the auditory temporal processing and, maybe, of other factors not considered in this study, such as attention and memory.
A controversial matter about dyslexia is to define whether difficulties related to auditory processing are present generally, or specifically for the perception of temporal differences of speech sounds, that is, whether the difficulty is specific for rapid temporal changes or gather a broader range of AP(24). A
study compared groups of children with auditory processing disorder and children with dyslexia regarding the performance in tests of (central) AP(25). Individuals with dyslexia presented
altered results only for temporal test. Another study also found similar results; that is, worse performance when compared to the control group only for the temporal skill, and results within normal range for speech-in-noise and dichotic digit tests(12). In this study, the comparison between groups showed
altered results also in the Dichotic digit test (LE). These results corroborate other findings that verified worse performance of children with dyslexia in all tests of AP applied (Dichotic digit, Dichotic non-verbal and SSW)(26).
Besides behavioral tests, P300 was also performed. In this test, although not statistically significant, there was a difference between results of the study group and the control group for latency values, with higher values observed in the study group (Table 4). The same occurred for amplitude values. Despite the lower absolute values of amplitude presented by the study group when compared to the control group, these findings were not significant.
A study investigated P300 in 43 children with scholar failure and in 60 children without this background(27). Children with
scholar failure presented higher values of P300 latency, as well as in the present study.
Comparing the averages of each group in both researches, it is observed that in the other research the difference of perfor-mance between the groups was a lot higher; the mean latency
Table 4. Comparison of latency and amplitude of P300 between Study and Control groups
P300
Study group (n=22)
Control group (n=16)
RE LE RE LE
Latency
Mean 319.88 318.03 307.47 304.35 SD 52.91 28.19 41.01 39.93
Ear effect 0.893 0.697
Group effect RE=0.440; LE=0.223 Amplitude
Mean 3.66 4.97 4.66 6.17
SD 3.07 4.01 4.13 4.55
Ear effect 0.154 0.255
Group effect RE=0.399; LE=0.393
* Significant values (p≤0.05) – Student’s t test
of P300 for the control group was 332.25 ms and for the study group was 413.23 ms. In the present study, the averages for the study group were 319.88 ms for RE and 318.03 ms for LE; and in the control group they were 307.47 ms for RE and 304.35 ms for LE. Nevertheless, there is an important methodological difference between the studies. The present research had as study group only children with dyslexia, while the study men-tioned before had children with scholar failure, probably caused by several reasons, not only by reading and writing difficulty. Possibly, those children presented an important language delay, which could justify a greater delay of P300 latency compared to children with dyslexia of the present study.
Other studies were carried out with dyslexic university stu-dents and controls(28,29). The authors found longer reaction time
and higher latency values of P300 for dyslexic readers when compared to the control groups. These studies presented simi-lar findings to the present research, even with the discrepancy regarding the age of participants. However, the authors found statistical significance of responses, which did not occur in the present study. In this case, the absence of statistical significan-ce may have been caused by the redusignifican-ced number of subjects when compared to one of the two studies(28) that investigated 40
dyslexic and 40 controls, or by the discrepancy of the number of subjects between the study group and the control group, since the other study(29) investigated 16 dyslexic and 16
con-trols. Another fact that may have influenced such difference is that both comparative studies investigated the potentials with speech stimuli and the present research was performed with non-verbal stimuli.
In face of the results found and the comparison with lite-rature, it might be suggested that dyslexic children present a disorder in the temporal processing that may be related to a disorder in the phonological processing. Nevertheless, it cannot be assured that this difficulty is specific of the temporal proces-sing, since there were indicia of other skills impairment, such as figure-ground, evidenced by the Dichotic digit test results. The electrophysiological test (P300) was not capable of corroborate findings of temporal AP disorders observed in behavioral tests of the present research. Maybe, if verbal stimuli were used instead of the tone burst, the difference between the groups would have been significant. Furthermore, the number of subjects may also have influenced the obtaining of statistical significance for P300.
Thus, we suggest that further researches investigate the auditory processing of children with dyslexia through electro-physiological tests using speech stimuli. The hypothesis is that maybe this kind of stimulus may evidence more effectively the differences between the temporal auditory processing in the two groups studied.
CONCLUSION
Findings of this study suggest that children with dyslexia present auditory temporal processing and figure-ground dis-order, evidenced by behavioral tests of auditory processing. There was no significant difference between the performances of both groups for P300.
* JC was the author of the dissertation that generated the manuscript. She was responsible for data collection. CFBM contributed with conclusion of the findings and manuscript elaboration. ES contributed with the elaboration of the research project, and supervised the dissertation and manuscript elaboration.
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