Electrophysiological and behavioral evidence of auditory processing deficits in children with reading disorder

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Abstract

Objective

The aim of the research was to investigate auditory processing abilities in children with reading disorders using electrophysiological and behavioral tasks.

Methods

Differences in auditory processing between control, compensated (age appropriate reading skills with a history of reading disorder), and reading disordered groups were systematically investigated.

Results

The reading disorder group had significantly lower results than control and compensated reader groups for most tests in the reading and auditory processing test battery. All children with a reading disorder did not pass at least one behavioral test of auditory processing, and hence would be diagnosed clinically as having an auditory processing disorder (APD). The reading disorder group also had significantly smaller /ga/-evoked mismatch negativity (MMN) area than the control group. Compensated and control groups had similar results for the electrophysiological and behavioral auditory processing tests. Correlation analyses showed that reading fluency and accuracy and nonword scores (measured using Castle and Coltheart's word/nonword test) correlated significantly with most APD measures.

Conclusions

The general profile of auditory processing deficits in children with reading disorder was a combination of deficits on frequency patterns (i.e. frequency pattern test) and absent or small /ga/-evoked MMN. Significant results from the correlation analyses support the co-morbidity of reading and auditory processing disorders.

Significance

Children with reading disorders are likely to have auditory processing disorders.

Introduction

Auditory processing and reading disorders have been linked in a number of studies (Ahissar et al., 2000, Amitay et al., 2002, Walker et al., 2002). Some investigators claim a causal relationship between auditory processing disorders (APDs) and reading disorders (Farmer and Klein, 1993, Farmer and Klein, 1995; Nagarajan et al., 1999, Tallal, 1984, Tallal et al., 1993). Others support a speech-specific hypothesis that reading disorders result from problems in linguistic coding (Liberman, 1998, Studdert-Kennedy and Mody, 1995). Irrespective of the underlying cause, populations with reading disorders consistently display poor phonological awareness (Brady and Shankweiler, 1991, Bretherton and Holmes, 2003, Catts and Kamhi, 1999, Serniclaes et al., 2001). Phonological awareness refers to the ability to think about, talk about, and manipulate speech sounds in words (Catts and Kamhi, 1999). Several studies have reported poor auditory processing associated with reading disorders (see review by McArthur and Bishop, 2001), but the link between auditory processing, phonological awareness, and reading ability is still not well understood. The current study investigates the link between reading disorder, phonological awareness, and auditory processing.

In a recent study, King et al. (2003) investigated the performance of young adults with dyslexia on auditory processing tasks such as the frequency pattern test (FPT) and duration pattern test (DPT) and found that 5 of the 11 subjects failed both tests. In contrast, Walker et al. (2002) found no significant differences in FPT scores between adults with dyslexia and a control group. Other studies have used different behavioral tasks such as same–different tasks (Tallal, 1980), identification of rapidly presented high–low frequency tones (Farmer and Klein, 1993, Heath et al., 1999, Reed, 1989, Tallal, 1980), or gap detection (Farmer and Klein, 1993) to investigate auditory processing in children and adults with reading disorders. There is a lack of consistency in the tasks and outcomes of different studies. The current study thus included a variety of behavioral tasks used clinically to investigate the patterns of auditory processing deficits in children with reading disorder.

Studies investigating auditory evoked potentials in adults and children with learning or reading disorders have measured either obligatory cortical responses or the mismatch negativity (MMN). Mismatch negativity is a cortical response that occurs when there is a change in a repetitive sequence of auditory stimuli (Näätänen et al., 1978). Thus, MMN enables objective measurement of auditory discrimination ability even when the subjects are not motivated or actively attending to the stimuli (Näätänen, 1995, Tiitinen et al., 1994).

Studies have investigated MMN in children and adults with reading disorders using speech stimuli and simple or complex tones (Baldeweg et al., 1999; Schulte-Körne et al., 1998, Schulte-Körne et al., 1999a, Schulte-Körne et al., 1999b). There have been mixed results for tonal stimuli. Using simple tones, Schulte-Körne et al. (1999b) found no MMN differences between their reading disorder and control children, whereas Baldeweg et al. (1999) found poorer tone-evoked MMN in adults with dyslexia. Similarly, Kujala et al. (2003) found that adults with dyslexia had poorer MMN than control subjects for sequential tonal pairs. The present study investigated MMN using a wide range of stimuli (speech, chords and tones). The aim was to determine whether children with reading disorders show evidence of auditory processing deficits as measured using MMN for both speech and nonspeech stimuli. It was hypothesized that more complex stimuli (speech and chords) will result in poorer MMN in children with reading disorder compared to control children.

Impairments in the explicit discrimination and sequencing of speech sounds occur in populations with phonological awareness problems (Bradley and Bryant, 1983, Heilman et al., 1996). Adults with dyslexia display subtle problems discriminating speech sounds when tested under rigorous conditions (Cornelissen et al., 1996, Lieberman et al., 1985). Thus, one would expect that discrimination of sounds measured using MMN would be affected in adults and children with dyslexia and phonological awareness problems.

The obligatory cortical responses (P1–N1–P2) represent more elementary levels of sensory coding, but are more robust than MMN and easily identifiable (Stapells, 2002). The obligatory responses can be evoked by a range of speech and nonspeech stimuli. Cortical response peaks occur at about 60, 120, and 170 ms, respectively, in school-aged children (Kraus et al., 1993a). P1 is believed to be elicited from primary and/or secondary auditory cortex (Kushnerenko et al., 2002, Ponton et al., 2002, Pool et al., 1989). P2 emerges at about 8–10 years and shows significant variability in children below 15 years of age (Ponton et al., 2002, Purdy et al., 2002). School-aged children can show both an early and a late ‘N1’ (Sharma et al., 1997). In young children the morphology of the earlier (‘N160’) and later (‘N250’) negativity varies with interstimulus interval (ISI) (Ceponiene et al., 1998). N250 is generated in the region of Heschl's gyrus in the supratemporal plane (Takeshita et al., 2002). Short ISIs were used in the current study to shorten test time. At short ISIs of less than 1 s, children show P1 and N250 response most consistently to auditory stimulation (Ceponiene et al., 1998, Ponton et al., 2000, Takeshita et al., 2002). Thus, due to the short ISI used in the current study, obligatory responses recorded from the children primarily consisted of P1 and N250 peaks. The obligatory cortical responses are minimally affected by attention (Näätänen, 1992), do not depend on the subject responding to the stimulus, and are sensitive to auditory processing deficits in children (Purdy et al., 2002, Tonnquist-Uhlen, 1996). Therefore, P1 and/or N250 may be an effective measure for identifying APD in children with reading disorder.

Some children who are ‘at risk’ (e.g. due to family history or early speech and language problems) do not develop a reading disorder (Menyuk et al., 1991, Pennington and Lefly, 2001, Scarborough, 1990; Snowling et al., 2000, Snowling et al., 2003). Shaywitz et al., 1999, Shaywitz et al., 2003 followed a group of subjects who were diagnosed as poor readers when they were children through to adulthood. When tested as adolescents and adults, some of the subjects had ‘compensated’ (improved accuracy but not fluent) for their earlier reading difficulties. Functional magnetic resonance imaging (fMRI) showed differences in brain activation during reading tasks between poor and compensated readers when they were tested as adults, suggesting differences in underlying neural mechanisms for reading disorders that recover versus those that do not.

In the current study, children who were at least 2 years behind their age-peers in reading ability were compared to a ‘compensated’ group whose parents reported a previous history of reading difficulties but who reportedly had age-appropriate reading skills at the time of their participation in the study. Both reading disordered and ‘compensated’ groups were compared to a ‘control’ group of children with no previous reading or learning difficulties. It was hypothesized that these 3 groups would differ from each other on measures of auditory processing.

Thus, the overall aims of the current study were to

  • systematically investigate the differences between reading disorder, compensated readers and control groups using behavioral and electrophysiological measures of auditory processing, and

  • determine the presence of APD and the general profile of auditory processing deficits in children with reading disorder.

Section snippets

Subjects

Subjects were aged 8–12 years, had no history of hearing problems, and had normal peripheral hearing. Peripheral hearing was tested using pure-tone and immittance (tympanometry, ipsilateral and contralateral 1-kHz acoustic reflexes) audiometry, and transient click-evoked otoacoustic emissions (OAE). Pure-tone air-conduction thresholds were less than 20 dB HL at octave frequencies from 250 Hz to 8 kHz. All subjects had Type A tympanograms, acoustic reflex thresholds less than 110 dB HL, and OAE

Age and gender

There were no age differences between the 3 groups [F(2,56)=0.99, P<0.400]. The ratio between girls and boys for the CG (4 girls and 17 boys) and the RD groups (4 girls and 19 boys) was around 1:4 but the CR group was smaller with an approximate ratio of 1:3 for girls and boys (4 girls and 11 boys). A χ2 test showed no significant differences in the gender ratio between the 3 groups (P>0.05).

Reading and vocabulary tests

Means, standard deviations, and ranges of scores for the reading, and vocabulary tests are listed in

Reading and vocabulary

As expected, the children in the RD group had poor reading fluency and accuracy scores. Although their PPVT scores were within the normal range, children in the RD group had significantly poorer scores on this test than did the children in the CG and CR groups. The group differences in PPVT vocabulary scores paralleled the group differences in reading scores. A possible explanation for this could be what Stanovich (1986) referred to as the ‘Matthew Effect’ whereby ‘the rich get richer and the

Conclusions

All the children in the RD group showed evidence of auditory processing problems, based on either one or more behavioral tests, or their MMN results, or both. Thus, most children who participated in the current study who had a persistent reading disorder had a co-existing auditory processing disorder. Most children had difficulty with FPT task and the others showed different profiles of APD. Correlations between reading fluency and accuracy, nonword reading, and auditory processing measures

References (90)

  • A. Sharma et al.

    Developmental changes in P1 and N1 central auditory responses elicited by consonant–vowel syllables

    Electroencephalogr Clin Neurophysiol

    (1997)
  • S.E. Shaywitz et al.

    Neural systems for compensation and persistence: young adult outcome of childhood reading disability

    Biol Psychiatry

    (2003)
  • K. Takeshita et al.

    Maturational change of parallel auditory processing in school-aged children revealed by simultaneous recording of magnetic and electric cortical responses

    Clin Neurophysiol

    (2002)
  • P. Tallal

    Auditory temporal perception, phonics, and reading disabilities in children

    Brain Lang

    (1980)
  • M. Ahissar et al.

    Auditory processing parallels reading abilities in adults

    PNAS

    (2000)
  • C. Alain et al.

    Event-related brain activity associated with auditory pattern processing

    Neuroreport

    (1998)
  • T. Alpeter et al.

    A factor analytical investigation of the use of the PPVT-R as a measure of general achievement

    J Clin Psychol

    (1986)
  • S. Amitay et al.

    Auditory processing deficits in reading disabled adults

    J Assoc Res Otolaryngol

    (2002)
  • A. Andersen et al.

    Frequency discrimination and dyslexia. A pilot study

    Skolespsykologi

    (1987)
  • T. Baldeweg et al.

    Impaired auditory frequency discrimination in dyslexia detected with mismatch evoked potentials

    Ann Neurol

    (1999)
  • T.J. Bellis

    Assessment and management of central auditory processing disorders in educational settings: from science to practice

    (1996)
  • Bench RJ, Doyle JM. The BKB/A (Bamford-Kowal-Bench/Australian vesion) sentence lists for hearing-impaired children...
  • L. Bradley et al.

    Categorizing sounds and learning to read: a casual connection

    Nature

    (1983)
  • S. Brady et al.

    Phonological processes in literacy

    (1991)
  • H. Catts et al.

    Causes of reading difficulties

  • R. Ceponiene et al.

    Interstimulus interval and auditory event-related potentials in children: evidence for multiple generators

    Electro Clin Neurophysiol

    (1998)
  • R. Ceponiene et al.

    Sound complexity and ‘speechness’ effects on pre-attentive auditory discrimination in children

    Int J Psychophysiol

    (2002)
  • L. Cestnick et al.

    Auditory temporal processing and lexical/nonlexical reading in developmental dyslexics

    J Am Acad Audiol

    (2000)
  • S.D. Dalebout et al.

    Reliability of mismatch negativity in the responses of individual listeners

    J Am Acad Audiol

    (2001)
  • W. De Weirdt

    Speech perception and frequency discrimination in good and poor readers

    Appl Psychol

    (1988)
  • S. DeMartino et al.

    The ‘temporal processing deficit’: hypothesis in dyslexia: new experimental evidence

    Brain Cogn

    (2001)
  • Dunn LM, Dunn LM. Peabody picture vocabulary test, 3rd edition. Circle Pines, MN:AGS Publishing;...
  • V.T. Edwards et al.

    New norms for comparing children's lexical and nonlexical reading: a further look at subtyping dyslexia

    Aust J Psychol

    (1999)
  • M.E. Farmer et al.

    Auditory and visual temporal processing in dyslexic and normal readers

    Ann NY Acad Sci

    (1993)
  • M.E. Farmer et al.

    The evidence for a temporal processing deficit linked to dyslexic: a review

    Psychol Bull Rev

    (1995)
  • Gilmore A, Croft C, Reid R. Burt word reading test—New Zealand revision, Wellington, New Zealand;...
  • S.M. Heath et al.

    Auditory temporal processing in disabled readers with and without oral language delay

    J Child Psychol Psychiatry

    (1999)
  • E. Heiervang et al.

    Auditory processing in children with dyslexia

    J Child Psychol Psychiatry Allied Disciplines

    (2002)
  • K.M. Heilman et al.

    Developmental dyslexia: a motor-articulatory feedback hypothesis

    Ann Neurol

    (1996)
  • J. Jerger et al.

    Report of the consensus conference on the diagnosis of auditory processing disorders in school-aged children

    J Am Acad Audiol

    (2000)
  • G. Keidser et al.

    The National Acoustic Laboratories' (NAL) CDs of speech and noise for hearing aid evaluation: normative data and potential applications

    The Aust NZ J Audiol

    (2002)
  • R.W. Keith

    Random gap detection test

    (2000)
  • W.M. King et al.

    Comorbid auditory processing disorder in developmental dyslexia

    Ear Hear

    (2003)
  • N. Kraus et al.

    Mismatch negativity event-related potential elicited by speech stimuli

    Ear Hear

    (1992)
  • N. Kraus et al.

    Speech-evoked cortical potentials in children

    J Am Acad Audiol

    (1993)
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