Clinical neurophysiology of visual and auditory processing in dyslexia: A review

Abstract

Neurophysiological studies on children and adults with dyslexia provide a deeper understanding of how visual and auditory processing in dyslexia might relate to reading deficits. The goal of this review is to provide an overview of research findings in the last two decades on motion related and contrast sensitivity visual evoked potentials and on auditory event related potentials to basic tone and speech sound processing in dyslexia. These results are particularly relevant for three important theories about causality in dyslexia: the magnocellular deficit hypothesis, the temporal processing deficit hypothesis and the phonological deficit hypothesis. Support for magnocellular deficits in dyslexia are primarily provided from evidence for altered visual evoked potentials to rapidly moving stimuli presented at low contrasts. Consistently ERP findings revealed altered neurophysiological processes in individuals with dyslexia to speech stimuli, but evidence for deficits processing certain general acoustic information relevant for speech perception, such as frequency changes and temporal patterns, are also apparent.

Introduction

Dyslexia is a specific developmental disorder in learning to read, which is not the direct result of impairments in general intelligence, gross neurological deficits, uncorrected visual or auditory problems, emotional disturbances or inadequate schooling. (International Classification of Diseases, ICD-10, 2009; Dilling et al., 1991; DSM IV-TR American Psychiatric Association, 2000). Dyslexia accompanies the individual throughout their lifespan and interferes with academic achievement or activities of daily living that require reading skills (Shaywitz et al., 1999). It occurs in all known languages (Lindgren et al., 1985, McBride-Chang et al., 2008) and is one of the most common developmental disorders affecting around 5% of school-aged children (Shaywitz et al., 1990, Katusic et al., 2001). Socioeconomic status and family factors are known to influence the development of reading abilities, but are not causally related to dyslexia (Stevenson and Fredman, 1990, Vellutino et al., 2004).

Since the first description of dyslexic cases a familial aggregation was observed (Morgan, 1896). Family and twin studies clearly point to a genetic basis of this complex disorder and first candidate genes have been found (Smith et al., 1983, Taipale et al., 2003; for reviews see Paracchini et al., 2007, Schumacher et al., 2007). A key function of these genes is their involvement in neuronal migration and axon growth. Imaging studies have clearly demonstrated an altered cortical network in dyslexic subjects that comprises left and right superior temporal cortices, left inferior temporal-occipital cortices and both left and right inferior frontal and posterior temporo-parietal cortices (for review see Schlaggar and McCandliss, 2007).

A number of electrophysiological studies have provided evidence for basic perceptual deficits in dyslexia. Abnormal event-related potentials (ERPs; amplitude, latency, topography) for auditory processing of non-speech and speech sounds were found in dyslexic children and adults. Analogously, altered visual evoked potentials (VEPs) were reported in dyslexic subjects when non-linguistic stimuli were presented.

We conducted a PubMed search spanning two decades of research using dyslexia and reading disorder as keywords in combination with event related potentials, ERPs, VEPs, motion onset, contrast sensitivity and mismatch negativity and found 74 papers reporting on electrophysiological correlates of dyslexia (studies with unclear group selection criteria or reporting magnetoencephalography (MEG) data were excluded). Forty articles primarily concerned visual processing of non-linguistic material (e.g. graphical material that varied on spatial frequency, contrast and temporal frequency) and linguistic material (e.g. letters, words, lexical, syntactic and semantic aspects of word comprehension). Auditory perception of non-linguistic material (e.g. sinus tones), speech sounds (e.g. speech contrasts like /da/ vs. /ga/) and phonological processing (e.g. rhyme judgements) were reported in 34 articles. For both auditory and visual perception approximately half of the articles investigated ERP correlates elicited by non-speech and non-linguistic stimuli. The goal of this review is to summarize and integrate investigations conducted on the neurophysiological correlates of basic perceptual visual ERPs to motion and contrast sensitivity, as well as auditory ERPs to tones and speech sounds, in dyslexia over the last 20 years. Because the definition of reading disorders can be quite broad, we attempted to only include those studies which explicitly recruited their participants according to below average reading (and in some cases spelling). In exceptional cases (e.g. Kraus et al., 1996) we included studies with less strict definitions of dyslexia, as we considered them to be very important for the review. In these cases, the discrepancy has been pointed out.

Visual and auditory perception deficits in dyslexia have been reported since the beginning of dyslexia research (Hinshelwood, 1895, Morgan, 1896, Borel-Maisonny, 1951). Since then, it has been repeatedly shown that phonological processing is one of the most relevant factors for learning to read and spell and is impaired in dyslexic children, adults and in compensated adults (for reviews see Rack, 1994, Snowling, 2000, Ramus et al., 2003).

Based on observations of aphasic children in the 1970’s (Tallal and Piercy, 1973a) a temporal processing theory was formulated in order to explain perceptual deficits that could account for the phonological processing deficits observed in dyslexia (Tallal, 1980a, Tallal, 2004). Since then numerous studies were conducted to explore the basic auditory deficits in dyslexia by investigating the ability to discriminate non-speech stimuli (Farmer and Klein, 1995, McArthur and Bishop, 2001). The temporal processing theory was extended to the perception of non-linguistic visual stimuli (Stein, 2001). For both areas, neurophysiological studies have made major contributions to the understanding of the neurobiological correlates of dyslexia.

For this review we chose to focus on these two research lines, visual and auditory processing of non-linguistic and sub-lexical stimuli, in dyslexia. The first reason for this selection is that more than 36 empirical papers have been published on these topics. Secondly, several common remediation programs, at least in Europe, are based on the assumption of basic visual or auditory perception deficits in dyslexia. These are often time consuming interventions, for both therapists and clients. If the empirical basis for such interventions is low, the use of these interventions in therapeutic settings should be critically discussed. Thirdly, there continues to be an urgent need to improve the understanding of the aetiology of dyslexia despite more than 100 years of research. Although a phonological deficit is often found in dyslexic individuals (between 30% and 60% depending on the study), its aetiology remains, for the most part poorly understood.

We begin with a summary of the ERP studies on visual processing of non-linguistic stimuli followed by a discussion on the literature covering the basic auditory processing of non-linguistic stimuli. The auditory processing review culminates with speech (sub-lexical) perception and includes studies on early predictors. We have decided to integrate speech perception, which focuses on examining discrimination abilities between consonant–vowel (CV) stimuli and cortical auditory evoked potentials to CV stimuli, because there is accumulating evidence that speech perception is one of the best predictors of reading disability (Guttorm et al., 2005, Lyytinen et al., 2005a, Lyytinen et al., 2005b). Furthermore, the first patho-physiological pathway model, from gene function to speech perception in dyslexia, has recently been described (Roeske et al., 2009). This finding renders ERP correlates of speech promising candidates for understanding the aetiology of dyslexia.