theories

http://brain.oxfordjournals.org/content/126/4/841.full

Introduction

Developmental dyslexia is traditionally defined as a discrepancy between reading ability and intelligence in children receiving adequate reading tuition. Since the definition is entirely behavioural, it leaves open the causes for reading failure. It is now well established that dyslexia is a neurological disorder with a genetic origin, which is currently being investigated. The disorder has lifelong persistence, reading retardation being merely one of its manifestations. Beyond this consensus, and despite decades of intensive research, the underlying biological and cognitive causes of the reading retardation are still hotly debated. Indeed, there are no less than three major theories of dyslexia. The goal of the present study is to produce evidence to decide between these theories.

The major theories of developmental dyslexia

We begin by providing a neutral overview of the different theories of dyslexia, as described by their proponents. Note that there are different versions of each theory in the literature, which we are not able to represent in detail. Instead, we have chosen to describe the currently most prominent version of each theory.

The phonological theory

The phonological theory postulates that dyslexics have a specific impairment in the representation, storage and/or retrieval of speech sounds. It explains dyslexics’ reading impairment by appealing to the fact that learning to read an alphabetic system requires learning the grapheme–phoneme correspondence, i.e. the correspondence between letters and constituent sounds of speech. If these sounds are poorly represented, stored or retrieved, the learning of grapheme–phoneme correspondences, the foundation of reading for alphabetic systems, will be affected accordingly (Bradley and Bryant, 1978; Vellutino, 1979;Snowling, 1981; Brady and Shankweiler, 1991). While theorists have different views about the nature of the phonological problems, they agree on the central and causal role of phonology in dyslexia. The phonological theory therefore postulates a straightforward link between a cognitive deficit and the behavioural problem to be explained. At the neurological level, it is usually assumed that the origin of the disorder is a congenital dysfunction of left‐hemisphere perisylvian brain areas underlying phonological representations, or connecting between phonological and orthographic representations.

Support for the phonological theory comes from evidence that dyslexic individuals perform particularly poorly on tasks requiring phonological awareness, i.e. conscious segmentation and manipulation of speech sounds. However, evidence for poor verbal short‐term memory and slow automatic naming in dyslexics also points to a more basic phonological deficit, perhaps having to do with the quality of phonological representations, or their access and retrieval (Snowling, 2000). Anatomical work (Galaburda et al., 1985; Geschwind and Galaburda, 1985) and functional brain imaging studies support the notion of a left perisylvian dysfunction as a basis for the phonological deficit (Paulesu et al., 1996, 2001; Shaywitz et al., 1998; Brunswick et al., 1999; McCrory et al., 2000;Pugh et al., 2000; Temple et al., 2001; Shaywitz et al., 2002).

In order to better differentiate the phonological theory from the others, we discuss here only the strong version of the theory: that the cognitive deficit is specific to phonology. Indeed, challengers of the phonological theory do not dispute the existence of a phonological deficit and its contribution to reading retardation; rather, they uphold that the disorder is much more extended, having its roots in general sensory, motor or learning processes, and that the phonological deficit is just one aspect or consequence of the more general disorder.

The rapid auditory processing theory

The most obvious way to challenge the specificity of the phonological deficit is to postulate that it is secondary to a more basic auditory deficit. This is the claim of the rapid auditory processing theory, which specifies that the deficit lies in the perception of short or rapidly varying sounds (Tallal, 1980; Tallal et al., 1993). Support for this theory arises from evidence that dyslexics show poor performance on a number of auditory tasks, including frequency discrimination (McAnally and Stein, 1996; Ahissar et al., 2000) and temporal order judgement (Tallal, 1980;Nagarajan et al., 1999) (see reviews by Farmer and Klein, 1995; McArthur and Bishop, 2001). Abnormal neurophysiological responses to various auditory stimuli have also been demonstrated (McAnally and Stein, 1996;Nagarajan et al., 1999; Kujala et al., 2000; Temple et al., 2000; Ruff et al., 2002). The failure to correctly represent short sounds and fast transitions would cause further difficulties in particular when such acoustic events are the cues to phonemic contrasts, as in /ba/ versus /da/. There is indeed also evidence that dyslexics may have poorer categorical perception of certain contrasts (Mody et al., 1997; Adlard and Hazan, 1998; Serniclaeset al., 2001). In this view, the auditory deficit is therefore the direct cause, in the course of development, of the phonological deficit, and hence of the difficulty in learning to read. The original version of the auditory theory made no particular claim at the biological level, but we will see below that this is now specified within the magnocellular theory.

The visual theory

The visual theory (Lovegrove et al., 1980; Livingstone et al., 1991; Stein and Walsh, 1997) reflects another long‐standing tradition in the study of dyslexia, that of considering it as a visual impairment giving rise to difficulties with the processing of letters and words on a page of text. This may take the form of unstable binocular fixations, poor vergence (Cornelissen et al., 1993; Stein and Fowler, 1993; Eden et al., 1994), or increased visual crowding (Spinelli et al., 2002). The visual theory does not exclude a phonological deficit, but emphasizes a visual contribution to reading problems, at least in some dyslexic individuals. At the biological level, the proposed aetiology of the visual dysfunction is based on the division of the visual system into two distinct pathways that have different roles and properties: the magnocellular and parvocellular pathways. The theory postulates that the magnocellular pathway is selectively disrupted in certain dyslexic individuals, leading to deficiencies in visual processing, and, via the posterior parietal cortex, to abnormal binocular control and visuospatial attention (Stein and Walsh, 1997; Hariet al., 2001). Evidence for magnocellular dysfunction comes from anatomical studies showing abnormalities of the magnocellular layers of the lateral geniculate nucleus (Livingstone et al., 1991), psychophysical studies showing decreased sensitivity in the magnocellular range, i.e. low spatial frequencies and high temporal frequencies, in dyslexics (Lovegroveet al., 1980; Cornelissen et al., 1995), and brain imaging studies (Eden et al., 1996).

The cerebellar theory

Yet another view is represented by the automaticity/cerebellar theory of dyslexia (Nicolson and Fawcett, 1990; Nicolson et al., 2001) (henceforth referred to as the cerebellar theory). Here the biological claim is that the dyslexic’s cerebellum is mildly dysfunctional and that a number of cognitive difficulties ensue. First, the cerebellum plays a role in motor control and therefore in speech articulation. It is postulated that retarded or dysfunctional articulation would lead to deficient phonological representations. Secondly, the cerebellum plays a role in the automatization of overlearned tasks, such as driving, typing and reading. A weak capacity to automatize would affect, among other things, the learning of grapheme–phoneme correspondences. Support for the cerebellar theory comes from evidence of poor performance of dyslexics in a large number of motor tasks (Fawcett et al., 1996), in dual tasks demonstrating impaired automatization of balance (Nicolson and Fawcett, 1990), and in time estimation, a non‐motor cerebellar task (Nicolson et al., 1995). Brain imaging studies have also shown anatomical, metabolic and activation differences in the cerebellum of dyslexics (Rae et al., 1998;Nicolson et al., 1999; Brown et al., 2001; Leonard et al., 2001).

The magnocellular theory

Finally, there is a unifying theory that attempts to integrate all the findings mentioned above. A generalization of the visual theory, the magnocellular theory (Stein and Walsh, 1997) postulates that the magnocellular dysfunction is not restricted to the visual pathways but is generalized to all modalities (visual and auditory as well as tactile). Furthermore, as the cerebellum receives massive input from various magnocellular systems in the brain, it is also predicted to be affected by the general magnocellular defect (Stein et al., 2001). Through a single biological cause, this theory therefore manages to account for all known manifestations of dyslexia: visual, auditory, tactile, motor and, consequently, phonological (for an attentional variant see Hari and Renvall, 2001). Beyond the evidence pertaining to each of the theories described previously, evidence specifically relevant to the magnocellular theory includes magnocellular abnormalities in the medial as well as the lateral geniculate nucleus of dyslexics’ brains (Livingstone et al., 1991; Galaburda et al., 1994), poor performance of dyslexics in the tactile domain (Grant et al., 1999;Stoodley et al., 2000), and the co‐occurrence of visual and auditory problems in certain dyslexics (Witton et al., 1998; Cestnick, 2001; van Ingelghem et al., 2001).

Although the auditory and visual theories have been presented here separately for historical and logical reasons, their supporters now agree that visual and auditory disorders in dyslexia are part of a more general magnocellular dysfunction. We will therefore not discuss the visual and auditory theories independently. Rather, we will restrict the discussion to a comparison between the phonological, cerebellar and magnocellular theories.

A critical look

The major weakness of the phonological theory is its inability to explain the occurrence of sensory and motor disorders in dyslexic individuals. Supporters of the phonological theory typically dismiss these disorders as not part of the core features of dyslexia. They consider their co‐occurrence with the phonological deficit as potential markers of dyslexia, but do not see them as playing a causal role in the aetiology of reading impairment (e.g. Snowling, 2000).

The cerebellar theory also fails to account for sensory disorders, but its proponents entertain the idea of distinct cerebellar and magnocellular dyslexia subtypes (Fawcett and Nicolson, 2001). Another problem for the cerebellar theory is that the causal link postulated between articulation and phonology relies on an outdated view of the motor theory of speech, according to which the development of phonological representations relies on speech articulation. This view has long been abandoned in the light of cases of normal phonological development despite severe dysarthria or apraxia of speech (for a discussion see Liberman and Mattingly, 1985;Ramus et al., 2003). Finally, it remains uncertain what proportion of dyslexics are affected by motor problems. A number of studies have failed to find any (Wimmer et al., 1998; van Daal and van der Leij, 1999;Kronbichler et al., 2002), others have found motor problems only in a subgroup of dyslexics (Yap and van der Leij, 1994; Ramus et al., 2003), and it has been suggested that motor dysfunction is found only in dyslexic children who also have attention‐deficit hyperactivity disorder (ADHD) (Denckla et al., 1985; Wimmer et al., 1999).

The magnocellular theory, unique in its ability to account for all manifestations of dyslexia, is undoubtedly attractive. Nevertheless, it also has its problems and has been facing growing criticism in recent years (e.g. Ramus, 2001). One line of criticism emphasizes a number of failures to replicate findings of auditory disorders in dyslexia (Heath et al., 1999; Hill et al., 1999; McArthur and Hogben, 2001). Other studies do find auditory deficits in dyslexics, but only in a subgroup, ranging from a few isolated individuals to 50% of the population studied (Tallal, 1980;Reed, 1989; Manis et al., 1997; Mody et al., 1997; Adlard and Hazan, 1998; Lorenzi et al., 2000; Marshall et al., 2001; Rosen and Manganari, 2001). Another line of criticism focuses on results inconsistent with the idea that the auditory deficit lies in ‘rapid’ auditory processing, and therefore with magnocellular function: indeed, with some tasks ‘rapid’ auditory processing is found to be intact, while with others ‘slow’ auditory processing is found to be impaired (Reed, 1989; McAnally and Stein, 1996; Adlard and Hazan, 1998; Schulte‐Körne et al., 1998b; Witton et al., 1998; Nittrouer, 1999; Lorenzi et al., 2000; Rosen and Manganari, 2001;Share et al., 2002). It is also argued that auditory deficits do not predict phonological deficits (Mody et al., 1997; Schulte‐Körne et al., 1998a;Bishop et al., 1999; Marshall et al., 2001; Rosen and Manganari, 2001;Share et al., 2002). Criticism of the visual side of the magnocellular theory also focuses on failures to replicate findings of a visual deficit (Victor et al., 1993; Johannes et al., 1996), or on findings of such a deficit only in a subgroup (Cornelissen et al., 1995; Witton et al., 1998; Amitay et al., 2002), and on inconsistencies between predictions and empirical results. Most notably, visual impairments, when found, seem to be observed across a whole range of stimuli, not just those specifically tapping the magnocellular system (Skottun, 2000; Amitay et al., 2002; Farrag et al., 2002). There is also negative evidence regarding cross‐modal sensory deficits (Heim et al., 2001). More generally, the idea that the magno‐/parvocellular distinction can be extended to non‐visual sensory systems remains controversial (personal communication, B. Skottun, 2002).

In summary, the phonological theory suffers from its inability to explain the sensory and motor disorders that occur in a significant proportion of dyslexics, while the magnocellular theory suffers mainly from its inability to explain the absence of sensory and motor disorders in a significant proportion of dyslexics. The cerebellar theory presents both types of problems.

Of course, it is possible that the three theories are true of different individuals. For instance, there could be three partially overlapping subtypes of dyslexia, each being an independent contribution to reading difficulties: phonological, auditory/visual, and cerebellar. Alternatively, it could also be that just one theory accounts for every case of dyslexia, and that the other manifestations observed are markers, i.e. they are associated without causation. In order to tease apart the many possible alternatives, we need to be able to answer such questions as: What proportion of dyslexics have a given deficit? Are there dissociations between certain deficits? Are there systematic associations between certain deficits? Unfortunately, the current literature does not contain answers to any of these questions. Indeed, virtually all studies have focused on just one or a few tasks within one modality, and most of them have only analysed group differences, making it impossible to assess what proportion of dyslexics are really affected by a deficit.

Three notable exceptions are worth mentioning. Witton et al. (1998) have shown significant differences between dyslexic and controls in frequency modulation (FM) detection at 2 Hz and coherent motion detection. The individual data reported suggest that four dyslexics out of 17 had abnormal performance in the visual task, nine out of 17 in the auditory task, and 15 out of 17 in non‐word reading. The absence of phonological and cerebellar tasks prevents the assessment of what might explain the reading impairment of the seven dyslexics who have normal visual and auditory performance, and to analyse the relationships between all the variables and their predictive power with respect to reading.

Van Ingelghem and colleagues tested both visual and auditory gap detection in dyslexic children and found significant group effects for both (Van Ingelghem et al., 2001). They report that nine dyslexics out of 10 were impaired in the auditory task and seven out of 10 in the visual task. However, their criterion for being impaired was that the individual’s threshold be above the 95% confidence interval for the control group, that is, for 10 individuals, >0.67 SD above the control mean. This makes it an extremely liberal criterion, since if the control group is normally distributed, ∼25% of the controls should also meet it (individual control data not available). Again, cerebellar and phonological performance was not tested. This study is also potentially undermined by the fact that the two groups were not matched in non‐verbal intelligence quotient (IQ), a factor that is known to affect performance significantly in psychophysical tasks (Ahissar et al., 2000).

It seems that only one study to date has assessed all the relevant modalities in a group of dyslexics (Kronbichler et al., 2002). The authors administered a battery of phonological tests and tests of auditory illusory movement perception, visual coherent motion detection, and peg moving. They report significant differences between the two groups in the phonological tests, but none in the auditory, visual or motor tasks. Unfortunately, no individual data are reported to allow assessment of whether some dyslexics could have sensory or motor disorders, and the relationships between the variables are not analysed. In all three studies, only one task for each modality was administered, leaving open the possibility that other, more sensitive tasks, might change the picture significantly.

The present study

Our aim was to produce data that would enable us to start answering questions concerning associations, dissociations and, eventually, causal relationships between sensory, motor, phonological and reading disorders. Our approach was that of a multiple case study: by having the most comprehensive neuropsychological profile for each individual, we sought to identify who had which combination of disorders and, crucially, who did not have a given disorder. We therefore created a battery of psychometric, phonological, auditory, visual and cerebellar tests to be administered to each subject. Within each domain, we selected several tasks that have, according to the literature, most consistently shown differences between dyslexics and controls.

Because we felt that dissociations between disorders would be the most informative, we selected a special dyslexic population, consisting of university students. Obviously, the few dyslexics who enter university are not representative of the whole population: they may be more intelligent, resourceful and socially privileged, and may have received better help with respect to reading. Most importantly, we hypothesized that they would be least likely to accumulate several types of disorders. For instance, if a phonological and a visual disorder can appear independently, an individual having both disorders should be less likely to succeed academically than an individual with just one of them. By studying a high‐achieving population, we therefore maximized our chances of finding pure cases of the different possible subtypes of dyslexia. For the same reason, we also minimized the chances of studying individuals with another comorbid developmental disorder, such as specific language impairment (SLI), ADHD and developmental coordination disorder, which would be an undesirable confound.

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