Electrophysiological Evidence against the Magnocellular Deficit Theory in Developmental Dyslexia

Melissa Sue Sayeur, Renée Béland, Dave Ellemberg, Caroline Perchet, Michelle McKerral, Maryse Lassonde, Karyne Lavoie

National Institute of Health and Medical Research, Montreal, France.
Research Centre in Neuropsychology and Cognition, University of Montreal, Montreal, Canada.
Research Centre, Sainte-Justine Hospital, Montreal, Canada.

DOI: 10.4236/jbbs.2013.32025                

Abstract

Over the last two decades, the hypothesis of a magnocellular deficit in dyslexia has raised considerable interest and controversy. Using an electrophysiological procedure (visual evoked potentials, VEP), we compared magnocellular and parvocellular contrast and spatial frequency-response functions between phonological dyslexics (n = 16) and a typical reading group (n = 12) matched for age and socioeconomic background. No significant differences were found between the two groups in the amplitude of the VEP components associated with either magnocellular or parvocellular responses. However, topographic analyses revealed a group difference in the distribution of amplitude in the right frontal and left temporal regions, which appeared to be underactivated in dyslexics. These results suggest a deficit in the higher-level cortical regions involved in phonological and/or linguistic processing, and calls into question the notion of a magnocellular involvement in dyslexia.

Keywords

Dyslexia; Magnocellular and Parvocellular Pathways; Visual Evoked Potentials; Contrast Sensitivity; Spatial Frequencies

1. Introduction

A substantial proportion of children (15% - 20%) have a specific reading disability [1,2]. The latest edition of the Diagnostic and Statistical Manual of Mental Disorders (DSM-IV) defines dyslexia as a specific reading disability affecting reading accuracy, reading speed or reading comprehension, despite normal intellectual abilities, sensory functioning (i.e., visual or auditory), socioeconomic, and educational opportunities [3]. Dyslexia is diagnosed if the child is reading significantly below the expected level for the child’s chronological age and general intellect [4].

Much of the recent evidence indicates that dyslexia could result from a deficit in phonological processing. Impaired phonological processing would result from a dysfunction of the neuronal circuits that are responsible for establishing spelling-to-sound correspondences in reading acquisition. Several neuroimaging studies have confirmed this hypothesis by identifying functional disruptions of the neural systems responsible for phonological analysis in dyslexics compared to typical readers (TR) group [2,5]. For example, Breier, Simos, Fletcher et al. [6] found abnormal activation in language areas within the temporal cortex, and Hoeft, Meyler, Hernandez et al. [7] showed reduced activation in the parietal cortex. Furthermore, genetic linkage studies have found a locus on chromosome 2 for the transmission of deficits in phonological awareness and subsequent reading difficulties [8]. Finally, numerous studies have shown that phonological skills in pre-school children are a good predictor of their later reading proficiency [9-15].

In addition to the deficit in phonological processing, a number of studies have suggested that individuals with dyslexia also have anomalies in certain aspects of visual processing: a) poor oculomotor ability during reading, including frequent and longer fixations and shorter saccades; and b) poor ocular convergence and divergence [16]. Since the mid-1970s, it has been persistently argued that an impairment in one of the main neuronal pathways of the visual system, the magnocellular pathway, is at the root of dyslexia [17-20]. A better understanding of the magnocellular deficit hypothesis requires a brief explanation of the role of the magnocellular (M) and parvocellullar (P) systems in vision. The M and P pathways originate from the retina, project to the M and P layers of the lateral geniculate nucleus (LGN), and remain anatomically separate until they reach the primary visual cortex (area V1) [21,22]. At the cortical level, the M and P pathways are also known, respectively, as the dorsal (M) or “where/how” stream, and ventral (P) or “what” stream. The M and P pathways differ in terms of anatomy, physiology, and functionality [23-27]; the dorsal (M) stream is mainly responsible for perceiving rapid motion, localizing objects and targets, and is more sensitive to low contrasts and low spatial frequencies [4,28-31], whereas the ventral (P) stream is mainly responsible for perceiving forms, colours and identifying targets, and is more sensitive to high contrasts and high spatial frequencies [4, 28-31]. Physiological and psychophysical studies have demonstrated that the M and P streams inhibit each other’s activity, and that their contribution is reciprocal [32,33]. To date, the exact implication of the magnocellular pathway in reading has not been fully established; nevertheless, many hypotheses have been proposed. For example, Breitmeyer’s [34,35] visual masking model suggests an increase in visual persistence in dyslexics caused by reduced inhibition of the parvocellular pathway resulting from the putative magnocellular deficit. Alternately, other authors argue that a dysfunctional magnocellular system could reduce visual sensitivity to moving or flickering stimuli [36], and consequently interfere with lexical decision tasks [37] or small letter detection [38]. Although the empirical support for the magnocellular deficit theory of dyslexia is weak, it remains a highly debated issue [38-44].

According to some authors, the magnocellular deficit theory could explain the phonological deficit in dyslexics [45]. The implication of this theory is that individuals with impaired phonological processing would exhibit processing deficits across all sensory modalities, including vision and audition. To illustrate, a child having difficulty processing these critical, rapid auditory changes could be further unable to distinguish /b/ and /d/ or to learn the grapheme-phoneme correspondence involved in early reading. The findings of several studies using different approaches have supported the magnocellular deficit theory of dyslexia. In anatomical studies, for example, brain autopsies of adults who had dyslexia revealed anomalies in the magnocellular layers of the LGN, although the parvocellular layers were intact [39]. In addition, anatomical evidence indicates that the cells in the M layers of the LGN are smaller and more disorganized compared to those in a control group [46,47]. Furthermore, functional brain imaging has demonstrated that, compared to good readers, dyslexics show underactivation in some regions of the dorsal stream (MT or V5) that respond to motion [48-50].

Both psychophysical and visual evoked potential (VEP) studies have provided some evidence for deficits in the magnocellular system in dyslexia. Specifically, psychophysical studies report reduced sensitivity to stimuli that contain lower spatial frequencies and/or higher temporal frequencies [38,41,45,50-52], and VEP studies have shown that, compared to good readers, dyslexics present reduced amplitude and/or increased latency of the P1 and/or the N2 components when presented with stimuli designed to elicit a magnocellular response [39,53-57]. Finally, dyslexic individuals showed increased latency and reduced amplitude over the occipital and parietotemporal cortex, as measured by motion-onset VEPs [54,58]. However, it is important to note that the specific pattern of results varies widely across studies due to differences in subjects’ age or experimental design or to comorbid disorders such as ADHD.

In fact, few VEP studies have used optimal stimuli to dissociate the M and P pathway responses. For example, most studies used checkerboard patterns to activate responses from a wide range of spatial frequency mechanisms that are not restricted to the magnocellular pathway [39,59-61]. Moreover, the majority of studies based their conclusions on inductive reasoning, either because they used stimulus conditions that tested only one pathway (either M or P), or they used paradigms constructed from a theoretical rationale based on animal studies that have not been validated in humans. Finally, the studies that did investigate both the M and P pathway responses used different paradigms to do so, which limits comparison and consequently data interpretation [62].

A study by Ellemberg et al. [63] used VEPs to identify and isolate characteristic responses of the M and P pathways in human adults. Specifically, using vertical sinusoidal gratings, they found that at the lowest spatial frequencies (< 2c/deg), the waveform was composed of the P1 component only. This component had the characteristic M contrast response: it appeared at the lowest contrast level used (2%), and its amplitude rapidly saturated to reach asymptote at about 12% contrast. At higher spatial frequency, a second component appeared, the N1, which had the characteristics of the P contrast response; that is, it appeared at higher contrasts (about 10% - 20%), dominated at the highest spatial frequency, and appeared not to saturate in amplitude. Because of the distinct contrast responses of the P1 and N1 components, the VEPs were also able to dissociate the contribution of the M and P streams at intermediate spatial frequencies. This was the first human study to confirm that the two systems operate over a spatial frequency continuum, and that they can be dissociated using a single stimulus (an intermediate spatial frequency at medium contrasts).

The goal of the present study was to verify the hypothesis of a magnocellular deficit in developmental dyslexia using a paradigm that provides a more direct measurement and comparison of the M and P responses, which has been validated in adults and young children [28,29,63].

2. Materials and Methods

2.1. Subjects

16 dyslexic children and 12 typical readers participated in the study. The mother tongue of all participants was French. Each child was assessed by an optometrist, and all had normal or corrected-to-normal visual acuity with no history of visual disorders. All children scored a full scale IQ above 90 on the Wechsler Intelligence Scale for Children—3rd Edition (WISC-III, Table 1) and they all underwent reading and phonological tasks to assess their reading and phonological abilities (Table 2). The procedures were explained and informed consent was obtained from the parents. The experimental protocol was approved by the Research Ethics Board of the University of Montreal.

The dyslexic group consisted of 13 boys and 3 girls, aged 8.5 to 13.5 years (mean age: 10.88 years ± 1.49 years). Inclusion criteria’s were: a two-year delay in reading acquisition and the absence of neurological, auditory, visual, and psychiatric disorders. In addition, all children had dyslexia of the phonological type, as indicated by their poor results on tasks assessing reading and phonological abilities. The typical reading (TR) development group consisted of 12 children, 9 boys and 3 girls, aged 9 to 12 years (mean age: 10.6 years ± 1.09 years). All children had normal reading abilities. None had a history of language delay, neurological, auditory, visual, psychiatric disorders, or learning disabilities.

Table 1. Results obtained at the Wechsler Intelligence Scale for Children—3rd Edition (WISC-III) for each subject.

Table 2. Results on tasks to assess reading and phonological abilities for each subject.

2.2. Reading and Phonological Tasks

A French reading test, created by the Research Institute and Psychopedagogy Evaluation (IREP), comprised two timed tasks: one assessing reading fluency and one assessing reading comprehension. In the reading fluency condition, which lasted 8 minutes, the child was asked to read a series of short paragraphs. For each paragraph, the child was required to cross out the word that contradicted the meaning of the paragraph. In the comprehension component, the child answered a series of multiple-choice questions, trying to answer as many questions as possible in 10 minutes. Phonological awareness was assessed using tasks involving both phonological sensitivity (rhyme judgement, auditory discrimination task) and metaphonological awareness (nonword repetition, rhyme production, synthesis, segmentation, and inversion). All tasks were preceded by practice items where the children received feedback on their performance.

2.3. Stimuli and Apparatus

The stimuli consisted of vertical sinusoidal gratings 18˚ wide and 18˚ high when viewed from a distance of 114 cm. Four levels of contrast (4, 16, 32, and 90%) were presented at a spatial frequency of 4.0 c/deg, and four spatial frequencies (2.0, 4.0, 8.0, and 16 c/deg) were presented at 16% contrast. These values were chosen because they were shown to best represent the characteristic M and P contrast and spatial frequency response functions by Ellemberg et al. [63]. The strongest M response was expected in the 4 c/deg/4% condition, whereas the strongest P response was expected at 16 c/deg/16%. Contrast levels were established using the Michelson contrast formula [64].

The stimuli were generated by a Power Macintosh computer using Pixx software and displayed on a 21-inch View Sonic monitor at a frame rate of 75 Hz and a pixel resolution of 1024 × 768. VEPs were recorded with Sa Instruments bioamplifiers and data were filtered and averaged using InStep (version IV). The average luminance of the stimuli was maintained at 35 cd·m⁻² and the ambient luminance was 8 cd·m^–2.

2.4. Procedure

The children viewed the screen binocularly from a distance of 114 cm. They were instructed to fixate on a small cross (0.25˚) positioned at the centre of the display. Each grating phase was reversed at a temporal frequency of 1 Hz (2 reversals/sec), for a total of 190 reversals. The order of presentation was randomized across children to control for effects of habituation and/or fatigue. An experimental session, including electrode placement and the administration of the seven conditions, lasted about one hour.

2.5. Recording

Cortical responses were recorded from the following leads: Fp1, Fp2, Af3, Af4, F7, F3, Fz, F4, F8, FC3, FC4, C3, C1, Cz, C2, C4, CP3, CP4, Tp7, Tp8, T7, T8, P3, P4, P7, P8, Pz, O1, O2, Oz (as defined by the international 10 - 20 system), with reference to linked earlobes. Tin electrodes were placed on the scalp with an ElectroCap^™. Electrode impedance was kept below 5 khoms. Digital recording rate was 256 Hz and a 0.02 - 30 Hz analog bandpass was applied.

2.6. Data Analysis

Following a commonly used and well accepted convention [62,63], the N1 peak was defined as the point where amplitude was the lowest between 50 and 90 ms, and the P1 peak as the point where amplitude was the highest between 80 and 140 ms. N1 and P1 amplitudes were measured relative to baseline, which was calculated from the average amplitude of the first 30 ms after the onset of averaging [62,63,65,66]. For the statistical analysis, analyses of variance (ANOVAs) were run on the amplitude data, separately for each waveform P1 and N1 and separately for contrast and spatial frequency.

2.7. Topographic Analysis

We completed a topographic analysis on the VEP signals by identifying the maximum amplitude of the peak at Oz and calculating the response on all leads for each child. For statistical comparison, data were analyzed using StatMap for topographical analysis (DigiMed Systems Inc.) and a McCarthy-Wood correction was run to normalize the results.

3. Results

Figure 1 presents the average waveforms for the dyslexic and TR groups for the optimal M condition (1a) and the P condition (1b).

Conflicts of Interest

The authors declare no conflicts of interest.

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