Connectionist neuropsychology: uncovering ultimate causes of acquired dyslexia

Acquired dyslexia offers a unique window on to the nature of the cognitive and neural architecture supporting skilled reading. This paper provides an integrative overview of recent empirical and computational work on acquired dyslexia within the context of the primary systems framework as implemented in connectionist neuropsychological models. This view proposes that damage to general visual, phonological or semantic processing abilities are the root causes of different forms of acquired dyslexia. Recent case-series behavioural evidence concerning pure alexia, phonological dyslexia and surface dyslexia that supports this perspective is presented. Lesion simulations of these findings within connectionist models of reading demonstrate the viability of this approach. The commitment of such models to learnt representations allows them to capture key aspects of performance in each type of acquired dyslexia, particularly the associated non-reading deficits, the role of relearning and the influence of individual differences in the premorbid state of the reading system. Identification of these factors not only advances our understanding of acquired dyslexia and the mechanisms of normal reading but they are also relevant to the complex interactions underpinning developmental reading disorders.     

Language cannot be reduced to biology: Perspectives from neuro-developmental disorders affecting language learning

The study of language knowledge guided by a purely biological perspective prioritizes the study of syntax. The essential process of syntax is recursion — the ability to generate an infinite array of expressions from a limited set of elements. Researchers working within the biological perspective argue that this ability is possible only because of an innately specified genetic makeup that is specific to human beings. Such a view of language knowledge may be fully justified in discussions on biolinguistics, and in evolutionary biology. However, it is grossly inadequate in understanding language-learning problems, particularly those experienced by children with neurodevelopmental disorders such as developmental dyslexia, Williams syndrome, specific language impairment and autism spectrum disorders. Specifically, syntax-centered definitions of language knowledge completely ignore certain crucial aspects of language learning and use, namely, that language is embedded in a social context; that the role of envrironmental triggering as a learning mechanism is grossly underestimated; that a considerable extent of visuo-spatial information accompanies speech in day-to-day communication; that the developmental process itself lies at the heart of knowledge acquisition; and that there is a tremendous variation in the orthographic systems associated with different languages. All these (socio-cultural) factors can influence the rate and quality of spoken and written language acquisition resulting in much variation in phenotypes associated with disorders known to have a genetic component. Delineation of such phenotypic variability requires inputs from varied disciplines such as neurobiology, neuropsychology, linguistics and communication disorders. In this paper, I discuss published research that questions cognitive modularity and emphasises the role of the environment for understanding linguistic capabilities of children with neuro-developmental disorders. The discussion pertains to two specific disorders, developmental dyslexia and Williams syndrome.     

Reading text increases binocular disparity in dyslexic children

Children with developmental dyslexia show reading impairment compared to their peers, despite being matched on IQ, socio-economic background, and educational opportunities. The neurological and cognitive basis of dyslexia remains a highly debated topic. Proponents of the magnocellular theory, which postulates abnormalities in the M-stream of the visual pathway cause developmental dyslexia, claim that children with dyslexia have deficient binocular coordination, and this is the underlying cause of developmental dyslexia. We measured binocular coordination during reading and a non-linguistic scanning task in three participant groups: adults, typically developing children, and children with dyslexia. A significant increase in fixation disparity was observed for dyslexic children solely when reading. Our study casts serious doubts on the claims of the magnocellular theory. The exclusivity of increased fixation disparity in dyslexics during reading might be a result of the allocation of inadequate attentional and/or cognitive resources to the reading process, or suboptimal linguistic processing per se.     

When words fail us: insights into language processing from developmental and acquired disorders

Acquired disorders of language represent loss of previously acquired skills, usually with relatively specific impairments. In children with developmental disorders of language, we may also see selective impairment in some skills; but in this case, the acquisition of language or literacy is affected from the outset. Because systems for processing spoken and written language change as they develop, we should beware of drawing too close a parallel between developmental and acquired disorders. Nevertheless, comparisons between the two may yield new insights. A key feature of connectionist models simulating acquired disorders is the interaction of components of language processing with each other and with other cognitive domains. This kind of model might help make sense of patterns of comorbidity in developmental disorders. Meanwhile, the study of developmental disorders emphasizes learning and change in underlying representations, allowing us to study how heterogeneity in cognitive profile may relate not just to neurobiology but also to experience. Children with persistent language difficulties pose challenges both to our efforts at intervention and to theories of learning of written and spoken language. Future attention to learning in individuals with developmental and acquired disorders could be of both theoretical and applied value.     

Developmental disorders: what can be learned from cognitive neuropsychology?

The discipline of cognitive neuropsychology has been important for informing theories of cognition and describing the nature of acquired cognitive disorders, but its applicability in a developmental context has been questioned. Here, we revisit this issue, asking whether the cognitive neuropsychological approach can be helpful for exploring the nature and causes of developmental disorders and, if so, how. We outline the key features of the cognitive neuropsychological approach, and then consider how some of the major challenges to this approach from a developmental perspective might be met. In doing so, we distinguish between challenges to the methods of cognitive neuropsychology and those facing its deeper conceptual underpinnings. We conclude that the detailed investigation of patterns of both associations and dissociations, and across both developmental and acquired cases, can assist in describing the cognitive deficits within developmental disorders and in delineating possible causal pathways to their acquisition.     

Iconicity as structure mapping

Linguistic and psycholinguistic evidence is presented to support the use of structure-mapping theory as a framework for understanding effects of iconicity on sign language grammar and processing. The existence of structured mappings between phonological form and semantic mental representations has been shown to explain the nature of metaphor and pronominal anaphora in sign languages. With respect to processing, it is argued that psycholinguistic effects of iconicity may only be observed when the task specifically taps into such structured mappings. In addition, language acquisition effects may only be observed when the relevant cognitive abilities are in place (e.g. the ability to make structural comparisons) and when the relevant conceptual knowledge has been acquired (i.e. information key to processing the iconic mapping). Finally, it is suggested that iconicity is better understood as a structured mapping between two mental representations than as a link between linguistic form and human experience.     

Reading and reading disturbance

Recent functional neuroimaging studies are generating novel insights into our knowledge of skilled and disturbed reading. In neurologically normal subjects, a double dissociation in neural activation in response to reading words and pseudowords has been revealed that corresponds to that observed in the comparison of semantic and phonological tasks. In patients with acquired dyslexia, functional imaging is demonstrating re-organisation within the reading system; in developmental dyslexia, functional imaging is being used to identify the impact of rehabilitation. Together, these findings have implications for cognitive models of reading that have previously relied on input from behavioural data.     

Synesthesia as a neuronal palimpsest

Synesthetes, a small fraction of the population, experience systematic, additional associations. For example, they may arbitrarily associate a specific color to each letter or number. Synesthesia has offered for the last ten years to cognitive science a unique opportunity to study the neural bases of subjective experience, drawing on individual differences just like in neuropsychology, but with healthy people. Here we review the current knowledge and propose a new theory, the "palimpsest hypothesis", a variant of the recycling hypothesis for reading. The neural development of written language expertise (a recent cultural invention acquired without any genetic modification) requires indeed the recycling of brain regions predisposed to expertise acquisition into reading regions. The palimpsest hypothesis supposes that for synesthetes recycling involves neuronal networks that were already specialized for color perception. Synesthetic colors would be the remains of this former expertise.     

Cognitive profile of students who enter higher education with an indication of dyslexia

For languages other than English there is a lack of empirical evidence about the cognitive profile of students entering higher education with a diagnosis of dyslexia. To obtain such evidence, we compared a group of 100 Dutch-speaking students diagnosed with dyslexia with a control group of 100 students without learning disabilities. Our study showed selective deficits in reading and writing (effect sizes for accuracy between d = 1 and d = 2), arithmetic (d≈1), and phonological processing (d>0.7). Except for spelling, these deficits were larger for speed related measures than for accuracy related measures. Students with dyslexia also performed slightly inferior on the KAIT tests of crystallized intelligence, due to the retrieval of verbal information from long-term memory. No significant differences were observed in the KAIT tests of fluid intelligence. The profile we obtained agrees with a recent meta-analysis of English findings suggesting that it generalizes to all alphabetic languages. Implications for special arrangements for students with dyslexia in higher education are outlined.     

The interface between genetics and psychology: lessons from developmental dyslexia

Developmental dyslexia runs in families, and twin studies have confirmed that there is a substantial genetic contribution to poor reading. The way in which discoveries in molecular genetics are reported can be misleading, encouraging us to think that there are specific genes that might be used to screen for disorder. However, dyslexia is not a classic Mendelian disorder that is caused by a mutation in a single gene. Rather, like many other common disorders, it appears to involve combined effects of many genes and environmental factors, each of which has a small influence, possibly supplemented by rare variants that have larger effects but apply to only a minority of cases. Furthermore, to see clearer relationships between genotype and phenotype, we may need to move beyond the clinical category of dyslexia to look at underlying cognitive deficits that may be implicated in other neurodevelopmental disorders.     

Developmental dyslexia is characterized by the co-existence of visuospatial and phonological disorders in Chinese children

Developmental dyslexia is a neurological condition that is characterized by severe impairment in reading skill acquisition in people with adequate intelligence and typical schooling [1], [2] and [3]. For English readers, reading impairment is critically associated with a phonological processing disorder [3], [4] and [5], which may co-occur with an orthographic (visual word form) processing deficit [6], but not with a general visual processing dysfunction in most dyslexics [7]. The pathophysiology of dyslexia varies across languages [8]: for instance, unlike English, written Chinese maps visually intricate graphic forms (characters) onto meanings; pronunciation of Chinese characters must be rote memorized. This suggests that, in Chinese, a fine-grained visuospatial analysis must be performed to activate characters' phonology and meaning; consequently, disordered phonological processing may commonly co-exist with abnormal visuospatial processing in Chinese dyslexia. To test this hypothesis, we conducted an fMRI experiment in which 12 Chinese dyslexics, shown previously [9] to exhibit a phonological disorder, performed a physical size judgment measuring visuospatial dimensions. Compared with 12 control subjects, the dyslexics showed weaker activations in left intraparietal sulcus (IPS) mediating visuospatial processing. Analyses of individual dyslexics' performances further suggest that developmental dyslexia in Chinese is commonly associated with the co-existence of a visuospatial deficit and a phonological disorder.     

Testing for the Dual-Route Cascade Reading Model in the Brain: An fMRI Effective Connectivity Account of an Efficient Reading Style

Neuropsychological data about the forms of acquired reading impairment provide a strong basis for the theoretical framework of the dual-route cascade (DRC) model which is predictive of reading performance. However, lesions are often extensive and heterogeneous, thus making it difficult to establish precise functional anatomical correlates. Here, we provide a connective neural account in the aim of accommodating the main principles of the DRC framework and to make predictions on reading skill. We located prominent reading areas using fMRI and applied structural equation modeling to pinpoint distinct neural pathways. Functionality of regions together with neural network dissociations between words and pseudowords corroborate the existing neuroanatomical view on the DRC and provide a novel outlook on the sub-regions involved. In a similar vein, congruent (or incongruent) reliance of pathways, that is reliance on the word (or pseudoword) pathway during word reading and on the pseudoword (or word) pathway during pseudoword reading predicted good (or poor) reading performance as assessed by out-of-magnet reading tests. Finally, inter-individual analysis unraveled an efficient reading style mirroring pathway reliance as a function of the fingerprint of the stimulus to be read, suggesting an optimal pattern of cerebral information trafficking which leads to high reading performance.     

Neural changes following remediation in adult developmental dyslexia

Brain imaging studies have explored the neural mechanisms of recovery in adults following acquired disorders and, more recently, childhood developmental disorders. However, the neural systems underlying adult rehabilitation of neurobiologically based learning disabilities remain unexplored, despite their high incidence. Here we characterize the differences in brain activity during a phonological manipulation task before and after a behavioral intervention in adults with developmental dyslexia. Phonologically targeted training resulted in performance improvements in tutored compared to nontutored dyslexics, and these gains were associated with signal increases in bilateral parietal and right perisylvian cortices. Our findings demonstrate that behavioral changes in tutored dyslexic adults are associated with (1) increased activity in those left-hemisphere regions engaged by normal readers and (2) compensatory activity in the right perisylvian cortex. Hence, behavioral plasticity in adult developmental dyslexia involves two distinct neural mechanisms, each of which has previously been observed either for remediation of developmental or acquired reading disorders.     

A sibling-pair based approach for mapping genetic loci that influence quantitative measures of reading disability

Family and twin studies consistently demonstrate a significant role for genetic factors in the aetiology of the reading disorder dyslexia. However, dyslexia is complex at both the genetic and phenotypic levels, and currently the nature of the core deficit or deficits remains uncertain. Traditional approaches for mapping disease genes, originally developed for single-gene disorders, have limited success when there is not a simple relationship between genotype and phenotype. Recent advances in high-throughput genotyping technology and quantitative statistical methods have made a new approach to identifying genes involved in complex disorders possible. The method involves assessing the genetic similarity of many sibling pairs along the lengths of all their chromosomes and attempting to correlate this similarity with that of their phenotypic scores. We are adopting this approach in an ongoing genome-wide search for genes involved in dyslexia susceptibility, and have already successfully applied the method by replicating results from previous studies suggesting that a quantitative trait locus at 6p21.3 influences reading disability.     

Pleiotropic effects of a chromosome 3 locus on speech-sound disorder and reading

Speech-sound disorder (SSD) is a complex behavioral disorder characterized by speech-sound production errors associated with deficits in articulation, phonological processes, and cognitive linguistic processes. SSD is prevalent in childhood and is comorbid with disorders of language, spelling, and reading disability, or dyslexia. Previous research suggests that developmental problems in domains associated with speech and language acquisition place a child at risk for dyslexia. Recent genetic studies have identified several candidate regions for dyslexia, including one on chromosome 3 segregating in a large Finnish pedigree. To explore common genetic influences on SSD and reading, we examined linkage for several quantitative traits to markers in the pericentrometric region of chromosome 3 in 77 families ascertained through a child with SSD. The quantitative scores measured several processes underlying speech-sound production, including phonological memory, phonological representation, articulation, receptive and expressive vocabulary, and reading decoding and comprehension skills. Model-free linkage analysis was followed by identification of sib pairs with linkage and construction of core shared haplotypes. In our multipoint analyses, measures of phonological memory demonstrated the strongest linkage (marker D3S2465, P=5.6 x 10(-5), and marker D3S3716, P=6.8 x 10(-4)). Tests for single-word decoding also demonstrated linkage (real word reading: marker D3S2465, P=.004; nonsense word reading: marker D3S1595, P=.005). The minimum shared haplotype in sib pairs with similar trait values spans 4.9 cM and is bounded by markers D3S3049 and D3S3045. Our results suggest that domains common to SSD and dyslexia are pleiotropically influenced by a putative quantitative trait locus on chromosome 3.     

Project DyAdd: Fatty acids and cognition in adults with dyslexia, ADHD, or both

Both attention deficit hyperactivity disorder (ADHD) and dyslexia are suggested to co-occur with altered fatty acid (FA) metabolism, but it is unknown how FAs are associated with the cognitive domains that characterize these disorders. In the project DyAdd, we investigated the associations between FAs in serum phospholipids and phonological processing, reading, spelling, arithmetic, executive functions, and attention. Healthy controls (n=36), adults with ADHD (n=26), dyslexia (n=36), or both (n=9) were included in the study. FAs included saturated, monounsaturated, total polyunsaturated, n-3, and n-6 FAs, together with n-6/n-3, AA/EPA, and LA/ALA ratios. When all the study subjects were included in the analyses, especially polyunsaturated FAs (PUFAs) were positively associated with cognition, but reading was least associated with FAs. These associations were modulated by gender, intelligence, n-3 PUFA intake, and group. Accordingly, within the ADHD group, only few associations emerged with PUFAs, n-6 PUFAs, and cognitive domains, whereas in the dyslexia group the more prevalent associations appeared with PUFAs and n-3 PUFAs.     

Interval timing in children: effects of auditory and visual pacing stimuli and relationships with reading and attention variables

Motor timing tasks have been employed in studies of neurodevelopmental disorders such as developmental dyslexia and ADHD, where they provide an index of temporal processing ability. Investigations of these disorders have used different stimulus parameters within the motor timing tasks that are likely to affect performance measures. Here we assessed the effect of auditory and visual pacing stimuli on synchronised motor timing performance and its relationship with cognitive and behavioural predictors that are commonly used in the diagnosis of these highly prevalent developmental disorders. Twenty-one children (mean age 9.6 years) completed a finger tapping task in two stimulus conditions, together with additional psychometric measures. As anticipated, synchronisation to the beat (ISI 329 ms) was less accurate in the visually paced condition. Decomposition of timing variance indicated that this effect resulted from differences in the way that visual and auditory paced tasks are processed by central timekeeping and associated peripheral implementation systems. The ability to utilise an efficient processing strategy on the visual task correlated with both reading and sustained attention skills. Dissociations between these patterns of relationship across task modality suggest that not all timing tasks are equivalent.     

Reading Performance Is Enhanced by Visual Texture Discrimination Training in Chinese-Speaking Children with Developmental Dyslexia

Background

High order cognitive processing and learning, such as reading, interact with lower-level sensory processing and learning. Previous studies have reported that visual perceptual training enlarges visual span and, consequently, improves reading speed in young and old people with amblyopia. Recently, a visual perceptual training study in Chinese-speaking children with dyslexia found that the visual texture discrimination thresholds of these children in visual perceptual training significantly correlated with their performance in Chinese character recognition, suggesting that deficits in visual perceptual processing/learning might partly underpin the difficulty in reading Chinese.

Methodology/Principal Findings

To further clarify whether visual perceptual training improves the measures of reading performance, eighteen children with dyslexia and eighteen typically developed readers that were age- and IQ-matched completed a series of reading measures before and after visual texture discrimination task (TDT) training. Prior to the TDT training, each group of children was split into two equivalent training and non-training groups in terms of all reading measures, IQ, and TDT. The results revealed that the discrimination threshold SOAs of TDT were significantly higher for the children with dyslexia than for the control children before training. Interestingly, training significantly decreased the discrimination threshold SOAs of TDT for both the typically developed readers and the children with dyslexia. More importantly, the training group with dyslexia exhibited significant enhancement in reading fluency, while the non-training group with dyslexia did not show this improvement. Additional follow-up tests showed that the improvement in reading fluency is a long-lasting effect and could be maintained for up to two months in the training group with dyslexia.

Conclusion/Significance

These results suggest that basic visual perceptual processing/learning and reading ability in Chinese might at least partially rely on overlapping mechanisms.     

A Common Left Occipito-Temporal Dysfunction in Developmental Dyslexia and Acquired Letter-By-Letter Reading?

Background

We used fMRI to examine functional brain abnormalities of German-speaking dyslexics who suffer from slow effortful reading but not from a reading accuracy problem. Similar to acquired cases of letter-by-letter reading, the developmental cases exhibited an abnormal strong effect of length (i.e., number of letters) on response time for words and pseudowords.

Results

Corresponding to lesions of left occipito-temporal (OT) regions in acquired cases, we found a dysfunction of this region in our developmental cases who failed to exhibit responsiveness of left OT regions to the length of words and pseudowords. This abnormality in the left OT cortex was accompanied by absent responsiveness to increased sublexical reading demands in phonological inferior frontal gyrus (IFG) regions. Interestingly, there was no abnormality in the left superior temporal cortex which—corresponding to the onological deficit explanation—is considered to be the prime locus of the reading difficulties of developmental dyslexia cases.

Conclusions

The present functional imaging results suggest that developmental dyslexia similar to acquired letter-by-letter reading is due to a primary dysfunction of left OT regions.     

Spatial and temporal measurements of eye movement in children with dyslexia

This paper presents the first reading data in Croatian collected with an eye-tracking device. The eye-tracking method allows for research into two crucial levels underlying reading: the visual and the cognitive. The aim of this paper is to show the differences in eye movements in children with dyslexia using the principles of cognitive-control view. Despite the well-known definitions and vast literature on dyslexia, the neural basis of dyslexia varies greatly on the individual level. The three children studied in this paper were tested behaviorally using set of language tests for language behavior assessment on all language levels: phonology, morphology, syntax, lexicon and pragmatics. Two children had low scores on most language tests, and all three children had poor reading and writing level. Each of the children had to read two texts silently while their eye movements were recorded by means of an infrared eye-tracking system. We analyzed the number, position, and duration of fixations and the number and position of regressive (or back) saccades. Our results show intergroup differences (between a typically developing child and the three children with dyslexia), and intragroup differences (among all three children with dyslexia). The great number of fixations, longer duration of fixations, and great number of regression saccades are the main features that differentiate the children with dyslexia form the typically developing child. The only difference found between language and visual subtypes of dyslexia was a shorter duration of fixations for the child with a visual processing disorder.