Marie Lallier

A case study of developmental phonological dyslexia: Is the attentional deficit in the perception of rapid stimuli sequences amodal?

The attentional blink (AB) refers to a decrease in accuracy that occurs when participants are required to detect the second of two rapidly sequential targets displayed randomly in a stream of distracters. Dyslexic individuals have been shown to exhibit a prolonged AB in the visual modality, interpreted as evidence of sluggish attentional shifting (SAS). However, the amodal SAS theory predicts that the disorder should further extend to the auditory modality, then resulting in a phonological disorder as typically found in developmental dyslexia. Otherwise, it has been demonstrated that a visual attention (VA) span deficit contributes to the poor reading outcome of dyslexic individuals, independently of their phonological skills. The present study assesses the amodality assumption of the SAS theory together with questioning its relation with the VA span deficit. For this purpose, visual and auditory ABs were explored in a well compensated young adult, LL, who exhibits a pure phonological dyslexia characterised by poor pseudo-word processing and poor phonological skills but preserved VA span. The investigation revealed two different kinds of deficits in LL. Her AB was prolonged and marginally deeper in the visual modality whereas a primarily deeper in amplitude and a subtle prolonged AB was found in the auditory modality. The atypical performance patterns of LL in both modalities suggest that her perceptual attention disorder is amodal as predicted by the SAS theory. This amodal disorder was here reported in a dyslexic participant with a phonological disorder, well in accordance with the hypothesis that sluggish auditory attention shifting contributes to difficulties in phoneme awareness and literacy acquisition. Furthermore, prolonged VA blink was observed in the absence of VA span disorder, thus suggesting that visual attentional shifting and VA span might be distinct mechanisms, contributing independently to reading acquisition and developmental dyslexia.

Behavioral and ERP evidence for amodal sluggish attentional shifting in developmental dyslexia

The goal of this study was to examine the claim that amodal deficits in attentional shifting may be the source of reading acquisition disorders in phonological developmental dyslexia (sluggish attentional shifting, SAS, theory, Hari & Renvall, 2001). We investigated automatic attentional shifting in the auditory and visual modalities in 13 dyslexic young adults with a phonological awareness deficit and 13 control participants, matched for cognitive abilities, using both behavioral and ERP measures. We tested automatic attentional shifting using a stream segregation task (perception of rapid succession of visual and auditory stimuli as one or two streams). Results of Experiment 1(behavioral) suggested that in order to process two successive stimuli separately dyslexic participants required a significantly longer inter-stimulus interval than controls regardless of sensory modality. In Experiment 2 (ERPs), the same participants were tested by means of an auditory and a visual oddball tasks involving variations in the tempo of the same alternating stimuli as Experiment 1. P3b amplitudes elicited by deviant tempos were differently modulated between groups, supporting predictions made on the basis of observations in Experiment 1. Overall, these results support the hypothesis that SAS in dyslexic participants might be responsible for their atypical perception of rapid sequential stimulus sequences in both the auditory and the visual modalities. Furthermore, these results bring new evidence supporting the link between amodal SAS and the phonological impairment in developmental dyslexia.

Out‐of‐synchrony speech entrainment in developmental dyslexia

Developmental dyslexia is a reading disorder often characterized by reduced awareness of speech units. Whether the neural source of this phonological disorder in dyslexic readers results from the malfunctioning of the primary auditory system or damaged feedback communication between higher‐order phonological regions (i.e., left inferior frontal regions) and the auditory cortex is still under dispute. Here we recorded magnetoencephalographic (MEG) signals from 20 dyslexic readers and 20 age‐matched controls while they were listening to ∼10‐s‐long spoken sentences. Compared to controls, dyslexic readers had (1) an impaired neural entrainment to speech in the delta band (0.5–1 Hz); (2) a reduced delta synchronization in both the right auditory cortex and the left inferior frontal gyrus; and (3) an impaired feedforward functional coupling between neural oscillations in the right auditory cortex and the left inferior frontal regions. This shows that during speech listening, individuals with developmental dyslexia present reduced neural synchrony to low‐frequency speech oscillations in primary auditory regions that hinders higher‐order speech processing steps. The present findings, thus, strengthen proposals assuming that improper low‐frequency acoustic entrainment affects speech sampling. This low speech‐brain synchronization has the strong potential to cause severe consequences for both phonological and reading skills. Interestingly, the reduced speech‐brain synchronization in dyslexic readers compared to normal readers (and its higher‐order consequences across the speech processing network) appears preserved through the development from childhood to adulthood. Thus, the evaluation of speech‐brain synchronization could possibly serve as a diagnostic tool for early detection of children at risk of dyslexia. Hum Brain Mapp 37:2767–2783, 2016.

Dyslexia in a French-Spanish bilingual girl: behavioural and neural modulations following a visual attention span intervention.

We report the case study of a French-Spanish bilingual dyslexic girl, MP, who exhibited a severe visual attention (VA) span deficit but preserved phonological skills. Behavioural investigation showed a severe reduction of reading speed for both single items (words and pseudo-words) and texts in the two languages. However, performance was more affected in French than in Spanish. MP was administered an intensive VA span intervention programme. Pre-post intervention comparison revealed a positive effect of intervention on her VA span abilities. The intervention further transferred to reading. It primarily resulted in faster identification of the regular and irregular words in French. The effect of intervention was rather modest in Spanish that only showed a tendency for faster word reading. Text reading improved in the two languages with a stronger effect in French but pseudo-word reading did not improve in either French or Spanish. The overall results suggest that VA span intervention may primarily enhance the fast global reading procedure, with stronger effects in French than in Spanish. MP underwent two fMRI sessions to explore her brain activations before and after VA span training. Prior to the intervention, fMRI assessment showed that the striate and extrastriate visual cortices alone were activated but none of the regions typically involved in VA span. Post-training fMRI revealed increased activation of the superior and inferior parietal cortices. Comparison of pre- and post-training activations revealed significant activation increase of the superior parietal lobes (BA 7) bilaterally. Thus, we show that a specific VA span intervention not only modulates reading performance but further results in increased brain activity within the superior parietal lobes known to housing VA span abilities. Furthermore, positive effects of VA span intervention on reading suggest that the ability to process multiple visual elements simultaneously is one cause of successful reading acquisition.

Cross-linguistic interactions influence reading development in bilinguals: a comparison between early balanced French-Basque and Spanish-Basque bilingual children

This study investigates whether orthographic consistency and transparency of languages have an impact on the development of reading strategies and reading sub-skills (i.e. phonemic awareness and visual attention span) in bilingual children. We evaluated 21 French (opaque)-Basque (transparent) bilingual children and 21 Spanish (transparent)-Basque (transparent) bilingual children at Grade 2, and 16 additional children of each group at Grade 5. All of them were assessed in their common language (i.e. Basque) on tasks measuring word and pseudoword reading, phonemic awareness and visual attention span skills. The Spanish speaking groups showed better Basque pseudoword reading and better phonemic awareness abilities than their French speaking peers, but only in the most difficult conditions of the tasks. However, on the visual attention span task, the French-Basque bilinguals showed the most efficient visual processing strategies to perform the task. Therefore, learning to read in an additional language affected differently Basque literacy skills, depending on whether this additional orthography was opaque (e.g. French) or transparent (e.g. Spanish). Moreover, we showed that the most noteworthy effects of Spanish and French orthographic transparency on Basque performance were related to the size of the phonological and visual grain used to perform the tasks.

Developmental evaluation of atypical auditory sampling in dyslexia: Functional and structural evidence.

Whether phonological deficits in developmental dyslexia are associated with impaired neural sampling of auditory information at either syllabic‐ or phonemic‐rates is still under debate. In addition, whereas neuroanatomical alterations in auditory regions have been documented in dyslexic readers, whether and how these structural anomalies are linked to auditory sampling and reading deficits remains poorly understood. In this study, we measured auditory neural synchronization at different frequencies corresponding to relevant phonological spectral components of speech in children and adults with and without dyslexia, using magnetoencephalography. Furthermore, structural MRI was used to estimate cortical thickness of the auditory cortex of participants. Dyslexics showed atypical brain synchronization at both syllabic (slow) and phonemic (fast) rates. Interestingly, while a left hemispheric asymmetry in cortical thickness was functionally related to a stronger left hemispheric lateralization of neural synchronization to stimuli presented at the phonemic rate in skilled readers, the same anatomical index in dyslexics was related to a stronger right hemispheric dominance for neural synchronization to syllabic‐rate auditory stimuli. These data suggest that the acoustic sampling deficit in development dyslexia might be linked to an atypical specialization of the auditory cortex to both low and high frequency amplitude modulations. Hum Brain Mapp 36:4986–5002, 2015.

Impact of orthographic transparency on typical and atypical reading development: evidence in French-Spanish bilingual children.

The present study aimed to quantify cross-linguistic modulations of the contribution of phonemic awareness skills and visual attention span (VA Span) skills (number of visual elements that can be processed simultaneously) to reading speed and accuracy in 18 Spanish-French balanced bilingual children with and without developmental dyslexia. The children were administered two similar reading batteries in French and Spanish. The deficits of the dyslexic children in reading accuracy were mainly visible in their opaque orthography (French) whereas difficulties indexed by reading speed were observed in both their opaque and transparent orthographies. Dyslexic children did not exhibit any phonemic awareness problems in French or in Spanish, but showed poor VA Span skills compared to their control peers. VA span skills correlated with reading accuracy and speed measures in both Spanish and French, whereas phonemic awareness correlated with reading accuracy only. Overall, the present results show that the VA Span is tightly related to reading speed regardless of orthographic transparency, and that it accounts for differences in reading performance between good and poor readers across languages. The present findings further suggest that VA Span skills may play a particularly important role in building-up specific word knowledge which is critical for lexical reading strategies.

Oscillatory "temporal sampling" and developmental dyslexia: toward an over-arching theoretical framework.

Human cognitive systems such as language represent the sensory world as unitary. For example, the “speech signal” is perceived as a single auditory stimulus, and different visual features and textures in the visual field are perceived holistically as unitary objects. Yet sensory neuroscience demonstrates the diversity of encoding in the neural systems supporting sensory perception. Different aspects of sensory information are processed in parallel, often at different timescales and by different populations of neurons. Further, research into the function of neuronal oscillations (e.g., Buzsaki and Draguhn, 2004) reveals a key role in processing sensory information. In this special issue, we investigate the developmental implications of one neuroscientific theory based on oscillations that is relevant to reading education and developmental dyslexia, the “temporal sampling” framework (hereafter TSF, Goswami, 2011). The TSF identifies specific oscillatory mechanisms that may be impaired in dyslexia. We expect that deeper understanding of neural mechanisms of information-processing will eventually enable deeper understanding of developmental disorders of learning, such as dyslexia. Developmental dyslexia is a disorder in the acquisition of successful reading and spelling skills that is found in ~7% of children across cultures. The ability to read and write—the achievement of literacy—is one of the most complex and sophisticated cognitive skills developed by the brain. Literacy skills develop as a result of direct teaching, usually in childhood, and become fluent during years of practice. By adulthood, most brains have read millions of words. This makes it difficult to disentangle cause from effect when studying sensory and neural factors. Dyslexia is usually only diagnosed after 2–3 years of schooling, when the brain has already had considerable experience of reading and reading tuition. Dyslexia is diagnosed when children who are receiving adequate teaching and who have no overt sensory or neurological problems fail to develop fast, efficient and age-appropriate reading and spelling. The TSF was proposed as the neural basis for the extraction of phonological information from speech via auditory oscillatory encoding (Goswami, in press). Based on work by Poeppel, Greenberg, Giraud, Ghitza and many others (Giraud and Poeppel, 2012, for a recent summary), the TSF linked “sampling” of the speech stream by auditory cortical networks operating at different timescales or oscillatory frequencies (delta, theta, gamma) to the emergence of phonological (linguistic) coding of speech by children. Poeppel and others argued that cortical oscillations enabled the representation of different temporal rates of amplitude modulation in the complex speech signal. These temporal frequency bands yield complementary “windows” of information relating to cognitive linguistic units such as syllables (theta rate) and phonemes (gamma rate, see Poeppel, 2003). Accordingly, the TSF proposed that atypical oscillatory sampling at one or more temporal rates in children with dyslexia could cause phonological difficulties in specifying linguistic units such as syllables. Phonological difficulties in dyslexia are related to difficulties in the accurate perception of amplitude “rise time” (related to modulation rate). The TSF proposed that atypical oscillatory entrainment at syllable-relevant rates of amplitude modulation (delta [~ stressed syllable rate], theta [~ syllable rate]) could be one neural cause of the “phonological deficit” found in children and adults with dyslexia across languages and orthographies. This theory is about early developmental mechanisms, nevertheless impaired oscillatory sampling in auditory cortex could, over developmental time, lead to atypical functioning of the left-lateralized “reading network” identified in many fMRI studies of older children (Richlan, 2012, for a recent overview; Clark et al., 2014, for a relevant longitudinal study). This should be true across languages. Indeed, rise time perception is impaired in English, French, Spanish, Hungarian, Finnish, Chinese, and Dutch dyslexic children (see Goswami and Leong, 2013, for an overview). The “phonological deficit” in dyslexia is found in all of these languages, and manifests as difficulties in oral tasks such as recognizing prosodic stress, counting syllables, and counting or deleting phonemes (the smallest phonological units in a language; Ziegler and Goswami, 2005, for a cross-language review). These and other phonological tasks are considered by some of the auditory-based contributions to the special issue (Lehongre et al., 2013; Power et al., 2013; White-Schwoch and Kraus, 2013; Sela, 2014 this issue). The aim of this special issue, however, was to simultaneously invite colleagues who work on visual sensory processing to consider whether atypical oscillatory “temporal sampling” may explain the pervasive visual processing deficits in dyslexia reported in many orthographies (e.g., Facoetti et al., 2010; Lallier and Valdois, 2012). Visual and auditory sensory theories of dyslexia are typically considered to compete with each other, indeed a recent review counted 12 competing theories of developmental dyslexia (Ramus and Ahissar, 2012). The act of reading of course depends upon many visual processes. Examples are (for alphabetic orthographies) serial letter recognition, visual grouping of repeating letter patterns in familiar words, and the left-to-right (or in some orthographies, right-to-left) horizontal linear tracking of print. Practice in reading (reading experience) will obviously train the brain in aspects of visual processing related to reading. Such visual practice is necessarily reduced in children with dyslexia (reading is effortful, so the child reads less). Disentangling the effects of reading experience on the brain across the many different sensory and cognitive components that support the development of reading and writing is thus experimentally challenging. Nevertheless, by studying particular aspects of non-linguistic visual processing in isolation (such as magnocellular function, or eye movements), research can begin to disentangle cause from effect in developmental dyslexia. In this special issue, a number of the different aspects of impaired visual and visuo-spatial attentional processing found in dyslexia are studied and possible relations with oscillatory temporal sampling are considered (see De Luca et al., 2013; Lallier et al., 2013; Conlon et al., 2013; Gori et al., 2014; Ruffino et al., 2014; Varvara et al., 2014 this issue). Theoretically, these contributions consider whether spatiotemporal sampling of information by the visual system may be impaired in dyslexia (see Pammer, 2014; Vidyasagar, 2013 this issue). Indeed, Vidyasagar argues that a visual sampling impairment may be primary to the auditory difficulties in dyslexia documented by other contributors, a provocative claim which requires longitudinal studies. In fact, in order to establish the possible causal role of different visual and auditory sensory processes to reading development, and to identify their sequential contributions during the developmental learning trajectory, a range of developmental research designs are required. At minimum, evidence is required that: the sensory/neural deficit precedes being taught to read the sensory/neural deficit affects aspects of cognitive development other than reading (e.g., musical development for auditory deficits, conceptual development for visual deficits) in predictable ways the sensory/neural deficit can be demonstrated when children with dyslexia are compared to younger children whose reading skills are matched with the dyslexics (this research design aims to equate the effect of reading experience on the brain; the reading level match research design) developmental trajectories are followed in longitudinal studies, exploring the complex interplay of auditory and visual sensory/neural and cognitive processes during the development of reading, thereby establishing the developmental primacy of the candidate deficit the sensory/neural deficit is consistent across different languages and orthographies training the candidate deficit has demonstrable effects upon subsequent reading development Longitudinal studies, beginning before reading is taught and carried out across languages, are enormously important to the field (e.g., Boets et al., 2011; Franceschini et al., 2012). Sensory/neural deficits may change over developmental time. Perhaps a sensory factor critical for early development becomes less relevant when studying older children, or is no longer apparent when studying adults. Sensory/neural deficits may also manifest differently in different languages, for example as a consequence of factors such as orthographic grain size (e.g., the phonemic grain size is practiced by readers of alphabetic languages, whereas Japanese readers practice the syllable grain size) or phonology (e.g., rhythmic or phonetic differences, such as whether a language has many sonorant phonemes and is syllable-timed, such as Spanish, or many plosive phonemes and is stress-timed, such as English). Reading difficulties may be comorbid with other difficulties such as attention-deficit-hyperactivity disorder (ADHD); the possible effects of co-morbid disorders on sensory processing must be taken into account (Thaler et al., 2009). The studies in this special issue document and calibrate some of these aspects of auditory and visual processing that seem to be important in developmental dyslexia. Incorporating all of these aspects of sensory processing into oscillatory studies will be the next task for developmental research into dyslexia.

Sequential Versus Simultaneous Processing Deficits in Developmental Dyslexia

Despite the large number of studies conducted on developmental dyslexia, the cause(s) of the disorder still remain(s) unclear. Researchers in this field still struggle to understand the reason why abnormal reading acquisition occurs in children who receive appropriate environmental opportunities to achieve a good education, and present normal intellectual efficiency. This introduction will focus on the presentation of the phonological hypothesis, and then move onto the presentation of the visual attention span hypothesis, which predicts at least two proximal causes to developmental dyslexia. Setting the theoretical framework for these hypotheses will help to understand why sequential and simultaneous dimensions for visual and auditory processing may have independent roles to play in typical and atypical reading development.

Orthographic transparency modulates the grain size of orthographic processing: Behavioral and ERP evidence from bilingualism

Grapheme-to-phoneme mapping regularity is thought to determine the grain size of orthographic information extracted whilst encoding letter strings. Here we tested whether learning to read in two languages differing in their orthographic transparency yields different strategies used for encoding letter-strings as compared to learning to read in one (opaque) language only. Sixteen English monolingual and 16 early Welsh-English bilingual readers undergoing event-related brain potentials (ERPs) recordings were asked to report whether or not a target letter displayed at fixation was present in either a nonword (consonant string) or an English word presented immediately before. Bilinguals and monolinguals showed similar behavioural performance on target detection presented in words and nonwords, suggesting similar orthographic encoding in the two groups. By contrast, the amplitude of ERPs locked to the target letters (P3b, 340-570 ms post target onset, and a late frontal positive component 600-1,000 ms post target onset) were differently modulated by the position of the target letter in words and nonwords between bilinguals and monolinguals. P3b results show that bilinguals who learnt to read simultaneously in an opaque and a transparent orthographies encoded orthographic information presented to the right of fixation more poorly than monolinguals. On the opposite, only monolinguals exhibited a position effect on the late positive component for both words and nonwords, interpreted as a sign of better re-evaluation of their responses. The present study shed light on how orthographic transparency constrains grain size and visual strategies underlying letter-string encoding, and how those constraints are influenced by bilingualism.