Left ventral occipitotemporal activation during orthographic and semantic processing of auditory words.

The present fMRI study investigated the hypothesis that activation of the left ventral occipitotemporal cortex (vOT) in response to auditory words can be attributed to lexical orthographic rather than lexico-semantic processing. To this end, we presented auditory words in both an orthographic ("three or four letter word?") and a semantic ("living or nonliving?") task. In addition, a auditory control condition presented tones in a pitch evaluation task. The results showed that the left vOT exhibited higher activation for orthographic relative to semantic processing of auditory words with a peak in the posterior part of vOT. Comparisons to the auditory control condition revealed that orthographic processing of auditory words elicited activation in a large vOT cluster. In contrast, activation for semantic processing was only weak and restricted to the middle part vOT. We interpret our findings as speaking for orthographic processing in left vOT. In particular, we suggest that activation in left middle vOT can be attributed to accessing orthographic whole-word representations. While activation of such representations was experimentally ascertained in the orthographic task, it might have also occurred automatically in the semantic task. Activation in the more posterior vOT region, on the other hand, may reflect the generation of explicit images of word-specific letter sequences required by the orthographic but not the semantic task. In addition, based on cross-modal suppression, the finding of marked deactivations in response to the auditory tones is taken to reflect the visual nature of representations and processes in left vOT.

Visual Experience Shapes Orthographic Representations in the Visual Word Form Area.

Current neurocognitive research suggests that the efficiency of visual word recognition rests on abstract memory representations of written letters and words stored in the visual word form area (VWFA) in the left ventral occipitotemporal cortex. These representations are assumed to be invariant to visual characteristics such as font and case. In the present functional MRI study, we tested this assumption by presenting written words and varying the case format of the initial letter of German nouns (which are always capitalized) as well as German adjectives and adverbs (both usually in lowercase). As evident from a Word Type × Case Format interaction, activation in the VWFA was greater to words presented in unfamiliar case formats relative to familiar case formats. Our results suggest that neural representations of written words in the VWFA are not fully abstract and still contain information about the visual format in which words are most frequently perceived.

Resting-State and Task-Based Functional Brain Connectivity in Developmental Dyslexia.

Reading requires the interaction between multiple cognitive processes situated in distant brain areas. This makes the study of functional brain connectivity highly relevant for understanding developmental dyslexia. We used seed-voxel correlation mapping to analyse connectivity in a left-hemispheric network for task-based and resting-state fMRI data. Our main finding was reduced connectivity in dyslexic readers between left posterior temporal areas (fusiform, inferior temporal, middle temporal, superior temporal) and the left inferior frontal gyrus. Reduced connectivity in these networks was consistently present for 2 reading-related tasks and for the resting state, showing a permanent disruption which is also present in the absence of explicit task demands and potential group differences in performance. Furthermore, we found that connectivity between multiple reading-related areas and areas of the default mode network, in particular the precuneus, was stronger in dyslexic compared with nonimpaired readers.

Accessing orthographic representations from speech: the role of left ventral occipitotemporal cortex in spelling.

The present fMRI study used a spelling task to investigate the hypothesis that the left ventral occipitotemporal cortex (vOT) hosts neuronal representations of whole written words. Such an orthographic word lexicon is posited by cognitive dual-route theories of reading and spelling. In the scanner, participants performed a spelling task in which they had to indicate if a visually presented letter is present in the written form of an auditorily presented word. The main experimental manipulation distinguished between an orthographic word spelling condition in which correct spelling decisions had to be based on orthographic whole-word representations, a word spelling condition in which reliance on orthographic whole-word representations was optional and a phonological pseudoword spelling condition in which no reliance on such representations was possible. To evaluate spelling-specific activations the spelling conditions were contrasted with control conditions that also presented auditory words and pseudowords, but participants had to indicate if a visually presented letter corresponded to the gender of the speaker. We identified a left vOT cluster activated for the critical orthographic word spelling condition relative to both the control condition and the phonological pseudoword spelling condition. Our results suggest that activation of left vOT during spelling can be attributed to the retrieval of orthographic whole-word representations and, thus, support the position that the left vOT potentially represents the neuronal equivalent of the cognitive orthographic word lexicon.

Top-down and bottom-up influences on the left ventral occipito-temporal cortex during visual word recognition: an analysis of effective connectivity.

The functional role of the left ventral occipito-temporal cortex (vOT) in visual word processing has been studied extensively. A prominent observation is higher activation for unfamiliar but pronounceable letter strings compared to regular words in this region. Some functional accounts have interpreted this finding as driven by top-down influences (e.g., Dehaene and Cohen [2011]: Trends Cogn Sci 15:254-262; Price and Devlin [2011]: Trends Cogn Sci 15:246-253), while others have suggested a difference in bottom-up processing (e.g., Glezer et al. [2009]: Neuron 62:199-204; Kronbichler et al. [2007]: J Cogn Neurosci 19:1584-1594). We used dynamic causal modeling for fMRI data to test bottom-up and top-down influences on the left vOT during visual processing of regular words and unfamiliar letter strings. Regular words (e.g., taxi) and unfamiliar letter strings of pseudohomophones (e.g., taksi) were presented in the context of a phonological lexical decision task (i.e., "Does the item sound like a word?"). We found no differences in top-down signaling, but a strong increase in bottom-up signaling from the occipital cortex to the left vOT for pseudohomophones compared to words. This finding can be linked to functional accounts which assume that the left vOT contains neurons tuned to complex orthographic features such as morphemes or words [e.g., Dehaene and Cohen [2011]: Trends Cogn Sci 15:254-262; Kronbichler et al. [2007]: J Cogn Neurosci 19:1584-1594]: For words, bottom-up signals converge onto a matching orthographic representation in the left vOT. For pseudohomophones, the propagated signals do not converge, but (partially) activate multiple orthographic word representations, reflected in increased effective connectivity.

Structural abnormalities in the dyslexic brain: a meta-analysis of voxel-based morphometry studies.

We used coordinate-based meta-analysis in order to objectively quantify gray matter abnormalities reported in nine Voxel-Based Morphometry studies of developmental dyslexia. Consistently across studies, reduced gray matter volume in dyslexic readers was found in the right superior temporal gyrus and left superior temporal sulcus. These results were related to findings from previous meta-analyses on functional brain abnormalities in dyslexic readers. Convergence of gray matter reduction and reading-related underactivation was found for the left superior temporal sulcus. Recent studies point to the presence of both functional and structural abnormalities in left temporal and occipito-temporal brain regions before reading onset.

Meta-analyzing brain dysfunctions in dyslexic children and adults.

We examined the evidence from functional imaging studies for predominance of a phonological left temporo-parietal (TP) dysfunction in dyslexic children and predominance of a visual-orthographic left occipito-temporal (OT) dysfunction in dyslexic adults. Separate meta-analyses of 9 studies with children (age means: 9-11 years) and of 9 studies with adults (age means: 18-30 years) and statistical comparison of these meta-analytic maps did find support for a dysfunction of a left ventral OT region in both children and adults. The findings on a possible predominance of a left TP dysfunction in children were inconclusive. Contrary to expectation, underactivation in superior temporal regions was only found for adults, but not for children. For children, underactivation was found in bilateral inferior parietal regions, but this abnormality was no longer present when foci identified by higher dyslexic task-negative activation (i.e., deactivation in response to reading compared to baseline) were excluded. These meta-analytic results are consistent with recent findings speaking for an early engagement of left OT regions in reading development and for an early failure of such an engagement in dyslexia.

A dual-route perspective on brain activation in response to visual words: evidence for a length by lexicality interaction in the visual word form area (VWFA).

Based on our previous work, we expected the Visual Word Form Area (VWFA) in the left ventral visual pathway to be engaged by both whole-word recognition and by serial sublexical coding of letter strings. To examine this double function, a phonological lexical decision task (i.e., "Does xxx sound like an existing word?") presented short and long letter strings of words, pseudohomophones, and pseudowords (e.g., Taxi, Taksi and Tazi). Main findings were that the length effect for words was limited to occipital regions and absent in the VWFA. In contrast, a marked length effect for pseudowords was found throughout the ventral visual pathway including the VWFA, as well as in regions presumably engaged by visual attention and silent-articulatory processes. The length by lexicality interaction on brain activation corresponds to well-established behavioral findings of a length by lexicality interaction on naming latencies and speaks for the engagement of the VWFA by both lexical and sublexical processes.

Dyslexia in regular orthographies: manifestation and causation.

This article summarizes our research on the manifestation of dyslexia in German and on cognitive deficits, which may account for the severe reading speed deficit and the poor orthographic spelling performance that characterize dyslexia in regular orthographies. An only limited causal role of phonological deficits (phonological awareness, phonological STM, and rapid naming) for the emergence of reading fluency and spelling deficits is inferred from two large longitudinal studies with assessments of phonology before learning to read. A review of our cross-sectional studies provides no support for several cognitive deficits (visual-attention deficit, magnocellular dysfunction, skill automatization deficit, and visual-sequential memory deficit), which were proposed as alternatives to the phonological deficit account. Finally, a revised version of the phonological deficit account in terms of a dysfunction in orthographic-phonological connectivity is proposed.

Functional abnormalities in the dyslexic brain: a quantitative meta-analysis of neuroimaging studies.

This study used foci from 17 original studies on functional abnormalities in the dyslexic brain to identify brain regions with consistent under- or overactivation. Studies were included when reading or reading-related tasks were performed on visually presented stimuli and when results reported coordinates for group differences. Activation likelihood estimation (ALE) was used for quantification. Maxima of underactivation were found in inferior parietal, superior temporal, middle and inferior temporal, and fusiform regions of the left hemisphere. With respect to left frontal abnormalities, we found underactivation in the inferior frontal gyrus to be accompanied by overactivation in the primary motor cortex and the anterior insula. Tentative functional interpretations of the activation abnormalities are provided.

A dual-route perspective on poor reading in a regular orthography: evidence from phonological and orthographic lexical decisions.

Impairments of the lexical and the nonlexical reading route were examined for German-speaking dyslexic readers by measuring accuracy and speed of phonological and orthographic lexical decisions. Different from English-based findings, we found little difficulty with the phonological distinction between pseudohomophones and nonwords, but a major difficulty with the orthographic distinction between words and pseudohomophones. Subtyping identified pure surface dyslexia cases but no case of pure phonological dyslexia. Dyslexic speed impairments were traced to three loci in the dual-route model: an impoverished orthographic lexicon, and slow access from orthographic to phonological lexicon entries (lexical route) and from graphemes to phonemes (nonlexical route). A review of distal cognitive deficits suggested that the orthographic lexicon is affected by phonological deficits and that the slow functioning of the lexical and the nonlexical route reflects a general visual-verbal speed impairment and not a purely visual-attentional deficit.

Visual target detection is not impaired in dyslexic readers.

In two previous studies we assessed a difficulty of dyslexic readers with letter string processing by using variants of the partial report paradigm, e.g., Averbach and Coriell [Averbach, E., & Coriell, A. S. (1961). Short-term memory in vision. Bell Systems Technical Journal, 40, 309-328] which requires report of a letter name in response to a position cue. The poor dyslexic performance was interpreted as evidence for a visual-attentional deficit of dyslexic readers. In the present study, we avoided verbal report by using a task which only required the detection of predefined targets (letters or pseudoletters) in strings. On this purely visual task, the dyslexic readers did not differ from non-impaired readers. This finding speaks against a basic visual-attentional deficit; rather it suggests that the dyslexic deficit on partial report paradigms stems from a problem in establishing a string representation which includes position and name codes.

Perhaps correlational but not causal: no effect of dyslexic readers' magnocellular system on their eye movements during reading.

During reading, dyslexic readers exhibit more and longer fixations and a higher percentage of regressions than normal readers. It is still a matter of debate, whether these divergent eye movement patterns of dyslexic readers reflect an underlying problem in word processing or whether they are - as the proponents of the magnocellular deficit hypothesis claim - associated with deficient visual perception that is causal for dyslexia. To overcome problems in the empirical linkage of the magnocellular theory with reading, a string processing task is presented that poses similar demands on visual perception (in terms of letter identification) and oculomotor control as reading does. Two experiments revealed no differences in the eye movement patterns of dyslexic and control readers performing this task. Furthermore, no relationship between the functionality of the participants' magnocellular system assessed by the coherent motion task and string processing were found. The perceptual and oculomotor demands required during string processing were functionally equivalent to those during reading and the presented consonant strings had similar visual characteristics as reading material. Thus, a strong inference can be drawn: Dyslexic readers do not seem to have difficulties with the accurate perception of letters and the control of their eye movements during reading - their reading difficulties therefore cannot be explained in terms of oculomotor and visuo-perceptual problems.

Evidence for a dysfunction of left posterior reading areas in German dyslexic readers.

The brain activity during a sentence reading task and a visual control task was examined with fMRI in 13 German dyslexic readers and 15 age-matched fluent readers (age: 14-16 years). These participants came from a longitudinal study and the dyslexic readers exhibited a persistent reading fluency deficit from early on. For the first time with German dyslexic readers, and in correspondence with the majority of functional imaging studies, we found reduced dyslexic activation in the left occipitotemporal cortex and in a small region of the left supramarginal gyrus. Enhanced activation was found in left inferior frontal and subcortical regions.

Impaired visual processing of letter and digit strings in adult dyslexic readers.

The slow word reading of developmental dyslexics may stem from a string processing impairment which in turn reflects visual attentional deficits. We indeed found substantially enhanced recognition time thresholds in the dyslexic adult readers. However, their position profiles were hard to reconcile with any of the discussed visual attentional deficit hypotheses and with the prediction that dyslexic readers suffer from an absent string processing system as they exhibited similar M-shaped position profiles for digit and letter strings as the normal reading controls.

Impaired visual processing of multi-element arrays is associated with increased number of eye movements in dyslexic reading.

For assessing simultaneous visual processing in dyslexic and normal readers a multi-element processing task was used which required the report of a single digit of briefly presented multi-digit arrays. Dyslexic readers exhibited higher recognition thresholds on 4- and 6-digit, but not on 2-digit arrays. Individual recognition thresholds on the multi-digit arrays were associated with number of eye movements during reading. The dyslexic multi-element processing deficit was not accompanied by deficient coherent motion detection or deficient visual precedence detection and was independent from deficits in phonological awareness and rapid naming. However, only about half of the dyslexic readers exhibited a multi-element processing deficit.

No deficits at the point of hemispheric indecision.

This study attempted to replicate a recent finding by Crow et al. [Neuropsychologia 36 (1998) 1275] showing that about equal skill of right and left hand (i.e. hemispheric indecision) is associated with deficits in cognitive and scholastic achievement. The present study assessed hemispheric indecision by using Annett's [Left, Right, Hand and Brain: The Right Shift Theory, Lawrence Erlbaum, London, 1985] peg moving test and by assessing the consistency of hand preference at school entrance. Non-verbal intelligence, reading and spelling accuracy were assessed about three years later. The sample consisted of 530 boys. Contrary to Crow et al., children with about equal hand skill did not show deficits in non-verbal intelligence, reading and spelling. Also, there were no deficits when inconsistent hand preference was taken as indication of hemispheric indecision. The findings cast doubt on the hemispheric indecision hypothesis and speak specifically against Orton's [Reading, Writing and Speech Problems in Children, Norton, New York, 1937] position, revived by Crow et al., that delayed or absent hemispheric dominance may lead to difficulties with the acquisition of reading and spelling.

On the automaticity/cerebellar deficit hypothesis of dyslexia: balancing and continuous rapid naming in dyslexic and ADHD children.

The present study examined the relationship of reading disability (RD) and attention deficit hyperactivity disorder (ADHD) to balancing problems. In the cerebellar deficit hypothesis of dyslexia of Nicolson et al. [Trends Neurosci. 24 (2001) 508], balancing problems are taken as sign of a cerebellar deficit and were found to be associated with dyslexia. Four groups of 10 children each, representing all combinations of RD (absent versus present) and ADHD (absent versus present), were included. However, poor balancing (assessed both singly and together with a secondary task) was not found to be associated with RD, but with ADHD. In contrast, poor performance on continuous rapid naming tasks (digit and color naming) was found to be associated with RD and not with ADHD.

Do current connectionist learning models account for reading development in different languages?

Learning to read a relatively irregular orthography, such as English, is harder and takes longer than learning to read a relatively regular orthography, such as German. At the end of grade 1, the difference in reading performance on a simple set of words and nonwords is quite dramatic. Whereas children using regular orthographies are already close to ceiling, English children read only about 40% of the words and nonwords correctly. It takes almost 4 years for English children to come close to the reading level of their German peers. In the present study, we investigated to what extent recent connectionist learning models are capable of simulating this cross-language learning rate effect as measured by nonword decoding accuracy. We implemented German and English versions of two major connectionist reading models, Plaut et al.'s (Plaut, D. C., McClelland, J. L., Seidenberg, M. S., & Patterson, K. (1996). Understanding normal and impaired word reading: computational principles in quasi-regular domains. Psychological Review, 103, 56-115) parallel distributed model and Zorzi et al.'s (Zorzi, M., Houghton, G., & Butterworth, B. (1998a). Two routes or one in reading aloud? A connectionist dual-process model. Journal of Experimental Psychology: Human Perception and Performance, 24, 1131-1161); two-layer associative network. While both models predicted an overall advantage for the more regular orthography (i.e. German over English), they failed to predict that the difference between children learning to read regular versus irregular orthographies is larger earlier on. Further investigations showed that the two-layer network could be brought to simulate the cross-language learning rate effect when cross-language differences in teaching methods (phonics versus whole-word approach) were taken into account. The present work thus shows that in order to adequately capture the pattern of reading acquisition displayed by children, current connectionist models must not only be sensitive to the statistical structure of spelling-to-sound relations but also to the way reading is taught in different countries.

When does the brain register deviances from standard word spellings?--An ERP study.

Event-related potentials (ERPs) in response to the standard form of words (e.g., taxi) were compared with ERPs in response to letter-altered (e.g., taksi) or case-altered forms (e.g., taXi). The altered forms always resulted in the same reading as the standard forms. First divergences between ERPs were found at around 160 ms. At occipital sites, the peak amplitude of the N160 was higher for standard than letter-altered strings. At frontal and central sites, the standard strings diverged from the altered strings persistently by higher positivity from about 160 ms onwards. These early ERP differences between standard and altered visual word forms speak for early contact between the letter input and stored visual-orthographic representations of words.