How interindividual differences in brain anatomy shape reading accuracy.

The capacity to read develops throughout intensive academic learning and training. Several studies have investigated the impact of reading on the brain, and particularly how the anatomy of the brain changes with reading acquisition. In the present study, we investigated the converse issue, namely whether and how reading acquisition is constrained by the anatomy of the brain. Using multimodal MRI, we found that (a) the pattern (continuous or interrupted sulcus) of the posterior part of the left lateral occipito-temporal sulcus (OTS) hosting the visual word form area (VWFA) predicts reading skills in adults; that (b) this effect is modulated by the age of reading acquisition; and that (c) the length of the OTS sulcal interruption is associated with reading skills. Because the sulcal pattern is determined in utero, our findings suggest that individual difference in reading skills can be traced back to early stages of brain development in addition to the well-established socioeconomic and educational factors.

Numerical abilities of school-age children with Developmental Coordination Disorder (DCD): A behavioral and eye-tracking study.

Developmental Coordination Disorder (DCD) is a disorder of motor coordination which interferes with academic achievement. Difficulties in mathematics have been reported. Performance in the number line task is very sensitive to atypical development of numerical cognition. We used a position-to-number task in which twenty 7-to-10years old children with DCD and 20 age-matched typically developing (TD) children had to estimate the number that corresponded to a hatch mark placed on a 0-100 number line. Eye movements were recorded. Children with DCD were less accurate and slower to respond than their peers. However, they were able to map numbers onto space linearly and used anchoring strategies as control. We suggest that the shift to a linear trend reflects the ability of DCD children to use efficient strategies to solve the task despite a possibly more imprecise underlying numerical acuity.

Mathematical difficulties in developmental coordination disorder: Symbolic and nonsymbolic number processing.

At school, children with Developmental Coordination Disorder (DCD) struggle with mathematics. However, little attention has been paid to their numerical cognition abilities. The goal of this study was to better understand the cognitive basis for mathematical difficulties in children with DCD. Twenty 7-to-10 years-old children with DCD were compared to twenty age-matched typically developing children using dot and digit comparison tasks to assess symbolic and nonsymbolic number processing and in a task of single digits additions. Results showed that children with DCD had lower performance in nonsymbolic and symbolic number comparison tasks than typically developing children. They were also slower to solve simple addition problems. Moreover, correlational analyses showed that children with DCD who experienced greater impairments in the nonsymbolic task also performed more poorly in the symbolic tasks. These findings suggest that DCD impairs both nonsymbolic and symbolic number processing. A systematic assessment of numerical cognition in children with DCD could provide a more comprehensive picture of their deficits and help in proposing specific remediation.

Adaptation of the human visual system to the statistics of letters and line configurations.

By adulthood, literate humans have been exposed to millions of visual scenes and pages of text. Does the human visual system become attuned to the statistics of its inputs? Using functional magnetic resonance imaging, we examined whether the brain responses to line configurations are proportional to their natural-scene frequency. To further distinguish prior cortical competence from adaptation induced by learning to read, we manipulated whether the selected configurations formed letters and whether they were presented on the horizontal meridian, the familiar location where words usually appear, or on the vertical meridian. While no natural-scene frequency effect was observed, we observed letter-status and letter frequency effects on bilateral occipital activation, mainly for horizontal stimuli. The findings suggest a reorganization of the visual pathway resulting from reading acquisition under genetic and connectional constraints. Even early retinotopic areas showed a stronger response to letters than to rotated versions of the same shapes, suggesting an early visual tuning to large visual features such as letters.

Timing the impact of literacy on visual processing.

Learning to read requires the acquisition of an efficient visual procedure for quickly recognizing fine print. Thus, reading practice could induce a perceptual learning effect in early vision. Using functional magnetic resonance imaging (fMRI) in literate and illiterate adults, we previously demonstrated an impact of reading acquisition on both high- and low-level occipitotemporal visual areas, but could not resolve the time course of these effects. To clarify whether literacy affects early vs. late stages of visual processing, we measured event-related potentials to various categories of visual stimuli in healthy adults with variable levels of literacy, including completely illiterate subjects, early-schooled literate subjects, and subjects who learned to read in adulthood (ex-illiterates). The stimuli included written letter strings forming pseudowords, on which literacy is expected to have a major impact, as well as faces, houses, tools, checkerboards, and false fonts. To evaluate the precision with which these stimuli were encoded, we studied repetition effects by presenting the stimuli in pairs composed of repeated, mirrored, or unrelated pictures from the same category. The results indicate that reading ability is correlated with a broad enhancement of early visual processing, including increased repetition suppression, suggesting better exemplar discrimination, and increased mirror discrimination, as early as ∼ 100-150 ms in the left occipitotemporal region. These effects were found with letter strings and false fonts, but also were partially generalized to other visual categories. Thus, learning to read affects the magnitude, precision, and invariance of early visual processing.

Effects of literacy in early visual and occipitotemporal areas of Chinese and French readers.

How does reading expertise change the visual system? Here, we explored whether the visual system could develop dedicated perceptual mechanisms in early and intermediate visual cortex under the pressure for fast processing that is particularly strong in reading. We compared fMRI activations in Chinese participants with limited knowledge of French and in French participants with no knowledge of Chinese, exploiting these doubly dissociated reading skills as a tool to study the neural correlates of visual expertise. All participants viewed the same stimuli: words in both languages and matched visual controls, presented at a fast rate comparable with fluent reading. In the Visual Word Form Area, all participants showed enhanced responses to their known scripts. However, group differences were found in occipital cortex. In French readers reading French, activations were enhanced in left-hemisphere visual area V1, with the strongest differences between French words and their controls found at the central and horizontal meridian representations. Chinese participants, who were not expert French readers, did not show these early visual activations. In contrast, Chinese readers reading Chinese showed enhanced activations in intermediate visual areas V3v/hV4, absent in French participants. Together with our previous findings [Szwed, M., Dehaene, S., Kleinschmidt, A., Eger, E., Valabregue, R., Amadon, A., et al. Specialization for written words over objects in the visual cortex. Neuroimage, 56, 330-344, 2011], our results suggest that the effects of extensive practice can be found at the lowest levels of the visual system. They also reveal their cross-script variability: Alphabetic reading involves enhanced engagement of central and right meridian V1 representations that are particularly used in left-to-right reading, whereas Chinese characters put greater emphasis on intermediate visual areas.

Literacy breaks mirror invariance for visual stimuli: a behavioral study with adult illiterates.

The ability to recognize 2 mirror images as the same picture across left-right inversions exists early on in humans and other primates. In order to learn to read, however, one must discriminate the left-right orientation of letters and distinguish, for instance, b from d. We therefore reasoned that literacy may entail a loss of mirror invariance. To evaluate this hypothesis, we asked adult literates, illiterates, and ex-illiterates to perform a speeded same-different task with letter strings, false fonts, and pictures regardless of their orientation (i.e., they had to respond "same" to mirror pairs such as "iblo oldi"). Literates presented clear difficulties with mirror invariance. This "mirror cost" effect was strongest with letter strings, but crucially, it was also observed with false fonts and even with pictures. In contrast, illiterates did not present any cost for mirror pairs. Interestingly, subjects who learned to read as adults also exhibited a mirror cost, suggesting that modest reading practice, late in life, can suffice to break mirror invariance.

The cortical representation of simple mathematical expressions.

Written mathematical notation conveys, in a compact visual form, the nested functional relations among abstract concepts such as operators, numbers or sets. Is the comprehension of mathematical expressions derived from the human capacity for processing the recursive structure of language? Or does algebraic processing rely only on a language-independent network, jointly involving the visual system for parsing the string of mathematical symbols and the intraparietal system for representing numbers and operators? We tested these competing hypotheses by scanning mathematically trained adults while they viewed simple strings ranging from randomly arranged characters to mathematical expressions with up to three levels of nested parentheses. Syntactic effects were observed in behavior and in brain activation measured with functional magnetic resonance imaging (fMRI) and magneto-encephalography (MEG). Bilateral occipito-temporal cortices and right parietal and precentral cortices appeared as the primary nodes for mathematical syntax. MEG estimated that a mathematical expression could be parsed by posterior visual regions in less than 180 ms. Nevertheless, a small increase in activation with increasing expression complexity was observed in linguistic regions of interest, including the left inferior frontal gyrus and the posterior superior temporal sulcus. We suggest that mathematical syntax, although arising historically from language competence, becomes "compiled" into visuo-spatial areas in well-trained mathematics students.

How learning to read changes the cortical networks for vision and language.

Does literacy improve brain function? Does it also entail losses? Using functional magnetic resonance imaging, we measured brain responses to spoken and written language, visual faces, houses, tools, and checkers in adults of variable literacy (10 were illiterate, 22 became literate as adults, and 31 were literate in childhood). As literacy enhanced the left fusiform activation evoked by writing, it induced a small competition with faces at this location, but also broadly enhanced visual responses in fusiform and occipital cortex, extending to area V1. Literacy also enhanced phonological activation to speech in the planum temporale and afforded a top-down activation of orthography from spoken inputs. Most changes occurred even when literacy was acquired in adulthood, emphasizing that both childhood and adult education can profoundly refine cortical organization.

Why do children make mirror errors in reading? Neural correlates of mirror invariance in the visual word form area.

Young children often make mirror errors when learning to read and write, for instance writing their first name from right to left in English. This competence vanishes in most adult readers, who typically cannot read mirror words but retain a strong competence for mirror recognition of images. We used fast behavioral and fMRI repetition priming to probe the brain mechanisms underlying mirror generalization and its absence for words in adult readers. In two groups of French and Japanese readers, we show that the left fusiform visual word form area, a major site of learning during reading acquisition, simultaneously shows a maximal effect of mirror priming for pictures and an absence of mirror priming for words. Thus, learning to read recruits an area which possesses a property of mirror invariance, seemingly present in all primates, which is deleterious for letter recognition and may explain children's transient mirror errors.

Reading normal and degraded words: contribution of the dorsal and ventral visual pathways.

Fast, parallel word recognition, in expert readers, relies on sectors of the left ventral occipito-temporal pathway collectively known as the visual word form area. This expertise is thought to arise from perceptual learning mechanisms that extract informative features from the input strings. The perceptual expertise hypothesis leads to two predictions: (1) parallel word recognition, based on the ventral visual system, should be limited to words displayed in a familiar format (foveal horizontal words with normally spaced letters); (2) words displayed in formats outside this field of expertise should be read serially, under supervision of dorsal parietal attention systems. We presented adult readers with words that were progressively degraded in three different ways (word rotation, letter spacing, and displacement to the visual periphery). Behaviorally, we identified degradation thresholds above which reading difficulty increased non-linearly, with the concomitant emergence of a word length effect on reading latencies reflecting serial reading strategies. fMRI activations were correlated with reading difficulty in bilateral occipito-temporal and parietal regions, reflecting the strategies required to identify degraded words. A core region of the intraparietal cortex was engaged in all modes of degradation. Furthermore, in the ventral pathway, word degradation led to an amplification of activation in the posterior visual word form area, at a level thought to encode single letters. We also found an effect of word length restricted to highly degraded words in bilateral occipitoparietal regions. Those results clarify when and how the ventral parallel visual word form system needs to be supplemented by the deployment of dorsal serial reading strategies.

Task-specific change of unconscious neural priming in the cerebral language network.

We explored the impact of task context on subliminal neural priming using functional magnetic resonance imaging. The repetition of words during semantic categorization produced activation reduction in the left middle temporal gyrus previously associated with semantic-level representation and dorsal premotor cortex. By contrast, reading aloud produced repetition enhancement in the left inferior parietal lobe associated with print-to-sound conversion and ventral premotor cortex. Analyses of effective connectivity revealed that the task set for reading generated reciprocal excitatory connections between the left inferior parietal and superior temporal regions, reflecting the audiovisual integration required for vocalization, whereas categorization did not produce such backward projection to posterior regions. Thus, masked repetition priming involves two distinct components in the task-specific neural streams, one in the parietotemporal cortex for task-specific word processing and the other in the premotor cortex for behavioral response preparation. The top-down influence of task sets further changes the directions of the unconscious priming in the entire cerebral circuitry for reading.

Fast reproducible identification and large-scale databasing of individual functional cognitive networks.

BACKGROUND: Although cognitive processes such as reading and calculation are associated with reproducible cerebral networks, inter-individual variability is considerable. Understanding the origins of this variability will require the elaboration of large multimodal databases compiling behavioral, anatomical, genetic and functional neuroimaging data over hundreds of subjects. With this goal in mind, we designed a simple and fast acquisition procedure based on a 5-minute functional magnetic resonance imaging (fMRI) sequence that can be run as easily and as systematically as an anatomical scan, and is therefore used in every subject undergoing fMRI in our laboratory. This protocol captures the cerebral bases of auditory and visual perception, motor actions, reading, language comprehension and mental calculation at an individual level. RESULTS: 81 subjects were successfully scanned. Before describing inter-individual variability, we demonstrated in the present study the reliability of individual functional data obtained with this short protocol. Considering the anatomical variability, we then needed to correctly describe individual functional networks in a voxel-free space. We applied then non-voxel based methods that automatically extract main features of individual patterns of activation: group analyses performed on these individual data not only converge to those reported with a more conventional voxel-based random effect analysis, but also keep information concerning variance in location and degrees of activation across subjects. CONCLUSION: This collection of individual fMRI data will help to describe the cerebral inter-subject variability of the correlates of some language, calculation and sensorimotor tasks. In association with demographic, anatomical, behavioral and genetic data, this protocol will serve as the cornerstone to establish a hybrid database of hundreds of subjects suitable to study the range and causes of variation in the cerebral bases of numerous mental processes.

Hierarchical coding of letter strings in the ventral stream: dissecting the inner organization of the visual word-form system.

Visual word recognition has been proposed to rely on a hierarchy of increasingly complex neuronal detectors, from individual letters to bigrams and morphemes. We used fMRI to test whether such a hierarchy is present in the left occipitotemporal cortex, at the site of the visual word-form area, and with an anterior-to-posterior progression. We exposed adult readers to (1) false-font strings; (2) strings of infrequent letters; (3) strings of frequent letters but rare bigrams; (4) strings with frequent bigrams but rare quadrigrams; (5) strings with frequent quadrigrams; (6) real words. A gradient of selectivity was observed through the entire span of the occipitotemporal cortex, with activation becoming more selective for higher-level stimuli toward the anterior fusiform region. A similar gradient was also seen in left inferior frontoinsular cortex. Those gradients were asymmetrical in favor of the left hemisphere. We conclude that the left occipitotemporal visual word-form area, far from being a homogeneous structure, presents a high degree of functional and spatial hierarchical organization which must result from a tuning process during reading acquisition.

Dynamics of prefrontal and cingulate activity during a reward-based logical deduction task.

We used behavioral and functional magnetic resonance imaging (fMRI) methods to probe the cerebral organization of a simple logical deduction process. Subjects were engaged in a motor trial-and-error learning task, in which they had to infer the identity of an unknown 4-key code. The design of the task allowed subjects to base their inferences not only on the feedback they received but also on the internal deductions that it afforded (autoevaluation). fMRI analysis revealed a large bilateral parietal, prefrontal, cingulate, and striatal network that activated suddenly during search periods and collapsed during ensuing periods of sequence repetition. Fine-grained analyses of the temporal dynamics of this search network indicated that it operates according to near-optimal rules that include 1) computation of the difference between expected and obtained rewards and 2) anticipatory deductions that predate the actual reception of positive reward. In summary, the dynamics of effortful mental deduction can be tracked with fMRI and relate to a distributed network engaging prefrontal cortex and its interconnected cortical and subcortical regions.

Cerebral bases of subliminal and supraliminal priming during reading.

Several studies have investigated the neural correlates of conscious perception by contrasting functional magnetic resonance imaging (fMRI) activation to conscious and nonconscious visual stimuli. The results often reveal an amplification of posterior occipito-temporal activation and its extension into a parieto-frontal network. However, some of these effects might be due to a greater deployment of attentional or strategical processes in the conscious condition. Here, we examined the brain activity evoked by visible and invisible stimuli, both of which were irrelevant to the task. We collected fMRI data in a masking paradigm in which subliminal versus supraliminal letter strings were presented as primes while subjects focused attention on another subsequent, highly visible target word. Under those conditions, prime visibility was associated with greater activity confined to bilateral posterior occipito-temporal cortices, without extension into frontal and parietal cortices. However, supraliminal primes, compared with subliminal primes, evoked more extensive repetition suppression in a widely distributed set of parieto-frontal areas. Furthermore, only supraliminal primes caused phonological repetition enhancement in left inferior frontal and anterior insular cortex. Those results suggest a 2-stage view of conscious access: Relative to masked stimuli, unmasked stimuli elicit increased occipito-temporal activity, thus allowing them to compete for global conscious access and to induce priming in multiple distant areas. In the absence of attention, however, their access to a second stage of distributed parieto-frontal processing may remain blocked.

Functional segregation of cortical language areas by sentence repetition.

The functional organization of the perisylvian language network was examined using a functional MRI (fMRI) adaptation paradigm with spoken sentences. In Experiment 1, a given sentence was presented every 14.4 s and repeated two, three, or four times in a row. The study of the temporal properties of the BOLD response revealed a temporal gradient along the dorsal-ventral and rostral-caudal directions: From Heschl's gyrus, where the fastest responses were recorded, responses became increasingly slower toward the posterior part of the superior temporal gyrus and toward the temporal poles and the left inferior frontal gyrus, where the slowest responses were observed. Repetition induced a decrease in amplitude and a speeding up of the BOLD response in the superior temporal sulcus (STS), while the most superior temporal regions were not affected. In Experiment 2, small blocks of six sentences were presented in which either the speaker voice or the linguistic content of the sentence, or both, were repeated. Data analyses revealed a clear asymmetry: While two clusters in the left superior temporal sulcus showed identical repetition suppression whether the sentences were produced by the same speaker or different speakers, the homologous right regions were sensitive to sentence repetition only when the speaker voice remained constant. Thus, hemispheric left regions encode linguistic content while homologous right regions encode more details about extralinguistic features like speaker voice. The results demonstrate the feasibility of using sentence-level adaptation to probe the functional organization of cortical language areas.

Subliminal convergence of Kanji and Kana words: further evidence for functional parcellation of the posterior temporal cortex in visual word perception.

Recent evidence has suggested that the human occipitotemporal region comprises several subregions, each sensitive to a distinct processing level of visual words. To further explore the functional architecture of visual word recognition, we employed a subliminal priming method with functional magnetic resonance imaging (fMRI) during semantic judgments of words presented in two different Japanese scripts, Kanji and Kana. Each target word was preceded by a subliminal presentation of either the same or a different word, and in the same or a different script. Behaviorally, word repetition produced significant priming regardless of whether the words were presented in the same or different script. At the neural level, this cross-script priming was associated with repetition suppression in the left inferior temporal cortex anterior and dorsal to the visual word form area hypothesized for alphabetical writing systems, suggesting that cross-script convergence occurred at a semantic level. fMRI also evidenced a shared visual occipito-temporal activation for words in the two scripts, with slightly more mesial and right-predominant activation for Kanji and with greater occipital activation for Kana. These results thus allow us to separate script-specific and script-independent regions in the posterior temporal lobe, while demonstrating that both can be activated subliminally.

Neural correlates of switching from auditory to speech perception.

Many people exposed to sinewave analogues of speech first report hearing them as electronic glissando and, later, when they switch into a 'speech mode', hearing them as syllables. This perceptual switch modifies their discrimination abilities, enhancing perception of differences that cross phonemic boundaries while diminishing perception of differences within phonemic categories. Using high-density evoked potentials and fMRI in a discrimination paradigm, we studied the changes in brain activity that are related to this change in perception. With ERPs, we observed that phonemic coding is faster than acoustic coding: The electrophysiological mismatch response (MMR) occurred earlier for a phonemic change than for an equivalent acoustic change. The MMR topography was also more asymmetric for a phonemic change than for an acoustic change. In fMRI, activations were also significantly asymmetric, favoring the left hemisphere in both perception modes. Furthermore, switching to the speech mode significantly enhanced activation in the posterior parts of the left superior gyrus and sulcus relative to the non-speech mode. When responses to a change of stimulus were studied, a cluster of voxels in the supramarginal gyrus was activated significantly more by a phonemic change than by an acoustic change. These results demonstrate that phoneme perception in adults relies on a specific and highly efficient left-hemispheric network, which can be activated in top-down fashion when processing ambiguous speech/non-speech stimuli.