Processing symbols in the ventral visual cortex : functional architecture and anatomical constraints

Le cortex visuel ventral chez l’homme se compose d’une mosaïque de régions spécialisées dans la reconnaissance de différentes catégories d’objets. Selon une organisation reproductible, certaines régions répondent préférentiellement aux visages, alors que d’autres sont plus activées par les maisons et les lieux, par les outils, ou encore par les parties du corps. Plusieurs facteurs ont été invoqués pour expliquer la préférence d’une région pour une catégorie donnée, tels que des biais pour le traitement de certaines caractéristiques visuelles (préférence pour la position fovéale ou périphérique des stimuli, pour leur fréquence spatiale haute ou basse), le degré d’exposition et d’expertise (expertise pour les voitures par exemple), ou la connectivité anatomique vers des réseaux cérébraux spécialisés dans le traitement d’un domaine particulier. Chez les enfants, l’apprentissage de la lecture de mots ou d’autres systèmes symboliques culturels provoque le développement de régions corticales dédiées, telles que l’aire de la forme visuelle des mots (VWFA), au sein d’une voie ventrale en partie déjà stabilisée. Ce développement ontologique tardif pour la reconnaissance de symboles, indépendamment de contraintes phylogénétiques propres à la lecture, facilite l’étude de ce qui façonne la spécialisation fonctionnelle au sein de la voie ventrale. Dans cette thèse, nous avons étudié la représentation des mots et des partitions de musique au sein du cortex visuel ventral en combinant des méthodes d’imagerie par résonance magnétique fonctionnelle et de diffusion, à des taches comportementales. D’abord, nous montrons que la localisation de la VWFA chez les adultes correspond, en comparaison à des régions voisines du cortex ventral, à une région connectée de manière optimale à celles du langage qui traitent le contenu sémantique et phonologique. Ensuite, nous montrons que les régions ventrales qui sous-tendent le décodage orthographique sont fonctionnellement hétérogènes selon un axe latero-médial. Les régions médianes semblent encoder les graphèmes de façon sérielle, sous le contrôle de régions pariétales, pour les convertir en phonèmes. A l’inverse, les régions latérales traitent les mots de façon plus flexible pour accéder au lexique. Ces études mettent en évidence le rôle majeur de la connectivité anatomique dans le développement d’une spécialisation fonctionnelle pour les mots, avec la contribution de connectivités diverses qui participent à l’hétérogénéité fonctionnelle du système de la forme visuelle des mots. Enfin, nous observons que la maîtrise de la lecture musicale a d’importantes conséquences sur la latéralisation ventrale d’autres catégories. D’une part, la latéralisation à gauche augmente dans des régions latérales ventrales pour toutes les catégories. D’autre part, la latéralisation à droite augmente dans des régions fusiformes postérieures, notamment pour le traitement des visages et des maisons. Ces conséquences, similaires à celles provoquées par l’apprentissage de la lecture de mots, révèlent des processus à la fois de compétition et de transfert entre catégories. Ainsi, nos résultats suggèrent que des mécanismes communs pourraient expliquer comment une expertise culturelle peut recycler et modifier le cortex visuel.The human ventral visual cortex hosts a mosaic of areas specialized in the recognition of different categories of objects. According to a reproducible pattern, some areas respond preferentially to faces, while others are more activated by places and buildings, by tools, or by body parts. Several factors have been proposed as major determinants of the preferred category of a given region, such as visual feature biases (preference for peripheral vs. foveal stimuli, or for high vs. low spatial frequencies), experience (e.g., car expertise) and white-matter connectivity to domain-specific brain networks. In children, learning to read words and other cultural symbols triggers the emergence of dedicated cortical areas, such as the visual word form area (VWFA), within a partially settled ventral pathway. This late ontological development for symbol recognition, free from reading-specific evolutionary constraints, facilitates the investigation of what shapes functional specialization in the ventral pathway. In the current work, we studied in particular the representation of words and musical scores in the ventral visual cortex, using functional magnetic resonance imaging (fMRI), diffusion-weighted imaging and behavioral tasks. First, we show that the location of the VWFA in adults corresponds to a region optimally connected to language regions supporting semantics and phonology, as compared to adjacent ventral cortex regions. Second, we demonstrate that ventral regions supporting orthographic decoding are heterogeneous along a medial-to-lateral axis. Medial regions seem to encode graphemes serially for phonological decoding, under the control of parietal regions. In contrast, lateral regions process words more flexibly for lexical access. These studies reveal a major role of white-matter connectivity in shaping functional specialization for words, with differential connections participating in the functional heterogeneity of the VWFA. Third, we observe that musical literacy has a large impact on lateralization patterns in the ventral stream. A domain general enhancement of leftward lateralization takes place in lateral ventral regions, together with a rightward shift in fusiform regions notably for the processing of faces and houses. These consequences probably reflect both competition between visual categories and transfer across them, and resemble the impact of reading acquisition. Together, our results show that common processes may explain how cultural expertise recycles and modifies the visual cortex

A mesial-to-lateral dissociation for orthographic processing in the visual cortex

International audienceEfficient reading requires a fast conversion of the written word to both phonological and semantic codes. We tested the hypothesis that, within the left occipitotemporal cortical regions involved in visual word recognition, distinct subregions harbor slightly different orthographic codes adapted to those 2 functions. While the lexico-semantic pathway may operate on letter or open-bigram information, the phonological pathway requires the identification of multiletter graphemes such as "ch" or "ou" in order to map them onto phonemes. To evaluate the existence of a specific stage of graphemic encoding, 20 adults performed lexical decision and naming tasks on words and pseudowords during functional MRI. Graphemic encoding was facilitated or disrupted by coloring and spacing the letters either congruently with multiletter graphemes (ch-ai-r) or incongruently with them (c-ha-ir). This manipulation affected behavior, primarily during the naming of pseudowords, and modulated brain activity in the left midfusiform sulcus, at a site medial to the classical visual word form area (VWFA). This putative grapheme-related area (GRA) differed from the VWFA in being preferentially connected functionally to dorsal parietal areas involved in letter-by-letter reading, while the VWFA showed effects of lexicality and spelling-to-sound regularity. Our results suggest a partial dissociation within left occipitotemporal cortex: the midfusiform GRA would encode orthographic information at a sublexical graphemic level, while the lateral occipitotemporal VWFA would contribute primarily to direct lexico-semantic access

Reading music and words: The anatomical connectivity of musicians’ visual cortex

International audienceMusical score reading and word reading have much in common, from their historical origins to their cognitive foundations and neural correlates. In the ventral occipitotemporal cortex (VOT), the specialization of the so-called Visual Word Form Area for word reading has been linked to its privileged structural connectivity to distant language regions. Here we investigated how anatomical connectivity relates to the segregation of regions specialized for musical notation or words in the VOT. In a cohort of professional musicians and non-musicians, we used probabilistic tractography combined with task-related functional MRI to identify the connections of individually defined word- and music-selective left VOT regions. Despite their close proximity, these regions differed significantly in their structural connectivity, irrespective of musical expertise. The music-selective region was significantly more connected to posterior lateral temporal regions than the word-selective region, which, conversely, was significantly more connected to anterior ventral temporal cortex. Furthermore, musical expertise had a double impact on the connectivity of the music region. First, music tracts were significantly larger in musicians than in non-musicians, associated with marginally higher connectivity to perisylvian music-related areas. Second, the spatial similarity between music and word tracts was significantly increased in musicians, consistently with the increased overlap of language and music functional activations in musicians, as compared to non-musicians. These results support the view that, for music as for words, very specific anatomical connections influence the specialization of distinct VOT areas, and that reciprocally those connections are selectively enhanced by the expertise for word or music reading

Connectivity between the visual word form area and the parietal lobe improves after the first year of reading instruction: a longitudinal MRI study in children

International audienceShortly after reading instruction, a region in the ventral occipital temporal cortex (vOTC) of the left hemisphere, the Visual Word Form Area (VWFA), becomes specialized for written words. Its reproducible location across scripts suggests important anatomical constraints, such as specific patterns of connectivity, notably to spoken language areas. Here, we explored the structural connectivity of the emerging VWFA in terms of its specificity relative to other ventral visual regions and its stability throughout the process of reading instruction in 10 children studied longitudinally over 2 years. Category-specific regions for words, houses, faces, and tools were identified in the left vOTC of each subject with functional MRI. With diffusion MRI and tractography, we reconstructed the connections of these regions at two time points (mean age ± standard deviation: 6.2±0.3, 7.2±0.4 years). We first showed that the regions for each visual category harbor their own specific connectivity, all of which precede reading instruction and remain stable throughout development. The most specific connections of the VWFA were to the dorsal posterior parietal cortex. We then showed that microstructural changes in these connections correlated with improvements in reading scores over the first year of instruction but not one year later in a subsample of 8 children (age: 8.4±0.3 years). These results suggest that the VWFA location depends on its connectivity to distant regions, in particular the left inferior parietal region which may play a crucial role in visual field maps and eye movement dynamics in addition to attentional control in letter-by-letter reading and disambiguation of mirror letters during the first stages of learning to read

Connectivity between the visual word form area and the parietal lobe improves after the first year of reading instruction: a longitudinal MRI study in children

International audienceShortly after reading instruction, a region in the ventral occipital temporal cortex (vOTC) of the left hemisphere, the Visual Word Form Area (VWFA), becomes specialized for written words. Its reproducible location across scripts suggests important anatomical constraints, such as specific patterns of connectivity, notably to spoken language areas. Here, we explored the structural connectivity of the emerging VWFA in terms of its specificity relative to other ventral visual regions and its stability throughout the process of reading instruction in 10 children studied longitudinally over 2 years. Category-specific regions for words, houses, faces, and tools were identified in the left vOTC of each subject with functional MRI. With diffusion MRI and tractography, we reconstructed the connections of these regions at two time points (mean age ± standard deviation: 6.2±0.3, 7.2±0.4 years). We first showed that the regions for each visual category harbor their own specific connectivity, all of which precede reading instruction and remain stable throughout development. The most specific connections of the VWFA were to the dorsal posterior parietal cortex. We then showed that microstructural changes in these connections correlated with improvements in reading scores over the first year of instruction but not one year later in a subsample of 8 children (age: 8.4±0.3 years). These results suggest that the VWFA location depends on its connectivity to distant regions, in particular the left inferior parietal region which may play a crucial role in visual field maps and eye movement dynamics in addition to attentional control in letter-by-letter reading and disambiguation of mirror letters during the first stages of learning to read

Damage to the medial motor system in stroke patients with motor neglect

International audienceBackground and objectives: Motor neglect (MN) is a clinically important condition whereby patients with unilateral brain lesions fail to move their contralateral limbs, despite normal muscle strength, reflexes, and sensation. MN has been associated with various lesion sites, including the parietal and frontal cortex, the internal capsule, the lenticulostriate nuclei, and the thalamus. In the present study, we explored the hypothesis that MN depends on a dysfunction of the medial motor system by performing a detailed anatomical analysis in four patients with MN. Methods: Ten patients participated in the study: four with MN, four with left visual neglect but without MN, and three patients with left hemiplegia without MN. We used specific scales for clinical and neuropsychological assessment. We drew the lesion borders directly onto the original brain images of each patient, and plotted the lesions on anatomical atlases for gray and white matter. Results: Lesion locations were highly heterogeneous in our MN patients, and included frontal and parietal sites, basal ganglia, and white matter. The only consistently damaged structure across all MN patients was the cingulum bundle, a major pathway of the medial motor system important for motor initiative, and a key connection with limbic structures crucial for motivational aspects of actions. Three MN patients with additional damage to lateral fronto-parietal networks had also signs of contralesional visual neglect. The cingulum bundle was intact in all the control patients with visual neglect or hemiplegia. Conclusions: Cingulum damage may induce MN through unilateral dysfunction of the medial motor system. Additional lateral fronto-parietal dysfunction can result in the association with visual neglect

Connectivity between the visual word form area and the parietal lobe improves after the first year of reading instruction: a longitudinal MRI study in children

International audienceShortly after reading instruction, a region in the ventral occipital temporal cortex (vOTC) of the left hemisphere, the Visual Word Form Area (VWFA), becomes specialized for written words. Its reproducible location across scripts suggests important anatomical constraints, such as specific patterns of connectivity, notably to spoken language areas. Here, we explored the structural connectivity of the emerging VWFA in terms of its specificity relative to other ventral visual regions and its stability throughout the process of reading instruction in 10 children studied longitudinally over 2 years. Category-specific regions for words, houses, faces, and tools were identified in the left vOTC of each subject with functional MRI. With diffusion MRI and tractography, we reconstructed the connections of these regions at two time points (mean age ± standard deviation: 6.2±0.3, 7.2±0.4 years). We first showed that the regions for each visual category harbor their own specific connectivity, all of which precede reading instruction and remain stable throughout development. The most specific connections of the VWFA were to the dorsal posterior parietal cortex. We then showed that microstructural changes in these connections correlated with improvements in reading scores over the first year of instruction but not one year later in a subsample of 8 children (age: 8.4±0.3 years). These results suggest that the VWFA location depends on its connectivity to distant regions, in particular the left inferior parietal region which may play a crucial role in visual field maps and eye movement dynamics in addition to attentional control in letter-by-letter reading and disambiguation of mirror letters during the first stages of learning to read

Functional and morphological correlates of developmental dyslexia: A multimodal investigation of the ventral occipitotemporal cortex

Background and Purpose The ventral occipitotemporal cortex (vOT) is a region crucial for reading acquisition through selective tuning to printed words. Developmental dyslexia is a disorder of reading with underlying neurobiological bases often associated with atypical neural responses to printed words. Previous studies have discovered anomalous structural development and function of the vOT in individuals with dyslexia. However, it remains unclear if or how structural abnormalities relate to functional alterations.Methods In this study, we acquired structural, functional (words and faces processing), and diffusion MRI data from 26 children with dyslexia (average age = 10.4 +/- 2.0 years) and 14 age-matched typically developing readers (average age = 10.4 +/- 1.6 years). Morphological indices of local gyrification, neurite density (i.e., dendritic arborization structure), and orientation dispersion (i.e., dendritic arborization orientation) were analyzed within the vOT region that showed preferential activation in typically developing readers for words (as compared to face stimuli).Results The two cohorts diverged significantly in both functional and structural measures. Compared to typically developing controls, children with dyslexia did not show selectivity for words in the left vOT (contrast: words > false fonts). This lack of tuning to printed words was associated with greater neurite dispersion heterogeneity in the dyslexia cohort, but similar neurite density. These group differences were not present in the homologous contralateral area, the right vOT.Conclusions Our findings provide new insight into the neurobiology of the lack of vOT word tuning in dyslexia by linking behavior, alterations in functional activation, and neurite organization