Mathieu Vigneau

Meta-analyzing left hemisphere language areas: phonology, semantics, and sentence processing.

The advent of functional neuroimaging has allowed tremendous advances in our understanding of brain-language relationships, in addition to generating substantial empirical data on this subject in the form of thousands of activation peak coordinates reported in a decade of language studies. We performed a large-scale meta-analysis of this literature, aimed at defining the composition of the phonological, semantic, and sentence processing networks in the frontal, temporal, and inferior parietal regions of the left cerebral hemisphere. For each of these language components, activation peaks issued from relevant component-specific contrasts were submitted to a spatial clustering algorithm, which gathered activation peaks on the basis of their relative distance in the MNI space. From a sample of 730 activation peaks extracted from 129 scientific reports selected among 260, we isolated 30 activation clusters, defining the functional fields constituting three distributed networks of frontal and temporal areas and revealing the functional organization of the left hemisphere for language. The functional role of each activation cluster is discussed based on the nature of the tasks in which it was involved. This meta-analysis sheds light on several contemporary issues, notably on the fine-scale functional architecture of the inferior frontal gyrus for phonological and semantic processing, the evidence for an elementary audio-motor loop involved in both comprehension and production of syllables including the primary auditory areas and the motor mouth area, evidence of areas of overlap between phonological and semantic processing, in particular at the location of the selective human voice area that was the seat of partial overlap of the three language components, the evidence of a cortical area in the pars opercularis of the inferior frontal gyrus dedicated to syntactic processing and in the posterior part of the superior temporal gyrus a region selectively activated by sentence and text processing, and the hypothesis that different working memory perception-actions loops are identifiable for the different language components. These results argue for large-scale architecture networks rather than modular organization of language in the left hemisphere.

What is right-hemisphere contribution to phonological, lexico-semantic, and sentence processing? Insights from a meta-analysis.

To evaluate the relative role of left and right hemispheres (RH) and describe the functional anatomy of RH during ortholinguistic tasks, we re-analyzed the 128 papers of a former left-hemisphere (LH) meta-analysis (Vigneau et al., 2006). Of these, 59 articles reported RH participation, providing 105 RH language contrasts including 218 peaks compared to 728 on the left, a proportion reflecting the LH language dominance. To describe inter-hemispheric interactions, in each of the language contrasts involving both hemispheres, we distinguished between unilateral and bilateral peaks, i.e. having homotopic activation in the LH in the same contrast. We also calculated the proportion of bilateral peaks in the LH. While the majority of LH peaks were unilateral (79%), a reversed pattern was observed in the RH; this demonstrates that, in contrast to the LH, the RH works in an inter-hemispheric manner. To analyze the regional pattern of RH participation, these unilateral and bilateral peaks were spatially clustered for each language component. Most RH phonological clusters corresponded to bilateral recruitment of auditory and motor cortices. Notably, the motor representation of the mouth and phonological working memory areas were exclusively left-lateralized, supporting the idea that the RH does not host phonological representations. Right frontal participation was not specific for the language component involved and appeared related to the recruitment of attentional and working memory areas. The fact that RH participation during lexico-semantic tasks was limited to these executive activations is compatible with the hypothesis that active inhibition is exerted from the LH during the processing of meaning. Only during sentence/text processing tasks a specific unilateral RH-temporal involvement was noted, likely related to context processing. These results are consistent with split-brain studies that found that the RH has a limited lexicon, with no phonological abilities but active involvement in the processing of context.

Word and non-word reading: What role for the Visual Word Form Area?

The putative role of the so-called Visual Word Form Area (VWFA) during reading remains under debate. For some authors, this region is specifically involved in a pre-lexical processing of words and pseudowords, whereas such specificity is challenged by others given the VWFA involvement during both non-word reading and word listening. Here, we further investigated this issue, measuring BOLD variations and their lateralization with fMRI during word and non-word reading, in order to evaluate the lexicality effect, and during reading and listening of words, in order to evaluate the impact of stimulus delivery modality on word processing networks. Region of interest (ROI) analysis was first performed in three target areas: 1-VWFA as defined by a meta-analysis of the word reading literature, 2-a middle temporal area (T2) found co-activated by both word reading and listening, 3-an inferior occipital area (OI) belonging to the unimodal visual cortex of the inferior occipital gyrus. VWFA activity was found not different between word and non-word reading but was more leftward lateralized during word reading due to a reduction of activity in the VWFA right counterpart. A similar larger leftward lateralization during word reading was also uncovered in the T2 ROI but was related to a larger left side activity. Such a lexicality effect was not observed in the OI ROI. By contrast, BOLD increases during listening were restricted to the left VWFA and T2 ROIs. Voxel-based analysis (SPM99) showed that semantic areas were more active during word than non-word reading and co-activated by both reading and listening, exhibiting a left lateralized activity in all tasks. These results indicate that the left VWFA would be the place where visual and verbal representations bind under the control of left semantic areas.

How verbal and spatial manipulation networks contribute to calculation: An fMRI study

The manipulation of numbers required during calculation is known to rely on working memory (WM) resources. Here, we investigated the respective contributions of verbal and/or spatial WM manipulation brain networks during the addition of four numbers performed by adults, using functional magnetic resonance imaging (fMRI). Both manipulation and maintenance tasks were proposed with syllables, locations, or two-digit numbers. As compared to their maintenance, numbers manipulation (addition) elicited increased activation within a widespread cortical network including inferior temporal, parietal, and prefrontal regions. Our results demonstrate that mastery of arithmetic calculation requires the cooperation of three WM manipulation systems: an executive manipulation system conjointly recruited by the three manipulation tasks, including the anterior cingulate cortex (ACC), the orbital part of the inferior frontal gyrus, and the caudate nuclei; a left-lateralized, language-related, inferior fronto-temporal system elicited by numbers and syllables manipulation tasks required for retrieval, selection, and association of symbolic information; and a right superior and posterior fronto-parietal system elicited by numbers and locations manipulation tasks for spatial WM and attentional processes. Our results provide new information that the anterior intraparietal sulcus (IPS) is involved in tasks requiring a magnitude processing with symbolic (numbers) and nonsymbolic (locations) stimuli. Furthermore, the specificity of arithmetic processing is mediated by a left-hemispheric specialization of the anterior and posterior parts of the IPS as compared to a spatial task involving magnitude processing with nonsymbolic material.

Impact of modality and linguistic complexity during reading and listening tasks

Reading and understanding speech are usually considered as different manifestations of a single cognitive ability, that of language. In this study, we were interested in characterizing the specific contributions of input modality and linguistic complexity on the neural networks involved when subjects understand language. We conducted an fMRI study during which 10 right-handed male subjects had to read and listen to words, sentences and texts in different runs. By comparing reading to listening tasks, we were able to show that the cerebral regions specifically recruited by a given modality were circumscribed to unimodal and associative unimodal cortices associated with the task, indicating that higher cognitive processes required by the task may be common to both modalities. Such cognitive processes involved a common phonological network as well as lexico-semantic activations as revealed by the conjunction between all reading and listening tasks. The restriction of modality-specific regions to their corresponding unimodal cortices was replicated when looking at brain areas showing a greater increase during the comprehension of more complex linguistic units than words (such as sentences and texts) for each modality. Finally, we discuss the possible roles of regions showing pure effect of linguistic complexity, such as the anterior part of the superior temporal gyrus and the ventro-posterior part of the middle temporal gyrus that were activated for sentences and texts but not for isolated words, as well as a text-specific region found in the left posterior STS.

Functional Magnetic Resonance Imaging Study of Piaget's Conservation-of-Number Task in Preschool and School-Age Children: A Neo-Piagetian Approach.

Jean Piagets theory is a central reference point in the study of logico-mathematical development in children. One of the most famous Piagetian tasks is number conservation. Failures and successes in this task reveal two fundamental stages in childrens thinking and judgment, shifting at approximately 7 years of age from visuospatial intuition to number conservation. In the current study, preschool children (nonconservers, 5-6 years of age) and school-age children (conservers, 9-10 years of age) were presented with Piagets conservation-of-number task and monitored by functional magnetic resonance imaging (fMRI). The cognitive change allowing children to access conservation was shown to be related to the neural contribution of a bilateral parietofrontal network involved in numerical and executive functions. These fMRI results highlight how the behavioral and cognitive stages Piaget formulated during the 20th century manifest in the brain with age.

Functional Asymmetries Revealed in Visually Guided Saccades: An fMRI Study

Because eye movements are a fundamental tool for spatial exploration, we hypothesized that the neural bases of these movements in humans should be under right cerebral dominance, as already described for spatial attention. We used functional magnetic resonance imaging in 27 right-handed participants who alternated central fixation with either large or small visually guided saccades (VGS), equally performed in both directions. Hemispheric functional asymmetry was analyzed to identify whether brain regions showing VGS activation elicited hemispheric asymmetries. Hemispheric anatomical asymmetry was also estimated to assess its influence on the VGS functional lateralization. Right asymmetrical activations of a saccadic/attentional system were observed in the lateral frontal eye fields (FEF), the anterior part of the intraparietal sulcus (aIPS), the posterior third of the superior temporal sulcus (STS), the occipitotemporal junction (MT/V5 area), the middle occipital gyrus, and medially along the calcarine fissure (V1). The present rightward functional asymmetries were not related to differences in gray matter (GM) density/sulci positions between right and left hemispheres in the precentral, intraparietal, superior temporal, and extrastriate regions. Only V1 asymmetries were explained for almost 20% of the variance by a difference in the position of the right and left calcarine fissures. Left asymmetrical activations of a saccadic motor system were observed in the medial FEF and in the motor strip eye field along the Rolando sulcus. They were not explained by GM asymmetries. We suggest that the leftward saccadic motor asymmetry is part of a general dominance of the left motor cortex in right-handers, which must include an effect of sighting dominance. Our results demonstrate that, although bilateral by nature, the brain network involved in the execution of VGSs, irrespective of their direction, presented specific right and left asymmetries that were not related to anatomical differences in sulci positions.

BIL&GIN: A neuroimaging, cognitive, behavioral, and genetic database for the study of human brain lateralization.

We report on a database, named BIL&GIN, designed for investigating the cognitive, behavioral, genetic, and brain morphological/functional correlates of hemispheric specialization. The database contains records from a sample of 453 adult participants enriched in left-handers (45%, N=205) as compared to the general population. For each subject, socio-demographic data, hand and eye laterality, family handedness, and cognitive abilities in the language, motor, visuo-spatial, and numerical domains have been recorded. T1-MRI and DTI data were also acquired, as well as resting-state functional MRI. Task-evoked functional MRI was performed in a sub-sample of 303 subjects (157 left-handers) using a customized functional battery of 16 cognitive tasks exploring the same three cognitive domains. Performances at the tasks executed in the magnet as well as post-acquisition debriefing were recorded. A saliva sample was obtained from the subjects of this sub-sample from which DNA was extracted. The BIL&GIN contains results of imaging data processing for each subject, namely maps of tissue (GM, WM, CSF) probability, cortical thickness, cortical surface, and diffusion parameters as well as regional values of these phenotypes for regions of both AAL and FreeSurfer parcellations. For the subjects who underwent FMRI, individual SPM contrast maps for each of the 8 runs were also calculated and included in the database, as well as corresponding BOLD variations in ROIs of the AAL and AICHA atlases, and Wilkes hemispheric functional lateralization index. The BIL&GIN data sharing is based on a collaborative model.

The weight of skill: Interindividual variability of reading related brain activation patterns in fluent readers

Abstract Neuroimaging studies of reading have so far mainly focused on the description of brain regions involved in processing writ words, particularly through approaches revealing the average activation pattern of entire groups of subjects. The aim of the present study was to contribute to the question of functional inter-individual variability of reading, and investigate whether reading can rely on different brain activation patterns, even in literate subjects, in a way that reflects their level of proficiency with written material. The present fMRI results obtained with a group of 33 literate subjects are consistent with models of reading postulating the existence of two routes to access words. They show that subject’s proficiency with written words is one factor that can shape the amount with which subjects rely on one route or the other. An essential functional set of brain regions was found to be reliably activated by each subject of our group, and its implication did not vary as a function of the reader’s skill. This set comprises regions devoted to the visual analysis of words (bilateral occipital regions and the left occipito-temporal junction), access to semantics (the basal temporal language area) and pronunciation (left rolandic sulcus) and could correspond to a direct access to words. Lower skilled readers showed a greater involvement of additional regions related to the grapho-phonological conversion of words. The deactivations observed in these regions for the most proficient readers indicate a functional independence of the two routes to access words.

A common neural system is activated in hearing non-signers to process French sign language and spoken French.

We used functional magnetic resonance imaging to investigate the areas activated by signed narratives in non-signing subjects naïve to sign language (SL) and compared it to the activation obtained when hearing speech in their mother tongue. A subset of left hemisphere (LH) language areas activated when participants watched an audio-visual narrative in their mother tongue was activated when they observed a signed narrative. The inferior frontal (IFG) and precentral (Prec) gyri, the posterior parts of the planum temporale (pPT) and of the superior temporal sulcus (pSTS), and the occipito-temporal junction (OTJ) were activated by both languages. The activity of these regions was not related to the presence of communicative intent because no such changes were observed when the non-signers watched a muted video of a spoken narrative. Recruitment was also not triggered by the linguistic structure of SL, because the areas, except pPT, were not activated when subjects listened to an unknown spoken language. The comparison of brain reactivity for spoken and sign languages shows that SL has a special status in the brain compared to speech; in contrast to unknown oral language, the neural correlates of SL overlap LH speech comprehension areas in non-signers. These results support the idea that strong relationships exist between areas involved in human action observation and language, suggesting that the observation of hand gestures have shaped the lexico-semantic language areas as proposed by the motor theory of speech. As a whole, the present results support the theory of a gestural origin of language.