Abstract

We herein propose an atlas of 32 sentence-related areas based on a 3-step method combining the analysis of activation and asymmetry during multiple language tasks with hierarchical clustering of resting-state connectivity and graph analyses. 144 healthy right-handers performed fMRI runs based on language production, reading and listening, both with sentences and lists of over-learned words. Sentence minus word-list BOLD contrast and left-minus-right BOLD asymmetry for each task were computed in pairs of homotopic regions of interest (hROIs) from the AICHA atlas. Thirty-two hROIs were identified that were conjointly activated and leftward asymmetrical in each of the three language contrasts. Analysis of resting-state temporal correlations of BOLD variations between these 32 hROIs allowed the segregation of a core network, SENT_CORE including 18 hROIs. Resting-state graph analysis applied to SENT_CORE hROIs revealed that the pars triangularis of the inferior frontal gyrus and the superior temporal sulcus were hubs based on their degree centrality (DC), betweenness, and participation values corresponding to epicentres of sentence processing. Positive correlations between DC and BOLD activation values for SENT_CORE hROIs were observed across individuals and across regions regardless of the task: the more a SENT_CORE area is connected at rest the stronger it is activated during sentence processing. DC measurements in SENT_CORE may thus be a valuable index for the evaluation of inter-individual variations in language areas functional activity in relation to anatomical or clinical patterns in large populations. SENSAAS (SENtence Supramodal Areas AtlaS), comprising the 32 supramodal sentence areas, including SENT_CORE network, can be downloaded at http://www.gin.cnrs.fr/en/tools/.

Highlights

  • Defining language areas is a complex enterprise because of the numerous possible approaches currently available to identify language-related regions

  • Among the 80 homotopic regions of interest (hROIs) jointly activated in the 3 contrasts (Table 1), 46 showed joint asymmetries

  • Two hROIs were located within the anterior insula (INSa2 and INSa3), while the INSa1 hROI was located medially and ventrally close to the amygdala

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Summary

Introduction

Defining language areas is a complex enterprise because of the numerous possible approaches currently available to identify language-related regions. Even when limiting the definition of language areas to that of essential language areas, different identification methods exist that provide various kinds of information. Surgical cortical stimulation studies have documented left hemisphere language areas in large samples of patients (Ojemann et al 1989; Tate et al 2014), but such mapping of eloquent areas is still limited to the cortical regions available to the neurosurgeon and is conducted in patients having potentially modified language organization. The probabilistic mapping of lesions combined with fine-grained aphasic patient evaluations of language performance have provided the community with very accurate descriptions of essential language areas (Dronkers and Ogar 2004; Dronkers et al 2004) this very important approach does not reveal how these cortical areas are organized in networks. Because each multiple cortical area altered by a given pathology is not involved in the language deficit, the comprehensive identification of language areas from lesions is a complex issue [see (Genon et al 2018a, b) for a review]

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