The genetic architecture of language functional connectivity

Mekki, Yasmina N; Guillemot, Vincent; Lemaître, Hervé; Carrión-Castillo, Amaia; Forkel, Stephanie J.; Frouin, Vincent; Philippe, Cathy

doi:10.1016/j.neuroimage.2021.118795

Cited by 23 publications

(25 citation statements)

References 117 publications

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“…The functional selectivity of Net1 regions is likely to be inherited from our ancestors and to be part of a language-ready brain (Boeckx & Benítez-Burraco, 2014). They are also supported by a specific brain architecture already present in children (Friederici, 2017) whose functional connectivity is genetically encoded (Mekki et al 2022, for the genetic regulation specifically involved in the perceptual-motor and semantic pathways of language).…”

Section: Discussionmentioning

confidence: 99%

Unraveling the functional attributes of the language connectome: crucial subnetworks, flexibility and variability

Roger

Almeida

Lœvenbruck

et al. 2022

Preprint

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Language processing is a highly integrative function, intertwining linguistic operations (processing the language code intentionally used for communication) and extra-linguistic processes (e.g., attention monitoring, predictive inference, long-term memory). This synergetic cognitive architecture requires a distributed and specialized neural substrate. Brain systems have mostly been examined at rest. However, task-related functional connectivity provides additional and valuable information about how information is processed when various cognitive states are involved. We gathered thirteen language fMRI tasks in a unique database of one hundred and fifty neurotypical adults (InLang database). The tasks were designed to assess a wide range of linguistic processes and subprocesses. From this database, we applied network theory as a computational tool to model the task-related functional connectome of language (LANG). The organization of this data-driven neurocognitive atlas of language is examined at multiple levels, uncovering its major components (or crucial subnetworks) and its anatomical and functional correlates. Furthermore, we estimate its reconfiguration as a function of linguistic demand (flexibility), or several factors such as age or gender (variability). By accounting for the multifaceted nature of language and modulating factors, this study can contribute to enrich and refine existing neurocognitive models of language. The LANG atlas can also be considered as a reference for comparative or clinical studies, involving a variety of patients and conditions.

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Section: Discussionmentioning

confidence: 99%

Unraveling the functional attributes of the language connectome: crucial subnetworks, flexibility and variability

Roger

Almeida

Lœvenbruck

et al. 2022

Preprint

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“…Given efforts currently underway to map the genetic architecture of neural traits (e.g., work by the ENIGMA consortium: Smit et al, 2021 ) there is a timely opportunity to leverage existing resources to further our understanding of musicality-language links. Large-scale data sets can now be creatively leveraged to map genetic variants to neural correlates of musicality and language traits (e.g., Mekki et al, 2022 , recently mapped the genetic architecture of resting-state functional connectivity in brain regions classically associated with language function). To identify neural endophenotypes as proposed by the MAPLE framework, future research can systematically draw on existing neural data that is linked with genetic and behavioral data, for example in biobank initiatives such as the UK Biobank ( Sudlow et al, 2015 ).…”

Section: Integrating Genetics Approaches Into Musicality-language Res...mentioning

confidence: 99%

“…Potential neural endophenotypes involving brain structures are already available as part of large-scale data sets that include both neural and genetic information, such as the UK Biobank ( Sudlow et al, 2015 ) or the Cohorts for Heart and Aging Research in Genomic Epidemiology (CHARGE) Consortium ( Psaty et al, 2009 ). We can also define functional neural endophenotypes of interest based on available neuroimaging studies of musical and language processing, extracting genomic or gene expression data associated with functional activation data ( Kong et al, 2020 ; Mekki et al, 2022 ). For example, Mekki et al (2022) defined a language network based on an existing meta-analysis of fMRI-based language-related function, then used the network to explore the genetic architecture of resting state functional connectivity in the inferred language network, using individual genotypes from the UK Biobank ( Sudlow et al, 2015 ).…”

Section: Supporting Evidence For the Maple Frameworkmentioning

confidence: 99%

“…We can also define functional neural endophenotypes of interest based on available neuroimaging studies of musical and language processing, extracting genomic or gene expression data associated with functional activation data ( Kong et al, 2020 ; Mekki et al, 2022 ). For example, Mekki et al (2022) defined a language network based on an existing meta-analysis of fMRI-based language-related function, then used the network to explore the genetic architecture of resting state functional connectivity in the inferred language network, using individual genotypes from the UK Biobank ( Sudlow et al, 2015 ). Therefore, even though neuroimaging during a language task was not conducted in UK Biobank participants, this triangulation among genes, brain, and behavior, makes it possible to gain insights into the genetic architecture of the relevant circuitry (although we do not yet know to what degree genetic associations with resting-state data reflect those that would be seen with task-based functional activation data from the same participants).…”

Section: Supporting Evidence For the Maple Frameworkmentioning

confidence: 99%

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The Musical Abilities, Pleiotropy, Language, and Environment (MAPLE) Framework for Understanding Musicality-Language Links Across the Lifespan

Nayak

Coleman

Ladányi

et al. 2022

Neurobiology of Language

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Using individual differences approaches, a growing body of literature finds positive associations between musicality and language-related abilities, complementing prior findings of links between musical training and language skills. Despite these associations, musicality has been often overlooked in mainstream models of individual differences in language acquisition and development. To better understand the biological basis of these individual differences, we propose the Musical Abilities, Pleiotropy, Language, and Environment (MAPLE) framework. This novel integrative framework posits that musical and language-related abilities likely share some common genetic architecture (i.e., genetic pleiotropy) in addition to some degree of overlapping neural endophenotypes, and genetic influences on musically and linguistically enriched environments. Drawing upon recent advances in genomic methodologies for unraveling pleiotropy, we outline testable predictions for future research on language development and how its underlying neurobiological substrates may be supported by genetic pleiotropy with musicality. In support of the MAPLE framework, we review and discuss findings from over seventy behavioral and neural studies, highlighting that musicality is robustly associated with individual differences in a range of speech-language skills required for communication and development. These include speech perception-in-noise, prosodic perception, morphosyntactic skills, phonological skills, reading skills, and aspects of second/foreign language learning. Overall, the current work provides a clear agenda and framework for studying musicality-language links using individual differences approaches, with an emphasis on leveraging advances in the genomics of complex musicality and language traits.

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“…The presence of FOXP2 , a gene known for its role in language ( Lai et al, 2001 ; Fisher, 2019 ), in one of these large deserts has attracted attention ( Kuhlwilm, 2018 ), as it raises the possibility that the incompatibility between Homo sapiens and other hominin in such persistent introgression deserts may point to (subtle, but real) cognitive/behavioral differences. Indeed, the presence in such deserts of not only FOXP2 but also other genes like ROBO1 , ROBO2 , and EPHA3 , all independently associated with language traits ( St Pourcain et al, 2014 ; Wang et al, 2015 ; Eising et al, 2021 ; Mekki et al, 2022 ), together with an earlier observation in Vernot et al (2016) that genes within large deserts are significantly enriched in the developing cerebral cortex and in the adult striatum, suggest a possible point of entry into some of the most distinctive aspects of the human condition ( Pääbo, 2014 ). Such considerations, combined with independent evidence that introgressed Neanderthal alleles show significant downregulation in brain regions ( McCoy et al, 2017 ), motivated us to focus on the brain in this study.…”

Section: Introductionmentioning

confidence: 92%

A Brain Region-Specific Expression Profile for Genes Within Large Introgression Deserts and Under Positive Selection in Homo sapiens

Buisan

Moriano

Andirkó

et al. 2022

Front. Cell Dev. Biol.

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Analyses of ancient DNA from extinct hominins have provided unique insights into the complex evolutionary history of Homo sapiens, intricately related to that of the Neanderthals and the Denisovans as revealed by several instances of admixture events. These analyses have also allowed the identification of introgression deserts: genomic regions in our species that are depleted of “archaic” haplotypes. The presence of genes like FOXP2 in these deserts has been taken to be suggestive of brain-related functional differences between Homo species. Here, we seek a deeper characterization of these regions and the specific expression trajectories of genes within them, taking into account signals of positive selection in our lineage. Analyzing publicly available transcriptomic data from the human brain at different developmental stages, we found that structures outside the cerebral neocortex, in particular the cerebellum, the striatum and the mediodorsal nucleus of the thalamus show the most divergent transcriptomic profiles when considering genes within large introgression deserts and under positive selection.

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The genetic architecture of language functional connectivity

Cited by 23 publications

References 117 publications

Unraveling the functional attributes of the language connectome: crucial subnetworks, flexibility and variability

Unraveling the functional attributes of the language connectome: crucial subnetworks, flexibility and variability

The Musical Abilities, Pleiotropy, Language, and Environment (MAPLE) Framework for Understanding Musicality-Language Links Across the Lifespan

A Brain Region-Specific Expression Profile for Genes Within Large Introgression Deserts and Under Positive Selection in Homo sapiens

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