eNeuro. 2024 Jun 17:ENEURO.0138-24.2024. doi: 10.1523/ENEURO.0138-24.2024. Online ahead of print.

ABSTRACT

Language is an evolutionarily salient faculty for humans that relies on a distributed brain network spanning across frontal, temporal, parietal, and subcortical regions. To understand whether the complex language network shares common or distinct genetic mechanisms, we examined the relationships between the genetic effects underlying the brain responses to language and a set of object domains that have been suggested to coevolve with language: tools, faces (indicating social), and body parts (indicating social and gesturing). Analyzing the twin datasets released by the Human Connectome Project (HCP) that had fMRI data from human twin subjects (monozygotic and dizygotic) undergoing language and working memory tasks contrasting multiple object domains (198 females and 144 males for the language task; 192 females and 142 males for the working memory task), we identified a set of cortical regions in the frontal and temporal cortices and subcortical regions whose activity to language was significantly genetically influenced. The heterogeneity of the genetic effects among these language clusters were corroborated by significant differences of the human gene expression profiles (AHBA dataset). Among them, the bilateral basal ganglia (mainly dorsal caudate) exhibited a common genetic basis for language, tool, and body part processing, and the right superior temporal gyrus exhibited a common genetic basis for language and tool processing across multiple types of analyses. These results uncovered the heterogeneous genetic patterns of language neural processes, shedding light on the evolution of language and its shared origins with tools and bodily functions.Significance Statement Human language entails a distributed brain network spanning across frontal, temporal, parietal, and subcortical regions. To elucidate the genetic basis underlying this complex language network, we adopted the HCP fMRI twin data to examine the relationship between the genetic effects for the brain responses to language and to object domains that have been hypothesized to coevolve with language (tools, social, and body actions). The bilateral basal ganglia exhibited a common genetic basis for language, tool, and body part processing, and the right superior temporal gyrus for language and tool processing. These results provide evidence for the heterogeneous genetic patterns of language neural processes and shed light on its potential origin with tools and bodily actions.

PMID:38886065 | DOI:10.1523/ENEURO.0138-24.2024