Language comprehension functionally modulates first-order relay thalamic nuclei

Language, a uniquely human higher-order cognitive function, has traditionally been attributed to cortical mechanisms with limited attention given to subcortical contributions. Recent advances in non-invasive neuroimaging have revealed that thalamic activity can be modulated by attention and task demands. Moreover, lesion studies have hinted at the thalamuss potential role in language processing. Nevertheless, the precise involvement of this structure in language remains unclear. Here, we argue that language-related modulations can occur as early as the sensory thalamic stage, challenging the conventional view of language preprocessing as a predominantly language function. Using functional MRI to image 40 human participants (both female and male) while processing linguistic and non-linguistic stimuli of three main language systems (reading, speech comprehension, and speech production), we demonstrate specific activation of first-order nuclei during targeted language system tasks: lateral geniculate (LGN) for reading, medial geniculate (MGN) for speech comprehension and ventrolateral (VLN) for speech production. Notably, we show linguistic versus non-linguistic stimuli exhibit functional modulations during comprehension tasks (reading and speech) of left MGN and, to a lesser extent, left LGN--in line with prior studies of lateralization of language processes. Multi-voxel classification analysis confirmed left-lateralized linguistic modulation in the MGN, but not in the LGN. Given the complexity of thalamic connectivity and its potential role in integrating sensory and cognitive processes, this work constitutes a relevant first step to further understand thalamic involvement and thalamocortical interactions in language function. Significant StatementThis is the first study to examine the involvement of first-order thalamic nuclei in three main language systems: reading, speech comprehension and production. Using fMRI, we show that the activation of sensory thalamus is modulated by the linguistic nature of the stimuli: the lateral geniculate nucleus distinguished real words from scrambled images, and the medial geniculate nucleus differentiated intelligible speech from nonsensical sounds. This modulation was left-lateralized, especially in the medial geniculate nucleus, suggesting a language-specific mechanism. Our findings challenge the cortico-centric view of language functions, demonstrating that thalamic involvement occurs at early stages of language processing. HighlightsO_LILanguage systems (reading, speech comprehension, speech production) can be used to functionally localize three main first-order thalamic nuclei (LGN, MGN, VLN); C_LIO_LILanguage systems show specific first-order thalamic nuclei engagement; C_LIO_LILanguage comprehension (reading and speech) modulates left-lateralized functional activation in corresponding first-order thalamic nuclei; C_LIO_LINo linguistic modulations were observed in terms of functional and structural connectivity. C_LI