Language comprehension functionally modulates first-order relay thalamic nuclei

Abstract

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 ask whether language- related modulations can be detected as early as the sensory thalamic stage. 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 offers a comprehensive characterization of first-order thalamic engagement across reading, speech comprehension, and speech production within the same participants, advancing our understanding of thalamic involvement and thalamocortical interactions in language function.