Model-based and model-free analyses of the neural correlates of tongue movements

Abstract

The tongue performs movements in all directions to subserve its diverse functions in chewing, swallowing, and speech production. The aims of the present study were twofold: using task-based functional MRI in a group of 17 healthy young participants, we studied (1) potential differences in the cerebral control of frontal, horizontal, and vertical tongue movements and (2) potential inter-individual differences in tongue motor control. To investigate differences between different tongue movements, we performed voxel-wise multiple linear regressions. To investigate inter-individual differences, we applied a novel approach, spatio-temporal filtering of independent components. For this approach, individual functional data sets were decomposed into spatially independent components and corresponding time courses using ICA. A temporal filter (correlation with the expected brain response) was used to identify independent components time-locked to the tongue motor task. A spatial filter (cross-correlation with established neurofunctional systems) was used to identify brain activity not time-locked to the task. Our results confirm the importance of an extended bilateral cortical and subcortical network for the control of tongue movements, including the lateral primary sensorimotor cortex, supplementary motor cortex, anterior cingulate gyrus, insula, basal ganglia, thalamus, and cerebellum. Frontal tongue movements, highly overlearned movements related to speech production, showed less activity in parts of the frontal and parietal lobes compared to horizontal and vertical movements and greater activity in parts of the left frontal and temporal lobes compared to vertical movements. The investigation of inter-individual differences revealed a component representing the tongue primary sensorimotor cortex time-locked to the task in all participants. Using the spatial filter, we found the default mode network in 16 of 17 participants, the left fronto-parietal network in 16, the right fronto-parietal network in 8, and the executive control network in 4 participants. Further detailed analyses of speech-related tongue movements are warranted to increase our understanding of tongue motor control as a crucial part of articulation. Spatio-temporal filtering of independent components appears to be a powerful approach to study inter-individual differences in task-based functional MRI. This approach may be particularly useful for the assessment of individual patients and may be related to individual clinical, behavioral, and genetic information.