Abstract
The tongue performs movements in all directions to subserve its diverse functions in chewing, swallowing, and speech production. Using task-based functional MRI in a group of 17 healthy young participants, we studied (1) potential differences in the cerebral control of frontal (protrusion), horizontal (side to side), and vertical (elevation) tongue movements and (2) 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 were decomposed into spatially independent components and corresponding time courses using independent component analysis. A temporal filter (correlation with the expected brain response) was used to identify independent components time-locked to the tongue motor tasks. A spatial filter (cross-correlation with established neurofunctional systems) was used to identify brain activity not time-locked to the tasks. Our results confirm the importance of an extended bilateral cortical and subcortical network for the control of tongue movements. Frontal (protrusion) tongue movements, highly overlearned movements related to speech production, showed less activity in the frontal and parietal lobes compared to horizontal (side to side) and vertical (elevation) movements and greater activity in the left frontal and temporal lobes compared to vertical movements (cluster-forming threshold of Z > 3.1, cluster significance threshold of p < 0.01, corrected for multiple comparisons). 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 four participants (Pearson's r > 0.4 between neurofunctional systems and individual components). These results demonstrate that spatio-temporal filtering of independent components allows to identify individual brain activity related to a specific task and also structured spatiotemporal processes representing known neurofunctional systems on an individual basis. This novel approach may be useful for the assessment of individual patients and results may be related to individual clinical, behavioral, and genetic information.
Highlights
The human tongue is a unique muscular and sensory organ with critical roles in several motor tasks, such as chewing, swallowing, respiration, and speech (Sawczuk and Mosier, 2001; Hiiemae and Palmer, 2003), in addition to its somatosensory (Pardo et al, 1997; Sakamoto et al, 2010) and gustatory functions (Kobayakawa et al, 2005; Hummel et al, 2010).To subserve its distinct motor tasks, the tongue contains intrinsic and extrinsic muscle fibers (Schumacher, 1927; AbdEl-Malek, 1939), which are extensively interwoven (Gaige et al, 2007)
Main results of the present task-based functional magnetic resonance imaging (FMRI) study on the neural correlates of tongue movements were: (1) All three tongue movements under investigation were controlled by the same neurofunctional system, consisting of the bilateral tongue primary sensorimotor cortex, supplementary motor cortex, anterior cingulate gyrus, basal ganglia, thalamus, and cerebellum
(3) Using a novel approach to characterize inter-individual differences in taskbased FMRI data, spatio-temporal filtering of independent components, we found consistent activation of the tongue primary sensorimotor cortex in all participants, and remarkable variability, e.g., in fronto-parietal and executive control networks
Summary
The human tongue is a unique muscular and sensory organ with critical roles in several motor tasks, such as chewing, swallowing, respiration, and speech (Sawczuk and Mosier, 2001; Hiiemae and Palmer, 2003), in addition to its somatosensory (Pardo et al, 1997; Sakamoto et al, 2010) and gustatory functions (Kobayakawa et al, 2005; Hummel et al, 2010).To subserve its distinct motor tasks, the tongue contains intrinsic and extrinsic muscle fibers (Schumacher, 1927; AbdEl-Malek, 1939), which are extensively interwoven (Gaige et al, 2007). Intrinsic fibers originate and insert within the tongue itself, while extrinsic fibers are attached to bony structures, such as the mandible, hyoid bone, or styloid process (Sanders and Mu, 2013). This complex biomechanical architecture is the basis for the tongue’s ability to move and alter its shape in all three dimensions (Kier and Smith, 1985). Intrinsic and extrinsic tongue muscles are innervated by the lateral and medial divisions of the hypoglossal nerve (cranial nerve XII), with different components of the musculature being supplied by different hypoglossal branches (Mu and Sanders, 2010) and controlled by distinct hypoglossal subnuclei (McClung and Goldberg, 2002)
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