Corticomotor plasticity induced by tongue-task training in humans: a longitudinal fMRI study

Abstract

Corticomotor pathways may undergo neuroplastic changes in response to acquisition of new motor skills. Little is known about the motor control strategies for learning new tongue tasks. The aim of this study was to investigate the longitudinal effect of novel tongue-task training on corticomotor neuroplasticity. Thirteen healthy, right-handed men, aged 24-35years (mean age±SD: 27.3±0.3years), performed a training task consisting of standardized tongue protrusion onto a force transducer. The tongue task consisted of a relax-protrude-hold-relax cycle with 1.0N as the target at the hold phase lasting for 1.5s. Subjects repeated this task for 1h. Functional magnetic resonance imaging was carried out before the tongue-task training (baseline), 1-h after the training, and one-day and one-week follow-up. During scanning, the subjects performed tongue protrusion in blocks interspersed with rest. A region-of-interest (ROI) approach and an explorative search were implemented for the analysis of corticomotor activity across conditions. All subjects completed the tongue-task training (mean success rate 43.0±13.2%). In the baseline condition, tongue protrusion resulted in bilateral activity in regions most typically associated with a motor task including medial frontal gyrus (supplementary motor area [SMA]), precentral gyrus (tongue motor cortex), putamen, thalamus, and cerebellum. The ROI analysis revealed increased activity in the precentral gyrus already 1h post-training. One day after the training, increased activity was observed in the precentral gyrus, SMA, putamen, and cerebellum. No increase was found 1week after training. Correlation analyses between changes in success rates and changes in the numbers of voxels showed robust associations for left Area 4a in primary motor cortex 1h, 1day, and 1week after the tongue-task training and for the left Area 4p in primary motor cortex and the left lateral premotor cortex 1day after the training. In the unrestricted analysis, increased activity was found in the parahippocampal gyrus 1h after the tongue-task training and remained for a week. Decreased activity was found in right post-central and middle frontal gyri 1h and 1week post-training. The results verified the involvement of specific corticomotor areas in response to tongue protrusion. Short-term tongue-task training was associated with longer-lasting (up to 1week) changes in motor-related brain activity. The results suggested that primary motor areas are involved in the early and late stages, while other motor areas mainly are engaged in the later stage of corticomotor neuroplasticity of the tongue.