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

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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 24–35 years (mean age ± SD: 27.3 ± 0.3 years), 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 1.0 N as the target at the hold phase lasting for 1.5 s. Subjects repeated this task for 1 h. 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 1 h post-training. One day after the training, increased activity was observed in the precentral gyrus, SMA, putamen, and cerebellum. No increase was found 1 week 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 1 h, 1 day, and 1 week after the tongue-task training and for the left Area 4p in primary motor cortex and the left lateral premotor cortex 1 day after the training. In the unrestricted analysis, increased activity was found in the parahippocampal gyrus 1 h after the tongue-task training and remained for a week. Decreased activity was found in right post-central and middle frontal gyri 1 h and 1 week 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 1 week) 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.

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Acknowledgments

BJS involvement was supported by CIHR grant MT-4918.

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Authors and Affiliations

  1. Department of Oral Rehabilitation, Graduate School of Dental Medicine, University of Hokkaido, Sapporo, Japan

    Taro Arima & Noboru Ohata

  2. Department of Oral Diagnosis and Dentomaxillofacial Radiology, Okayama University Hospital, Okayama, Japan

    Yoshinobu Yanagi

  3. Institute of Brain Science, National Yang-Ming University, Taipei, Taiwan

    David M. Niddam

  4. Center for Sensory-Motor Interaction, University of Aalborg, Aalborg, Denmark

    Lars Arendt-Nielsen

  5. Department of Occlusal and Oral Functional Rehabilitation, Graduate School of Medicine, Dentistry, and Pharmaceutical Sciences, University of Okayama, Okayama, Japan

    Shogo Minagi

  6. Faculty of Dentistry, University of Toronto, Toronto, Canada

    Barry J Sessle

  7. Department of Clinical Oral Physiology, University of Aarhus, Vennelyst Boulevard 9, 8000, Aarhus, Denmark

    Peter Svensson

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  1. Taro Arima
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Arima, T., Yanagi, Y., Niddam, D.M. et al. Corticomotor plasticity induced by tongue-task training in humans: a longitudinal fMRI study. Exp Brain Res 212, 199–212 (2011). https://doi.org/10.1007/s00221-011-2719-7

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