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Plasticity in corticomotor control of the human tongue musculature induced by tongue-task training

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Abstract

Transcranial magnetic stimulation (TMS) has been used to assess characteristics of the corticomotor control of the jaw muscles, but less is known about the cortical control of the human tongue and its modification by training. The aim of the present study was to determine the effect of training humans in a novel tongue-protrusion task for 1 week on corticomotor excitability as assessed by changes in electromyographic activity elicited in the tongue musculature by TMS, and in the tongue cortical motor map revealed by TMS. Eleven healthy subjects participated. Stimulus–response curves were generated from the motor evoked potentials (MEPs) recorded in the tongue musculature and, from the first dorsal interosseos (FDI) muscle as a control, at three time periods: at baseline, immediately after the 1-week training period, and at 2-weeks follow-up. In addition, the corticomotor representations of the tongue and FDI muscles were mapped on a 1×1 cm scalp grid. The tongue-training task required each subject to protrude the tongue onto a force transducer placed in front of the subject, and consisted of a relax–protrude–hold–relax cycle lasting 12.5 s with 1 N as the target at the hold phase. The subjects repeated this task for 60 min every day for 1 week. All subjects reported moderate levels of fatigue in the tongue during the first training day; however, these subjective reports decreased during the week (ANOVA P<0.001), and the subjects showed a progressive increase in their ability to perform the task successfully (P<0.001). The threshold for evoking MEPs by TMS in the tongue musculature was significantly decreased after the last training day compared with baseline and the 2-weeks follow-up (P<0.001). The amplitude of the MEPs in the tongue musculature was significantly increased at higher intensities of TMS after the last training day but returned to baseline values at the 2-weeks follow-up (P=0.005). No significant effect of the training on MEPs in the FDI was observed (P=0.493). Analysis of the corticomotor topographic maps revealed a significant (P<0.05) increase in excitability and, hence, the cortical area from which TMS could evoke MEPs in the tongue, although the center of gravity representation for the tongue or FDI muscles remained stable. The present findings suggest that a specific and reversible plasticity of the corticomotor excitability related to tongue muscle control can be induced when humans learn to perform successfully a novel tongue task.

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Acknowledgements

We gratefully acknowledge the support of the Danish Technical Research Council, and the Canadian Institutes for Health Research (grant MT-4918). BJS is the holder of a Canada Research Chair.

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Authors and Affiliations

  1. Orofacial Pain Laboratory, Center for Sensory-Motor Interaction, Aalborg University, Aalborg, Denmark

    Peter Svensson, Antonietta Romaniello & Lars Arendt-Nielsen

  2. Department of Clinical Oral Physiology, Dental School, Aarhus University, Vennelyst Boulevard 9, 8000, Aarhus C, Denmark

    Peter Svensson

  3. Department of Neurological Sciences, University "La Sapienza", Rome, Italy

    Antonietta Romaniello

  4. Faculty of Dentistry, The University of Toronto, Toronto, Ontario M5G 1G6, Canada

    Barry J. Sessle

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  1. Peter Svensson
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  2. Antonietta Romaniello
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  4. Barry J. Sessle
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Correspondence to Peter Svensson.

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Svensson, P., Romaniello, A., Arendt-Nielsen, L. et al. Plasticity in corticomotor control of the human tongue musculature induced by tongue-task training. Exp Brain Res 152, 42–51 (2003). https://doi.org/10.1007/s00221-003-1517-2

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