Skip to main content
SpringerLink
Log in

One hour of tongue-task training is associated with plasticity in corticomotor control of the human tongue musculature

Experimental Brain Research Aims and scope Submit manuscript

Cite this article

Abstract

Corticomotor control of the human tongue has been reported to undergo neuroplastic changes following several days of training in a tongue-protrusion task. The aims of the present study were to determine if a 1 h tongue-task training is sufficient to induce signs of neuroplastic changes in the corticomotor pathways, and to obtain preliminary information on the time course of such changes. Corticomotor excitability was assessed by changes in electromyographic activity evoked by transcortical magnetic stimulation (TMS) in 11 healthy subjects. Motor evoked potentials (MEPs) recorded in the tongue musculature and the first dorsal interosseous (FDI) muscle were assessed at four sessions: at baseline before training, 30 min after training, and 1 and 7 days after training. All subjects performed successfully the task (success rate: 38±4%). Thresholds for evoking MEPs by TMS in the tongue were decreased at 30 min, 1 and 7 days after training compared with baseline (ANOVA: P<0.001). Tongue MEP amplitudes were significantly increased at 1 day follow-up and had returned to baseline values at 7 days follow-up (ANOVA: P<0.001). No significant effect of tongue-task training on FDI MEPs was observed (ANOVA: P=0.160). Corticomotor topographic maps revealed increases (ANOVA: P<0.001) in area at the 1 day follow-up. The success rate was significantly correlated to the net increases in tongue MEPs at 1 day follow-up (Spearman: 0.615; P=0.0039). The present findings confirm that tongue task training is associated with plasticity of corticomotor excitability specifically related to the tongue musculature and further document that plasticity is evident within 30 min post-training and may last up to at least 7 days.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aou S, Woody CD, Birt D (1992) Increases in excitability of neurons of the motor cortex of cats after rapid acquisition of eye blink conditioning. J Neurosci 12:560–569

    PubMed  CAS  Google Scholar 

  • Carlstedt K, Henningsson G, Dahllof G (2003) A four-year longitudinal study of palatal plate therapy in children with Down syndrome: effects on oral motor function, articulation and communication preferences. Acta Odontol Scand 61:39–46

    PubMed  Google Scholar 

  • Classen J, Liepert J, Wise SP, Hallett M, Cohen LG (1998) Rapid plasticity of human cortical movement representation induced by practice. J Neurophysiol 79:1117–1123

    PubMed  CAS  Google Scholar 

  • Corfield DR, Murphy K, Josephs O, Fink GR, Frackowiak RSJ, Guz A, Adams L, Turner R (1999) Cortical and subcortical control of tongue movement in humans: a functional neuroimaging study using fMRI. J Appl Physiol 86:1468–1477

    PubMed  CAS  Google Scholar 

  • Di Lazzaro V, Oliviero A, Profice P, Saturno E, Pilato F, Insola A, Mazzone P, Tonali P, Rothwell JC (1998) Comparison of descending volleys evoked by transcranial magnetic and electric stimulation in conscious humans. Electroencephalogr Clin Neurophysiol 109:397–401

    Article  PubMed  CAS  Google Scholar 

  • Dubner R, Sessle BJ, Storey AT (1978) The neural basis of oral and facial function. Plenum, New York

    Google Scholar 

  • Fadiga L, Craighero L, Buccino G, Rizzolatti G (2002) Speech listening specifically modulates the excitability of tongue muscles: a TMS study. Eur J Neurosci 15:399–402

    Article  PubMed  Google Scholar 

  • Fischer-Brandies H, Avalle C, Limbrock GJ (1987) Therapy of orofacial dysfunctions in cerebral palsy according to Castillo-Morales: first results of a new treatment concept. Eur J Orthod 9:139–143

    PubMed  CAS  Google Scholar 

  • Garry MI, Kamen G, Nordstrom MA (2004) Hemispheric differences in the relationship between corticomotor excitability changes following a fine-motor task and motor learning. J Neurophysiol 91:1570–1578

    Article  PubMed  Google Scholar 

  • Halkjaer L, Melsen B, McMillan AS, Svensson P (2005) Influence of sensory deprivation and perturbation of trigeminal afferent fibers on corticomotor control of human tongue musculature. Exp Brain Res 17:1–7

    Article  Google Scholar 

  • Hallett M, Chen R, Ziemann U, Cohen LG (1999) Reorganization in motor cortex in amputees and in normal volunteers after ischemic limb deafferentation. Electroencephalogr Clin Neurophysiol Suppl 51:183–187

    PubMed  CAS  Google Scholar 

  • Hesselmann V, Sorger B, Lasek K, Guntinas-Lichius O, Krug B, Sturm V, Goebel R, Lackner K (2004) Discriminating the cortical representation sites of tongue and up movement by functional MRI. Brain Topogr 116:159–167

    Google Scholar 

  • Hiiemae KM, Palmer JB (2003) Tongue movements in feeding and speech. Crit Rev Oral Biol Med 14:413–429

    Article  PubMed  Google Scholar 

  • Karni A, Jezzard P, Adams MM, Turner R, Ungerleider LG (1995) Functional MRI evidence for adult motor cortex plasticity during skill learning. Science 377:155–158

    CAS  Google Scholar 

  • Karni A, Meyer G, Rey-Hipolito C, Jezzard P, Adams MM, Turner R, Ungerleider LG (1998) The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex. Proc Natl Acad Sci USA 95:861–868

    Article  PubMed  CAS  Google Scholar 

  • Kleim JA, Barbay S, Cooper NR, Hogg TM, Reidel CN, Remple MS, Nudo RJ (2002) Motor learning-dependent synaptogenesis is localized to functionally reorganized motor cortex. Neurobiol Learn Mem 77:63–77

    Article  PubMed  Google Scholar 

  • Kleim JA, Hogg TM, VandenBerg PM, Cooper NR, Bruneau R, Remple M (2004) Cortical synaptogenesis and motor map reorganization occur during late, but not early, phase of motor skill learning. J Neurosci 24:628–633

    Article  PubMed  CAS  Google Scholar 

  • Kleim JA, Lussnig E, Schwarz ER, Comery TA, Greenough WT (1996) Synaptogenesis and Fos expression in the motor cortex of the adult rat after motor skill learning. J Neurosci 16:4529–4535

    PubMed  CAS  Google Scholar 

  • Martin R, Murray GM, Kemppainen P, Masuda Y, Sessle BJ (1997) Functional properties of neurons in the primate tongue primary motor cortex during swallowing. J Neurophysiol 78:1516–1530

    PubMed  CAS  Google Scholar 

  • Martin RE, Kemppainen P, Masuda Y, Yao DY, Murray GM, Sessle BJ (1999) Features of cortically evoked swallowing in the awake primate (macaca fascicularis). J Neurophysiol 82:1529–1541

    PubMed  CAS  Google Scholar 

  • McMillan AS, Watson C, Walshaw D (1998) Improved reproducibility of magnetic stimulation-evoked motor potentials in the human masseter by a new method for locating stimulation sites on the scalp. Archs Oral Biol 43:665–668

    Article  CAS  Google Scholar 

  • Meyer B-U, Liebsch R, Röricht S (1997) Tongue motor responses following transcranial magnetic stimulation of the motor cortex and proximal hypoglossal nerve in man. Electroencephalog Clin Neurophysiol 105:15–23

    Article  CAS  Google Scholar 

  • Miller AJ (2002) Oral and pharyngeal reflexes in the mammalian nervous system: their diverse range in complexity and the pivotal role of the tongue. Crit Rev Oral Biol Med 13:409–425

    PubMed  CAS  Google Scholar 

  • Muellbacher W, Boroojerdi B, Ziemann U, Hallett M (2001) Analogous corticocortical inhibition and facilitation in ipsilateral and contralateral human motor cortex representations of the tongue. J Clin Neurophysiol 18:550–558

    Article  PubMed  CAS  Google Scholar 

  • Muellbacher W, Mathis J, Hess CW (1994) Electrophysiological assessment of central and peripheral motor routes to the lingual muscles. J Neurol Neurosurg Psychiatry 57:309–315

    PubMed  CAS  Google Scholar 

  • Muellbacher W, Ziemann U, Boroojerdi B, Cohen L, Hallett M (2001) Role of the human motor cortex in rapid motor learning. Exp Brain Res 136:431–438

    Article  PubMed  CAS  Google Scholar 

  • Muellbacher W, Ziemann U, Wissel J, Dang N, Kofler M, Facchini S, Boroojerdi B, Poewe W, Hallett M (2002) Early consolidation in human primary motor cortex. Nature 415:640–644

    Article  PubMed  CAS  Google Scholar 

  • Murray GM, Lin L-D, Moustafa EM, Sessle BJ (1991) Effects of reversible inactivation by cooling of the primate face motor cortex on the performance of a trained tongue-protrusion task and a trained biting task. J Neurophysiol 65:511–530

    PubMed  CAS  Google Scholar 

  • Murray GM, Sessle BJ (1992a) Functional properties of single neurons in the face primary motor cortex of the primate. I. Input and output feature so tongue motor cortex J Neurophysiol 67:747–758

    CAS  Google Scholar 

  • Murray GM, Sessle BJ (1992b) Functional properties of single neurons in the face primary motor cortex of the primate. II. Relations with trained orofacial motor behavior. J Neurophysiol 67:759–774

    CAS  Google Scholar 

  • Murray GM, Sessle BJ (1992c) Functional properties of single neurons in the face primary motor cortex of the primate. III. Relations with different directions of trained tongue protrusion. J Neurophysiol 67:775–785

    CAS  Google Scholar 

  • Nakasato N, Itoh H, Hatanaka K, Nakahara H, Kanno A, Yoshimoto T (2001) Movement-related magnetic fields to tongue protrusion. Neuroimage 14:924–935

    Article  PubMed  CAS  Google Scholar 

  • Pascual-Leone A, Grafman J, Hallett M (1994) Modulation of cortical motor output maps during development of implicit and explicit knowledge. Science 263:1287–1289

    Article  PubMed  CAS  Google Scholar 

  • Ray J (2001) Functional outcomes of orofacial myofunctional therapy in children with cerebral palsy. Int J Orofacial Myology 27:5–17

    PubMed  CAS  Google Scholar 

  • Remple MS, Bruneau RM, Van den Berg PM, Goertzen C, Kleim JA (2001) Sensitivity of cortical movement representations to motor experience: evidence that skill learning but not strength training induces cortical reorganization. Behav Brain Res 123:133–141

    Article  PubMed  CAS  Google Scholar 

  • Ridding MC, Brouwer B, Miles TS, Pitcher JB, Thompson PD (2000) Changes in muscle responses to stimulation of the motor cortex induced by peripheral nerve stimulation in human subjects. Exp Brain Res 131:135–143

    Article  PubMed  CAS  Google Scholar 

  • Rioult-Pedotti MS, Friedman D, Hess G, Donoghue JP (1998) Strengthening of horizontal cortical connections following skill learning. Nat Neurosci 1:230–234

    Article  PubMed  CAS  Google Scholar 

  • Rödel RM, Laskawi R, Markus H (2003) Tongue representation in the lateral cortical motor region of the human brain as assessed by transcranial magnetic stimulation. Ann Otol Rhinol Laryngol 112:71–76

    PubMed  Google Scholar 

  • Rösler KM, Schmid UD, Hess CW (1991) Transcranial magnetic stimulation of the facial nerve: where is the actual excitation site? Electroencephalogr Clin Neurophysiol 43:362–368

    Google Scholar 

  • Sanes JN, Donoghue JP (2000) Plasticity and primary motor cortex. Annu Rev Neurosci 23:393–415

    Article  PubMed  CAS  Google Scholar 

  • Sawczuk A, Mosier KM (2001) Neural control of tongue movement with respect to respiration and swallowing. Crit Rev Oral Biol Med 112:18–37

    Article  Google Scholar 

  • Sessle BJ, Yao D, Nishiura H, Yoshino K, Lee JC, Martin RE, Murray GM (2005) Properties and plasticity of the primate somatosensory and motor cortex related to orofacial sensorimotor function. Clin Exp Pharmacol Physiol 32:109–114

    Article  PubMed  Google Scholar 

  • Sessle BJ, Yao D (2002) Contribution of plasticity of sensorimotor cerebral cortex to development of communication skills. Commentary on Stuart G, Shanker SG and King BJ. Behav Brain Sci 25:638–639

    Article  Google Scholar 

  • Shinagawa H, Ono T, Ishiwata Y, Honda E, Sasaki T, Taira M, Iriki A, Kuroda T (2003) Hemispheric dominance of tongue control depends on the chewing-side preference. J Dent Res 82:278–283

    PubMed  CAS  Google Scholar 

  • Smith A (1992) The control of orofacial movements in speech. Crit Rev Oral Biol Med 3:233–267

    PubMed  CAS  Google Scholar 

  • Svensson P, Romaniello A, Arendt-Nielsen L, Sessle BJ (2003) Plasticity in corticomotor control of the human tongue musculature induced by tongue-task training. Exp Brain Res 1152:42–51

    Article  Google Scholar 

  • Ungerleider LG, Doyon J, Karni A (2002) Imaging brain plasticity during motor skill learning. Neurobiol Learn Mem 78:553–564

    Article  PubMed  Google Scholar 

  • Uy J, Ridding MC, Miles TS (2002) Stability of maps of human motor cortex made with transcranial magnetic stimulation. Brain Topogr 14:293–297

    Article  PubMed  Google Scholar 

  • Watanabe J, Sugiura M, Miura N, Watanabe Y, Maeda Y, Matsue Y, Kawashima R (2004) The human parietal cortex is involved in spatial processing of tongue movement: an fMRI study. Neuroimage 21:1289–1299

    Article  PubMed  Google Scholar 

  • Wilson SA, Thickbroom GW, Mastaglia FL (1993) Transcranial magnetic stimulation mapping of the motor cortex in normal subjects. J Neurol Sci 118:134–144

    Article  PubMed  CAS  Google Scholar 

  • Yamamura K, Narita N, Yao D, Martin RE, Masuda Y, Sessle BJ (2002) Effects of reversible bilateral inactivation of face primary motor cortex on mastication and swallowing. Brain Res 944:40–55

    Article  PubMed  CAS  Google Scholar 

  • Yao D, Yamamura K, Narita N, Martin RE, Murray GM, Sessle BJ (2002a) Neuronal activity patterns in primate primary motor cortex related to trained or semiautomatic jaw and tongue movements. J Neurophysiol 87:2531–2541

    Google Scholar 

  • Yao D, Yamamura K, Narita N, Murray GM, Sessle BJ (2002b) Effects of reversible cold block of face primary somatosensory cortex on orofacial movements and related face primary motor cortex neuronal activity. Somatosens Motor Res 19:261–271

    Article  Google Scholar 

  • Yao DY, Yoshino K, Nishiura H, Yamamura K, Sessle BJ (2002c) Plasticity in primate primary motor cortex (MI) associated with learning of tongue-protrusion task. Program No. 662.9. Abstract viewer/itinerary planner. Society for Neuroscience, Washington, DC

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

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

    P. Svensson, A. Romaniello, K. Wang & L. Arendt-Nielsen

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

    P. Svensson

  3. Department of Oral Maxillofacial Surgery, Aarhus University Hospital, Vennelyst Boulevard 9, 8000, Aarhus C, Denmark

    P. Svensson

  4. Department of Neurological Sciences, University “La Sapienza”, Rome, Italy

    A. Romaniello

  5. Faculty of Dentistry, University of Toronto, M5G 1G6, Toronto, ONT, Canada

    B.J. Sessle

Authors
  1. P. Svensson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Romaniello
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. K. Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. L. Arendt-Nielsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. B.J. Sessle
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to P. Svensson.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Svensson, P., Romaniello, A., Wang, K. et al. One hour of tongue-task training is associated with plasticity in corticomotor control of the human tongue musculature. Exp Brain Res 173, 165–173 (2006). https://doi.org/10.1007/s00221-006-0380-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-006-0380-3

Keywords

search

Navigation