Abstract
The aim was to test the hypothesis that short-term oral sensorimotor training of the jaw muscles would increase the precision of task performance and induce neuroplastic changes in the corticomotor pathways, related to the masseter muscle. Fifteen healthy volunteers performed six series with ten trials of an oral sensorimotor task. The task was to manipulate and position a spherical chocolate candy in between the anterior teeth and split it into two equal halves. The precision of the task performance was evaluated by comparing the ratio between the two split halves. A series of “hold-and-split” tasks was also performed before and after the training. The hold force and split force along with the electromyographic (EMG) activity of jaw muscles were recorded. Motor-evoked potentials and cortical motor maps of the right masseter muscle were evoked by transcranial magnetic stimulation. There was a significant effect of series on the precision of the task performance during the short-term oral sensorimotor training (P < 0.002). The hold force during the “hold-and-split” task was significantly lower after training than before the short-term training (P = 0.011). However, there was no change in the split force and the EMG activity of the jaw muscles before and after the training. Further, there was a significant increase in the amplitude of the motor-evoked potentials (P < 0.016) and in the motor cortex map areas (P = 0.033), after the short-term oral sensorimotor training. Therefore, short-term oral sensorimotor task training increased the precision of task performance and induced signs of neuroplastic changes in the corticomotor pathways, related to the masseter muscle.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Avivi-Arber L, Lee J-C, Sessle BJ (2011a) Chapter 9—Face sensorimotor cortex neuroplasticity associated with intraoral alterations. In: Jean Pierre Gossard RD, Arlette K (eds) Progress in brain research, vol 188. Elsevier, Amsterdam, pp 135–150
Avivi-Arber L, Martin R, Lee JC, Sessle BJ (2011b) Face sensorimotor cortex and its neuroplasticity related to orofacial sensorimotor functions. Arch Oral Biol 56:1440–1465. doi:10.1016/j.archoralbio.2011.04.005
Baad-Hansen L, Blicher JU, Lapitskaya N, Nielsen JF, Svensson P (2009) Intra-cortical excitability in healthy human subjects after tongue training. J Oral Rehabil 36:427–434. doi:10.1111/j.1365-2842.2009.01955.x
Boudreau SA, Hennings K, Svensson P, Sessle BJ, Arendt-Nielsen L (2010) The effects of training time, sensory loss and pain on human motor learning. J Oral Rehabil 37:704–718. doi:10.1111/j.1365-2842.2010.02103.x
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
Dellow PG, Lund JP (1971) Evidence for central timing of rhythmical mastication. J Physiol 215:1–13
Duchateau J, Semmler JG, Enoka RM (2006) Training adaptations in the behavior of human motor units. J Appl Physiol 101:1766–1775. doi:10.1152/japplphysiol.00543.2006
Gandolfo F, Li C, Benda BJ, Schioppa CP, Bizzi E (2000) Cortical correlates of learning in monkeys adapting to a new dynamical environment. Proc Natl Acad Sci U S A 97:2259–2263. doi:10.1073/pnas.040567097
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. doi:10.1152/jn.00595.2003
Hellmann D, Giannakopoulos NN, Blaser R, Eberhard L, Rues S, Schindler HJ (2011) Long-term training effects on masticatory muscles. J Oral Rehabil 38:912–920. doi:10.1111/j.1365-2842.2011.02227.x
Iida T, Komiyama O, Obara R, Baad-Hansen L, Kawara M, Svensson P (2014a) Repeated clenching causes plasticity in corticomotor control of jaw muscles. Eur J Oral Sci 122:42–48. doi:10.1111/eos.12101
Iida T, Overgaard A, Komiyama O, Weibull A, Baad-Hansen L, Kawara M, Sundgren PC, List T, Svensson P (2014b) Analysis of brain and muscle activity during low-level tooth clenching—a feasibility study with a novel biting device. J Oral Rehabil 41:93–100. doi:10.1111/joor.12128
Jaberzadeh S, Sakuma S, Zoghi M, Miles TS, Nordstrom MA (2008) Focal transcranial magnetic stimulation of motor cortex evokes bilateral and symmetrical silent periods in human masseter muscles. Clin Neurophysiol 119:693–703. doi:10.1016/j.clinph.2007.11.005
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 U S A 95:861–868
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. doi:10.1523/jneurosci.3440-03.2004
Komoda Y, Iida T, Kothari M, Komiyama O, Baad-Hansen L, Kawara M, Sessle B, Svensson P (2015) Repeated tongue lift movement induces neuroplasticity in corticomotor control of tongue and jaw muscles in humans. Brain Res. doi:10.1016/j.brainres.2015.09.016
Kothari M, Svensson P, Jensen J, Kjaersgaard A, Jeonghee K, Nielsen JF, Ghovanloo M, Baad-Hansen L (2013) Training-induced cortical plasticity compared between three tongue-training paradigms. Neuroscience 246:1–12. doi:10.1016/j.neuroscience.2013.04.040
Kothari M, Svensson P, Nielsen JF, Baad-Hansen L (2014) Influence of position and stimulation parameters on intracortical inhibition and facilitation in human tongue motor cortex. Brain Res 1557:83–89. doi:10.1016/j.brainres.2014.02.017
Kumar A, Svensson KG, Baad-Hansen L, Trulsson M, Isidor F, Svensson P (2014) Optimization of jaw muscle activity and fine motor control during repeated biting tasks. Arch Oral Biol 59:1342–1351. doi:10.1016/j.archoralbio.2014.08.009
Kumar A, Castrillon E, Svensson KG, Baad-Hansen L, Trulsson M, Svensson P (2015a) Effects of experimental craniofacial pain on fine jaw motor control: a placebo-controlled double-blinded study. Exp Brain Res. doi:10.1007/s00221-015-4245-5
Kumar A, Castrillon E, Svensson P (2015b) Can experimentally evoked pain in the jaw muscles or temporomandibular joint affect anterior bite force in humans? J Oral Facial Pain Headache 29:31–40. doi:10.11607/ofph.1268
Kumar A, Grigoriadis J, Trulsson M, Svensson P, Svensson KG (2015c) Effects of short-term training on behavioral learning and skill acquisition during intraoral fine motor task. Neuroscience 306:10–17. doi:10.1016/j.neuroscience.2015.06.065
Lotze M, Braun C, Birbaumer N, Anders S, Cohen LG (2003) Motor learning elicited by voluntary drive. Brain 126:866–872
Lu S, Baad-Hansen L, Zhang Z, Svensson P (2013) One hour jaw muscle training does not evoke plasticity in the corticomotor control of the masseter muscle. Arch Oral Biol 58:1483–1490. doi:10.1016/j.archoralbio.2013.06.012
Lund JP (1991) Mastication and its control by the brain stem. Crit Rev Oral Biol Med 2:33–64
Lund JP, Kolta A (2006) Generation of the central masticatory pattern and its modification by sensory feedback. Dysphagia 21:167–174. doi:10.1007/s00455-006-9027-6
McMillan AS, Watson C, Walshaw D (1998) Transcranial magnetic-stimulation mapping of the cortical topography of the human masseter muscle. Arch Oral Biol 43:925–931
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
Perez MA, Lungholt BK, Nyborg K, Nielsen JB (2004) Motor skill training induces changes in the excitability of the leg cortical area in healthy humans. Exp Brain Res 159:197–205. doi:10.1007/s00221-004-1947-5
Ridding MC, Rothwell JC (1995) Reorganisation in human motor cortex. Can J Physiol Pharmacol 73:218–222
Sessle BJ (2011) Chapter 5-face sensorimotor cortex: its role and neuroplasticity in the control of orofacial movements. Prog Brain Res 188:71–82. doi:10.1016/b978-0-444-53825-3.00010-3
Sessle BJ, Adachi K, Avivi-Arber L, Lee J, Nishiura H, Yao D, Yoshino K (2007) Neuroplasticity of face primary motor cortex control of orofacial movements. Arch Oral Biol 52:334–337. doi:10.1016/j.archoralbio.2006.11.002
Stefan K, Kunesch E, Cohen LG, Benecke R, Classen J (2000) Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 123(Pt 3):572–584
Svensson KG, Trulsson M (2009) Regulation of bite force increase during splitting of food. Eur J Oral Sci 117:704–710. doi:10.1111/j.1600-0722.2009.00691.x
Svensson KG, Trulsson M (2011) Impaired force control during food holding and biting in subjects with tooth- or implant-supported fixed prostheses. J Clin Periodontol 38:1137–1146. doi:10.1111/j.1600-051X.2011.01781.x
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 152:42–51. doi:10.1007/s00221-003-1517-2
Svensson P, Romaniello A, Wang K, Arendt-Nielsen L, Sessle BJ (2006) One hour of tongue-task training is associated with plasticity in corticomotor control of the human tongue musculature. Exp Brain Res 173:165–173. doi:10.1007/s00221-006-0380-3
Svensson KG, Grigoriadis J, Trulsson M (2013) Alterations in intraoral manipulation and splitting of food by subjects with tooth- or implant-supported fixed prostheses. Clin Oral Implants Res 24:549–555. doi:10.1111/j.1600-0501.2011.02418.x
Trulsson M (2006) Sensory-motor function of human periodontal mechanoreceptors. J Oral Rehabil 33:262–273. doi:10.1111/j.1365-2842.2006.01629.x
Trulsson M, Gunne HS (1998) Food-holding and -biting behavior in human subjects lacking periodontal receptors. J Dent Res 77:574–582
Trulsson M, Johansson RS (1996a) Encoding of tooth loads by human periodontal afferents and their role in jaw motor control. Prog Neurobiol 49:267–284
Trulsson M, Johansson RS (1996b) Forces applied by the incisors and roles of periodontal afferents during food-holding and -biting tasks. Exp Brain Res 107:486–496
Tyc F, Boyadjian A (2006) Cortical plasticity and motor activity studied with transcranial magnetic stimulation. Rev Neurosci 17:469–495
Watson C, Walshaw D, McMillan AS (2000) Effect of motor tasks on the cortical topography of the human masseter muscle. Arch Oral Biol 45:767–773
Westberg KG, Kolta A (2011) The trigeminal circuits responsible for chewing. Int Rev Neurobiol 97:77–98. doi:10.1016/b978-0-12-385198-7.00004-7
Wilson SA, Thickbroom GW, Mastaglia FL (1993) Transcranial magnetic stimulation mapping of the motor cortex in normal subjects. The representation of two intrinsic hand muscles. J Neurol Sci 118:134–144
Acknowledgments
The Section of Orofacial pain and Jaw Function, Department of Dentistry, Aarhus University, Denmark, Colgate–Palmolive A/S, Denmark, and Danish Dental Association, Denmark, funded this study.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Zhang, H., Kumar, A., Kothari, M. et al. Can short-term oral fine motor training affect precision of task performance and induce cortical plasticity of the jaw muscles?. Exp Brain Res 234, 1935–1943 (2016). https://doi.org/10.1007/s00221-016-4598-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-016-4598-4