Abstract
Ankle dorsiflexion force control is essential for performing daily living activities. However, the involvement of the corticospinal pathway during different ankle dorsiflexion tasks is not well understood. The objective of this study was to compare the corticospinal excitability during: (1) unilateral and bilateral; and (2) ballistic and tonic ankle dorsiflexion force control. Fifteen healthy young adults (age: 25.2 ± 2.8 years) participated in this study. Participants performed unilateral and bilateral isometric ankle dorsiflexion force-control tasks, which required matching a visual target (10% of maximal effort) as quickly and precisely as possible during ballistic and tonic contractions. Transcranial magnetic stimulation (TMS) was applied over the primary motor cortex to elicit motor-evoked potentials (MEPs) from the right tibialis anterior during: (i) pre-contraction phase; (ii) ascending contraction phase; (iii) plateau phase (tonic tasks only); and (iv) resting phase (control). Peak-to-peak MEP amplitude was computed to compare the corticospinal excitability during each experimental condition. MEP amplitudes significantly increased during unilateral contraction compared to bilateral contraction in the pre-contraction phase. There were no significant differences in the MEP amplitudes between the ballistic tasks and tonic tasks in any parts of the contraction phase. Although different strategies are required during ballistic and tonic contractions, the extent of corticospinal involvement appears to be similar. This could be because both tasks enhance the preparation for precise force control. Furthermore, our results suggest that unilateral muscle contractions may largely facilitate the central nervous system during movement preparation for unilateral force control compared to bilateral muscle contractions.
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References
Bastian AJ (2006) Learning to predict the future: the cerebellum adapts feedforward movement control. Curr Opin Neurobiol 16:645–649
Beaulé V, Tremblay S, Théoret H (2012) Interhemispheric control of unilateral movement. Neural Plast 2012:1–11. https://doi.org/10.1155/2012/627816
Chen R, Yaseen Z, Cohen LG, Hallett M (1998) Time course of corticospinal excitability in reaction time and self- paced movements. Ann Neurol 44:317–325. https://doi.org/10.1002/ana.410440306
Davranche K, Temesi J, Verges S, Hasbroucq T (2015) Transcranial magnetic stimulation probes the excitability of the primary motor cortex: a framework to account for the facilitating effects of acute whole-body exercise on motor processes. J Sport Health Sci 4:24–29. https://doi.org/10.1016/j.jshs.2014.09.001
Duque J, Murase N, Celnik P et al (2007) Intermanual differences in movement-related interhemispheric inhibition. J Cogn Neurosci 19:204–213. https://doi.org/10.1162/jocn.2007.19.2.204
Ferbert A, Priorit A, Rothwell JC et al (1992) Interhemispheric inhibition of the human motor cortex. J Physiol 453:525–546. https://doi.org/10.1113/jphysiol.1992.sp019243
Fling BW, Seidler RD (2012) Task-dependent effects of interhemispheric inhibition on motor control. Behav Brain Res 226:211–217. https://doi.org/10.1016/j.bbr.2011.09.018
Geertsen SS, Zuur AT, Nielsen JB (2010) Voluntary activation of ankle muscles is accompanied by subcortical facilitation of their antagonists. J Physiol 588:2391–2402. https://doi.org/10.1113/jphysiol.2010.190678
Grefkes C, Eickhoff SB, Nowak DA et al (2008) Dynamic intra- and interhemispheric interactions during unilateral and bilateral hand movements assessed with fMRI and DCM. Neuroimage 41:1382–1394. https://doi.org/10.1016/j.neuroimage.2008.03.048
Hirose S, Nambu I, Naito E (2018) Cortical activation associated with motor preparation can be used to predict the freely chosen effector of an upcoming movement and reflects response time: an fMRI decoding study. Neuroimage 183:584–596. https://doi.org/10.1016/j.neuroimage.2018.08.060
Hodges PW, Bui BH (1996) A comparison of computer-based methods for the determination of onset of muscle contraction using electromyography. Electroencephalo Clin Neurophysiol 101:511–519. https://doi.org/10.1016/S0921-884X(96)95190-5
Holl N, Zschorlich V (2011) Neural control of joint stability during a ballistic force production task. Exp Brain Res 210:229–242. https://doi.org/10.1007/s00221-011-2618-y
Kagamihara Y, Komiyama T, Ohi K, Tanaka R (1992) Facilitation of agonist motoneurons upon initiation of rapid and slow voluntary movements in man. Neurosci Res 14:1–11. https://doi.org/10.1016/S0168-0102(05)80002-1
Kawato M (1999) Internal models for motor control and trajectory planning Mitsuo Kawato. Curr Opin Neurobiol 9:718–727. https://doi.org/10.1016/s0959-4388(99)00028-8
Keller M, Taube W, Lauber B (2018) Task-dependent activation of distinct fast and slow (er) motor pathways during motor imagery. Brain Stimul 11:782–788. https://doi.org/10.1016/j.brs.2018.02.010
Kennefick M, Burma JS, van Donkelaar P, McNeil CJ (2019) Corticospinal excitability is enhanced while preparing for complex movements. Exp Brain Res 237:829–837. https://doi.org/10.1007/s00221-018-05464-0
Khodiguian N, Cornwell A, Lares E et al (2003) Expression of the bilateral deficit during reflexively evoked contractions. J Appl Physiol 94:171–178. https://doi.org/10.1152/japplphysiol.00703.2002
Kluding PM, Dunning K, O’Dell MW et al (2013) Foot drop stimulation versus ankle foot orthosis after stroke: 30-week outcomes. Stroke 44:1660–1669. https://doi.org/10.1161/STROKEAHA.111.000334
Liuzzi G, Zimerman M, Gerloff C et al (2011) Coordination of Uncoupled Bimanual Movements by Strictly Timed Interhemispheric Connectivity. J Neurosci 31:9111–9117. https://doi.org/10.1523/jneurosci.0046-11.2011
Meyer BU, Röricht S, Von Einsiedel HG et al (1995) Inhibitory and excitatory interhemispheric transfers between motor cortical areas in normal humans and patients with abnormalities of the corpus callosum. Brain 118:429–440. https://doi.org/10.1093/brain/118.2.429
Nielsen J, Petersen N, Deuschlt G, Ballegaard M (1993) Task-related changes in the effect of magnetic brain stimulation on spinal neurones in man. J Physiol 471:223–243. https://doi.org/10.1113/jphysiol.1993.sp019899
Oda S, Moritani T (1995) Movement-related cortical potentials during handgrip contractions with special reference to force and electromyogram bilateral deficit. Eur J Appl Physiol Occup Physiol 72:1–5. https://doi.org/10.1007/BF00964106
Otsuki T (1983) Decrease in human voluntary isometric arm strength induced by simultaneous bilateral exertion. Behav Brain Res 7:165–178. https://doi.org/10.1016/0166-4328(83)90190-0
Perez MA, Butler JE, Taylor JL (2014) Modulation of transcallosal inhibition by bilateral activation of agonist and antagonist proximal arm muscles. J Neurophysiol 111:405–414. https://doi.org/10.1152/jn.00322.2013
Pollok B, Gross J, Kamp D, Schnitzler A (2008) Evidence for anticipatory motor control within a cerebello-diencephalic- parietal network. J Cogn Neurosci 20:828–840. https://doi.org/10.1162/jocn.2008.20506
Rossi S, Hallett M, Rossini PM, Pascual-Leone A (2011) Screening questionnaire before TMS: an update. Clin Neurophysiol 122:1686. https://doi.org/10.1016/j.clinph.2010.12.037
Rossini PM, Burke D, Chen R et al (2015) Non-invasive electrical and magnetic stimulation of the brain, spinal cord, roots and peripheral nerves: basic principles and procedures for routine clinical and research application. An updated report from an I.F.C.N. Committee Clin Neurophysiol 126:1071–1107. https://doi.org/10.1016/j.clinph.2015.02.001
Roy FD, Norton JA, Gorassini MA (2007) Role of sustained excitability of the leg motor cortex after transcranial magnetic stimulation in associative plasticity. J Neurophysiol 98:657–667. https://doi.org/10.1152/jn.00197.2007
Schneider C, Lavoie BA, Barbeau H, Capaday C (2004) Timing of cortical excitability changes during the reaction time of movements superimposed on tonic motor activity. J Appl Physiol 97:2220–2227. https://doi.org/10.1152/japplphysiol.00542.2004
Schneiders AG, Sullivan SJ, Malley KJO et al (2010) A Valid and Reliable Clinical Determination of Footedness. Phys Med Rehabil 2:835–841. https://doi.org/10.1016/j.pmrj.2010.06.004
Škarabot J, Cronin N, Strojnik V, Avela J (2016) Bilateral deficit in maximal force production. 116:2057–2084 https://doi.org/10.1007/s00421-016-3458-z
Škarabot J, Alfonso RP, Cronin N et al (2016b) Corticospinal and transcallosal modulation of unilateral and bilateral contractions of lower limbs. Eur J Appl Physiol 116:2197–2214. https://doi.org/10.1007/s00421-016-3475-y
Taniguchi Y, Burle B, Vidal F, Bonnet M (2001) Deficit in motor cortical activity for simultaneous bimanual responses. Exp Brain Res 137:259–268. https://doi.org/10.1007/s002210000661
Taube W, Lundbye-jensen J, Schubert M et al (2011) Evidence that the cortical motor command for the initiation of dynamic plantarflexion consists of excitation followed by inhibition. PLoS One 6:4–10. https://doi.org/10.1371/journal.pone.0025657
Terao Y, Ugawa Y, Hanajima R et al (2000) Predominant activation of II-waves from the leg motor area by transcranial magnetic stimulation. Brain Res 859:137–146. https://doi.org/10.1016/S0006-8993(00)01975-2
Thompson AK, Stein RB (2004) Short-term effects of functional electrical stimulation on motor-evoked potentials in ankle flexor and extensor muscles. Exp Brain Res 159:491–500. https://doi.org/10.1007/s00221-004-1972-4
Vieluf S, Godde B, Reuter EM, Voelcker-Rehage C (2013) Effects of age and fine motor expertise on the bilateral deficit in force initiation. Exp Brain Res 231:107–116. https://doi.org/10.1007/s00221-013-3673-3
Vieluf S, Aschersleben G, Panzer S (2017) Lifespan development of the bilateral deficit in a simple reaction time task. Exp Brain Res 235:985–992. https://doi.org/10.1007/s00221-016-4856-5
Yamaguchi A, Milosevic M, Sasaki A, Nakazawa K (2019) Force control of ankle dorsiflexors in young adults: effects of bilateral control and leg dominance. J Mot Behav. https://doi.org/10.1080/00222895.2019.1609408
Ye X, Miller WM, Jeon S, Carr JC (2019) Sex comparisons of the bilateral deficit in proximal and distal upper body limb muscles. Hum Mov Sci 64:329–337. https://doi.org/10.1016/j.humov.2019.02.017
Acknowledgements
This project was supported by the Japan Society for the Promotion of Science (JSPS) Grants-in-Aid for Scientific Research (KAKENHI) [17F17733, 18H04082 and 18KK0272] and CREST, Japan Science and Technology Agency. We thank Dr. Hirofumi Sekiguchi and Dr. Tsuyoshi Nakajima and for providing help during the interpretations.
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Yamaguchi, A., Sasaki, A., Masugi, Y. et al. Changes in corticospinal excitability during bilateral and unilateral lower-limb force control tasks. Exp Brain Res 238, 1977–1987 (2020). https://doi.org/10.1007/s00221-020-05857-0
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DOI: https://doi.org/10.1007/s00221-020-05857-0