Abstract
Purpose
Extensive evidence exists that regular physical exercise offers neuroplastic benefits to the brain. In this study, exercise-specific effects on motor cortex plasticity were compared between 15 skilled and 15 endurance trained athletes and 8 controls.
Methods
Plasticity was tested with a paired associative stimulation (PAS) protocol. PAS is a non-invasive stimulation method developed to induce bidirectional changes in the excitability of the cortical projections to the target muscles. Motor cortex excitability was assessed by motor-evoked potentials (MEPs) in the task-relevant soleus muscle, elicited with transcranial magnetic stimulation, before and following PAS. To test for changes at the spinal level, soleus short latency stretch reflexes (SLSR) were elicited before and after PAS.
Results
PAS induced a significant (76 ± 83 %) increase in MEP amplitude in the skill group, without significant changes in the endurance (−7 ± 35 %) or control groups (21 ± 30 %). Baseline MEP/post MEP ratio was significantly different between the skill and endurance groups. SLSR remained unchanged after the PAS intervention.
Conclusion
The possible reason for differential motor cortex plasticity in skill and endurance groups is likely related to the different training-induced adaptations. The findings of the current study suggest that long-term skill training by skill group induced preferable adaptations in the task-related areas of the motor cortex because increased plasticity is known to enhance motor learning.
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Abbreviations
- EMG:
-
Electromyography
- LTP:
-
Long-term potentiation
- MEP:
-
Motor-evoked potential
- MVC:
-
Maximal voluntary contraction
- PAS:
-
Paired associative stimulation
- RMT:
-
Resting motor threshold
- SLSR:
-
Short latency stretch reflex
- TMS:
-
Transcranial magnetic stimulation
References
Adkins DL, Boychuk J, Remple MS, Kleim JA (2006) Motor training induces experience-specific patterns of plasticity across motor cortex and spinal cord. J Appl Physiol 101:1776–1782
Ahtiainen JP, Hulmi JJ, Kraemer WJ, Lehti M, Pakarinen A, Mero AA, Karavirta L, Sillanpää E, Selänne H, Alen M, Komulainen J, Kovanen V, Nyman K, Häkkinen K (2009) Strength, [corrected] endurance or combined training elicit diverse skeletal muscle myosin heavy chain isoform proportion but unaltered androgen receptor concentration in older men. Int J Sports Med 30:879–887
Alricsson M, Harms-Ringdahl K, Eriksson K, Werner S (2003) The effect of dance training on joint mobility, muscle flexibility, speed and agility in young cross-country skiers ? a prospective controlled intervention study. Scand J Med Sci Sports 13:237–243
Beck H, Goussakov IV, Lie A, Helmstaedter C, Elger CE (2000) Synaptic plasticity in the human dentate gyrus. J Neurosci 20:7080–7086
Cirillo J, Lavender AP, Ridding MC, Semmler JG (2009) Motor cortex plasticity induced by paired associative stimulation is enhanced in physically active individuals. J Physiol (Lond) 587:5831–5842
Cooke SF, Bliss TV (2006) Plasticity in the human central nervous system. Brain 129:1659–1673
Coubard OA, Duretz S, Lefebvre V, Lapalus P, Ferrufino L (2011) Practice of contemporary dance improves cognitive flexibility in aging. Front Aging Neurosci 3:13
Di Lazzaro V, Dileone M, Pilato F et al (2009) Associative motor cortex plasticity: direct evidence in humans. Cereb Cortex 19:2326–2330
Erickson KI, Prakash RS, Voss MW, Chaddock L, Hu L, Morris KS, White SM, Wójcicki TR, McAuley E, Kramer AF (2009) Aerobic fitness is associated with hippocampal volume in elderly humans. Hippocampus 19:1030–1039
Erickson KI, Weinstein AM, Sutton BP, Prakash RS, Voss MW, Chaddock L, Mailey EL, Szabo AN, White SM, Wojcicki TR, McAuley E, Kramer AF (2012) Beyond vascularization: aerobic fitness is associated with N-acetylaspartate and working memory. Brain Behav 2:32–41
Floyer-Lea A, Matthews PM (2004) Changing brain networks for visuomotor control with increased movement automaticity. J Neurophysiol 92:2405–2412
Frantseva MV, Fitzgerald PB, Chen R, Moller B, Daigle M, Daskalakis ZJ (2008) Evidence for impaired long-term potentiation in schizophrenia and its relationship to motor skill learning. Cereb Cortex 18:990–996
Hamada M, Strigaro G, Murase N, Sadnicka A, Galea JM, Edwards MJ, Rothwell JC (2012) Cerebellar modulation of human associative plasticity. J Physiol 590:2365–2374
Ishikawa M, Komi PV, Grey MJ, Lepola V, Bruggemann GP (2005) Muscle-tendon interaction and elastic energy usage in human walking. J Appl Physiol 99:603–608
Jung P, Ziemann U (2009) Homeostatic and nonhomeostatic modulation of learning in human motor cortex. J Neurosci 29:5597–5604
Karni A, Meyer G, Jezzard P, Adams MM, Turner R, Ungerleider LG (1995) Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 377:155–158
Katiuscia S, Franco C, Federico D, Davide M, Sergio D, Giuliano G (2009) Reorganization and enhanced functional connectivity of motor areas in repetitive ankle movements after training in locomotor attention. Brain Res 1297:124–134
Kattenstroth JC, Kalisch T, Holt S, Tegenthoff M, Dinse HR (2013) Six months of dance intervention enhances postural, sensorimotor, and cognitive performance in elderly without affecting cardio-respiratory functions. Front Aging Neurosci 5:5
Kempermann G, Fabel K, Ehninger D, Babu H, Leal-Galicia P, Garthe A, Wolf SA (2010) Why and how physical activity promotes experience-induced brain plasticity. Front Neurosci 4:189
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
Kleim JA, Cooper NR, VandenBerg PM (2002) Exercise induces angiogenesis but does not alter movement representations within rat motor cortex. Brain Res 934:1–6
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
Klintsova AY, Dickson E, Yoshida R, Greenough WT (2004) Altered expression of BDNF and its high-affinity receptor TrkB in response to complex motor learning and moderate exercise. Brain Res 1028:92–104
Kramer AF, Erickson KI (2007) Capitalizing on cortical plasticity: influence of physical activity on cognition and brain function. Trends Cogn Sci 11:342–348
Kumpulainen S, Mrachacz-Kersting N, Peltonen J, Voigt M, Avela J (2012) The optimal interstimulus interval and repeatability of paired associative stimulation when the soleus muscle is targeted. Exp Brain Res 221:241–249
Milton J, Solodkin A, Hluštík P, Small SL (2007) The mind of expert motor performance is cool and focused. Neuroimage 35:804–813
Monfils MH, Plautz EJ, Kleim JA (2005) In search of the motor engram: motor map plasticity as a mechanism for encoding motor experience. Neuroscientist 11:471–483
Mrachacz-Kersting N, Fong M, Murphy BA, Sinkjaer T (2007) Changes in excitability of the cortical projections to the human tibialis anterior after paired associative stimulation. J Neurophysiol 97:1951–1958
Nudo RJ, Milliken GW, Jenkins WM, Merzenich MM (1996) Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. J Neurosci 16:785–807
Oya T, Riek S, Cresswell AG (2009) Recruitment and rate coding organisation for soleus motor units across entire range of voluntary isometric plantar flexions. J Physiol 587:4737–4748
Plautz EJ, Milliken GW, Nudo RJ (2000) Effects of repetitive motor training on movement representations in adult squirrel monkeys: role of use versus learning. Neurobiol Learn Mem 74:27–55
Ridding MC, Ziemann U (2010) Determinants of the induction of cortical plasticity by non-invasive brain stimulation in healthy subjects. J Physiol 588:2291–2304
Rosenkranz K, Kacar A, Rothwell JC (2007a) Differential modulation of motor cortical plasticity and excitability in early and late phases of human motor learning. J Neurosci 27:12058–12066
Rosenkranz K, Williamon A, Rothwell JC (2007b) Motorcortical excitability and synaptic plasticity is enhanced in professional musicians. J Neurosci 27:5200–5206
Sanes JN, Donoghue JP (2000) Plasticity and primary motor cortex. Annu Rev Neurosci 23:393–415
Schubert M, Beck S, Taube W, Amtage F, Faist M, Gruber M (2008) Balance training and ballistic strength training are associated with task-specific corticospinal adaptations. Eur J Neurosci 27:2007–2018
Stefan K, Kunesch E, Cohen LG, Benecke R, Classen J (2000) Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 123:572–584
Stefan K, Wycislo M, Classen J (2004) Modulation of associative human motor cortical plasticity by attention. J Neurophysiol 92:66–72
Stefan K, Wycislo M, Gentner R, Schramm A, Naumann M, Reiners K, Classen J (2006) Temporary occlusion of associative motor cortical plasticity by prior dynamic motor training. Cereb Cortex 16:376–385
Thomas AG, Dennis A, Bandettini PA, Johansen-Berg H (2012) The effects of aerobic activity on brain structure. Front Psychol 3:86
Vaalto S, Julkunen P, Saisanen L, Kononen M, Maatta S, Karhu J (2013) Long-term plasticity may be manifested as reduction or expansion of cortical representations of actively used muscles in motor skill specialists. Neuro Report 24:596–600
Vaynman S, Gomez-Pinilla F (2005) License to run: exercise impacts functional plasticity in the intact and injured central nervous system by using neurotrophins. Neurorehabil Neural Repair 19:283–295
Wikgren J, Mertikas GG, Raussi P, Tirkkonen R, Äyräväinen L, Pelto-Huikko M, Koch LG, Britton SL, Kainulainen H (2012) Selective breeding for endurance running capacity affects cognitive but not motor learning in rats. Physiol Behav 106:95–100
Wu T, Kansaku K, Hallett M (2004) How self-initiated memorized movements become automatic: a functional MRI study. J Neurophysiol 91:1690–1698
Zehr PE (2002) Considerations for use of the Hoffmann reflex in exercise studies. Eur J ApplPhysiol 86:455–468
Ziemann U, Ilic TV, Pauli C, Meintzschel F, Ruge D (2004) Learning modifies subsequent induction of long-term potentiation-like and long-term depression-like plasticity in human motor cortex. J Neurosci 24:1666–1672
Ziemann U, Paulus W, Nitsche MA et al (2008) Consensus: motor cortex plasticity protocols. Brain Stimul 1:164–182
Acknowledgments
The authors are very grateful to the subjects who participated in the study and to the laboratory staff from the Neuromuscular Research Center (Department of Biology of Physical Activity) of the University of Jyväskylä, Finland, for their valuable contributions to this project.
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The authors declare no conflict of interest.
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Communicated by Dick F. Stegeman.
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Kumpulainen, S., Avela, J., Gruber, M. et al. Differential modulation of motor cortex plasticity in skill- and endurance-trained athletes. Eur J Appl Physiol 115, 1107–1115 (2015). https://doi.org/10.1007/s00421-014-3092-6
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DOI: https://doi.org/10.1007/s00421-014-3092-6