Abstract
Pairing an acute bout of lower-limb cycling exercise with skilled motor practice enhances acquisition and learning. However, it is not known whether an acute bout of exercise enhances a specific form of motor learning, namely motor adaptation, and if subsequent inter-limb transfer of this adaptation is enhanced. Seventeen young healthy participants performed a bout of cycling exercise and rest, on separate days, prior to right-arm reaching movements to visual targets under 45° rotated feedback of arm position (acquisition), followed by an immediate test of inter-limb transfer with the untrained left arm. After a 24-h delay, participants returned for a no-exercise retention test using the right and left arm with the same rotated visual feedback as acquisition. Results demonstrated that exercise enhanced right-arm adaptation during the acquisition and retention phases, and transiently enhanced aspects of inter-limb transfer, irrespective of usual levels of physical activity. Specifically, exercise enhanced movement accuracy, decreased reaction and movement time during acquisition, and increased accuracy during retention. Exercise shortened reaction time during the inter-limb transfer test immediately after right-arm acquisition but did not influence left-arm performance assessed at retention. These results indicate that an acute bout of exercise before practice enhances right-arm visuomotor adaptation (acquisition) and learning, and decreases reaction time during untrained left arm performance. The current results may have implications for the prescription of exercise protocols to enhance motor adaptation for healthy individuals and in clinical populations.
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References
Ainsworth BE, Haskell WL, Whitt MC et al (2000) Compendium of Physical Activities: an MET intensities. Med Sci Sport Exerc 32:S498–S516
Baayen R, Davidson D, Bates D (2008) Mixed-effects modeling with crossed random effects for subjects and items. J Mem Lang 59:390–412
Bao S, Lei Y, Wang J (2017) Experiencing a reaching task passively with one arm while adapting to a visuomotor rotation with the other can lead to substantial transfer of motor learning across the arms. Neurosci Lett 638:109–113. https://doi.org/10.1016/j.neulet.2016.12.028
Barr D, Levy R, Scheepers C, Tily H (2013) Random effects structure for confirmatory hypothesis testing: Keep it maximal. J Mem Lang 68:1–43. https://doi.org/10.1016/j.jml.2012.11.001
Bates D, Machler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01 doi
Boisgontier MP, Cheval B (2016) The anova to mixed model transition. Neurosci Biobehav Rev 68:1004–1005. https://doi.org/10.1016/j.neubiorev.2016.05.034
Boisgontier MP, Serbruyns L, Swinnen SP (2017) Physical Activity predicts performance in an unpracticed bimanual coordination task. Front Psychol 8:1–5. https://doi.org/10.3389/fpsyg.2017.00249
Booth M (2000) Assessment of physical activity: an international perspective. Res Q Exerc Sport 71:S114–S120
Borg G (1998) Borg’s perceived exertion and pain scales. Human Kinetics, Champaign, IL, USA
Box G, Cox D (1964) An analysis of transformations. J R Stat Soc Ser B Stat Methodol 26:211–252
Byun K, Hyodo K, Suwabe K et al (2014) Positive effect of acute mild exercise on executive function via arousal-related prefrontal activations: an fNIRS study. Neuroimage 98:336–345. https://doi.org/10.1016/j.neuroimage.2014.04.067
Cardoso de Oliveira S (2002) The neuronal basis of bimanual coordination: recent neurophysiological evidence and functional models. Acta Psychol (Amst) 110:139–159
Carroll TJ, Poh E, de Rugy A (2014) New visuomotor maps are immediately available to the opposite limb. J Neurophysiol 111:2232–2243. https://doi.org/10.1152/jn.00042.2014
Core Team R (2017) R: a language and environment for statistical computing. R Found. Stat. Comput. Vienna, Au
Craig C, Marshall A, Sjostrom M et al (2003) International physical activity questionnaire: 12-country reliability and validity. Med Sci Sport Exerc 35:1381–1395
Criscimagna-Hemminger SE, Donchin O, Gazzaniga MS, Shadmehr R (2003) Learned dynamics of reaching movements generalize from dominant to nondominant arm. J Neurophysiol 89:168–176. https://doi.org/10.1152/jn.00622.2002
Deng H, Macfarlane D, Thomas G et al (2008) Reliability and Validity of the IPAQ–Chinese: the Guangzhou Biobank Cohort Study. Med Sci Sport Exerc 40:303–307. https://doi.org/10.1249/mss.0b013e31815b0db5
Dionne JK, Henriques DY (2008) Interpreting ambiguous visual information in motor learning. J Vis 8:2.1–10. https://doi.org/10.1167/8.15.2
Dizio P, Lackner JR (1995) Motor adaptation to Coriolis force perturbations of reaching movements: endpoint but not trajectory adaptation transfers to the nonexposed arm. J Neurophysiol 74:1787–1792. https://doi.org/10.1152/jn.1995.74.4.1787
Doyon J, Benali H (2005) Reorganization and plasticity in the adult brain during learning of motor skills. Curr Opin Neurobiol 15:161–167. https://doi.org/10.1016/j.conb.2005.03.004
Doyon J, Owen AM, Petrides M et al (1996) Functional anatomy of visuomotor skill learning in human subjects examined with positron emission tomography. Eur J Neurosci 8:637–648
Doyon J, Gaudreau D, Laforce R Jr et al (1997) Role of the striatum, cerebellum, and frontal lobes in the learning of a visuomotor sequence. Brain Cogn 34:218–245
Doyon J, Penhune V, Ungerleider LG (2003) Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning. Neuropsychologia 41:252–262
Doyon J, Orban P, Barakat M et al (2011) Functional brain plasticity associated with motor learning. Med Sci (Paris) 27:413–420. https://doi.org/10.1051/medsci/2011274018
Elliott D, Roy EA (1981) Interlimb transfer after adaptation to visual displacement: patterns predicted from the functional closeness of limb neural control centres. Perception 10:383–387
Fernandez-Ruiz J, Wong W, Armstrong IT, Flanagan JR (2011) Relation between reaction time and reach errors during visuomotor adaptation. Behav Brain Res 219:8–14. https://doi.org/10.1016/j.bbr.2010.11.060
Ferrer-Uris B, Busquets A, Lopez-Alonso V et al (2017) Enhancing consolidation of a rotational visuomotor adaptation task through acute exercise. PLoS One 12:3–9. https://doi.org/10.1371/journal.pone.0175296
Galea JM, Vazquez A, Pasricha N et al (2011) Dissociating the roles of the cerebellum and motor cortex during adaptive learning: the motor cortex retains what the cerebellum learns. Cereb Cortex 21:1761–1770. https://doi.org/10.1093/cercor/bhq246
Haith A, Krakauer J (2013) Model-based and model-free mechanisms of human motor learning. Adv Exp Med Biol 782:1–21. https://doi.org/10.1007/978-3-319-47313-0
Haith AM, Huberdeau DM, Krakauer JW (2015) The influence of movement preparation time on the expression of visuomotor learning and savings. J Neurosci 35:5109–5117. https://doi.org/10.1523/JNEUROSCI.3869-14.2015
Huang HJ, Ahmed AA (2014) Reductions in muscle coactivation and metabolic cost during visuomotor adaptation. J Neurophysiol 112:2264–2274. https://doi.org/10.1152/jn.00014.2014
Huberdeau DM, Haith AM, Krakauer JW (2015) Formation of a long-term memory for visuomotor adaptation following only a few trials of practice. J Neurophysiol 114:969–977. https://doi.org/10.1152/jn.00369.2015
Judd C, Westfall J, Kenny D (2012) Treating stimuli as a random factor in social psychology: a new and comprehensive solution to a pervasive but largely ignored problem. J Pers Soc Psychol 103:54–69
Kagerer F, Contreras-Vidal J, Stelmach G (1997) Adaptation to gradual as compared with sudden visuo-motor distortions. Exp Brain Res 115:557–561
Kamijo K, Nishihira Y, Hatta A et al (2004) Differential influences of exercise intensity on information processing in the central nervous system. Eur J Appl Physiol 92:305–311. https://doi.org/10.1007/s00421-004-1097-2
Kamijo K, Nishihira Y, Higashiura T, Kuroiwa K (2007) The interactive effect of exercise intensity and task difficulty on human cognitive processing. Int J Psychophysiol 65:114–121. https://doi.org/10.1016/j.ijpsycho.2007.04.001
Krakauer JW, Ghilardi MF, Ghez C (1999) Independent learning of internal models for kinematic and dynamic control of reaching. Nat Neurosci 2:1026–1031. https://doi.org/10.1038/14826
Krakauer JW, Pine ZM, Ghilardi MF, Ghez C (2000) Learning of visuomotor transformations for vectorial planning of reaching trajectories. J Neurosci 20:8916–8924
Kumar N, Kumar A, Sonane B, Mutha PK (2018) Interference between competing motor memories developed through learning with different limbs. J Neurophysiol 120:1061–1073. https://doi.org/10.1152/jn.00905.2017
Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw 82:1–26. https://doi.org/10.18637/jss.v082.i13
Laszlo J, Baguley R, Bairstow P (1970) Bilateral transfer in tapping skill in the absence of peripheral information. J Mot Behav 2:261–271
Lei Y, Wang J (2014) Prolonged training does not result in a greater extent of interlimb transfer following visuomotor adaptation. Brain Cogn 91:95–99. https://doi.org/10.1016/j.bandc.2014.09.004
Lei Y, Bao S, Perez MA, Wang J (2017) Enhancing generalization of visuomotor adaptation by inducing use-dependent learning. Neuroscience 366:184–195. https://doi.org/10.1016/j.neuroscience.2017.10.004
Lulic T, El-Sayes J, Fassett HJ et al (2017) Physical activity levels determine exercise-induced changes in brain excitability. PLoS One 12:e0173672. https://doi.org/10.1371/journal.pone.0173672
Macintosh BJ, Crane DE, Sage MD et al (2014) Impact of a single bout of aerobic exercise on regional brain perfusion and activation responses in healthy young adults. PLoS One 8:e85163. https://doi.org/10.1371/journal.pone.0085163
Mäder U, Martin BW, Schutz Y, Marti B (2006) Validity of four short physical activity questionnaires in middle-aged persons. Med Sci Sport Exerc 38:1255–1266. https://doi.org/10.1249/01.mss.0000227310.18902.28
Malfait N, Ostry DJ (2004) Is interlimb transfer of force-field adaptation a cognitive response to the sudden introduction of load? J Neurosci 24:8084–8089. https://doi.org/10.1523/JNEUROSCI.1742-04.2004
Mang C, Snow N, Campbell K et al (2014) A single bout of aerobic exercise facilitates response to paired associative stimulation and promotes sequence-specific implicit motor learning. J Appl Physiol 117:1325–1336. https://doi.org/10.1152/japplphysiol.00498.2014
Mang CS, Brown KE, Neva JL et al (2016a) Promoting motor cortical plasticity with acute aerobic exercise: a role for cerebellar circuits. Neural Plast. https://doi.org/10.1155/2016/6797928
Mang CS, Snow NJ, Wadden KP et al (2016b) High-intensity aerobic exercise enhances motor memory retrieval. Med Sci Sport Exerc. https://doi.org/10.1249/MSS.0000000000001040
Masley S, Roetzheim R, Gualtieri T (2009) Aerobic exercise enhances cognitive flexibility. J Clin Psychol Med Settings 16:186–193. https://doi.org/10.1007/s10880-009-9159-6
Mattar AG, Gribble PL (2005) Motor learning by observing. Neuron 46:153–160. https://doi.org/10.1016/j.neuron.2005.02.009
Mazzoni P, Krakauer JW (2006) An implicit plan overrides an explicit strategy during visuomotor adaptation. J Neurosci 26:3642–3645. https://doi.org/10.1523/JNEUROSCI.5317-05.2006
Mooney RA, Coxon JP, Cirillo J et al (2016) Acute aerobic exercise modulates primary motor cortex inhibition. Exp Brain Res 234:1–8. https://doi.org/10.1007/s00221-016-4767-5
Morton SM, Lang CE, Bastian AJ (2001) Inter- and intra-limb generalization of adaptation during catching. Exp Brain Res 141:438–445. https://doi.org/10.1007/s002210100889
Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142. https://doi.org/10.1111/j.2041-210x.2012.00261.x
Neva JL, Henriques D (2013) Visuomotor adaptation and generalization with repeated and varied training. Exp Brain Res 226:363–372. https://doi.org/10.1007/s00221-013-3444-1
Neva JL, Brown KE, Mang CS et al (2017) An acute bout of exercise modulates both intracortical and interhemispheric excitability. Eur J Neurosci. https://doi.org/10.1111/ejn.13569
Oldfield R (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia Mar 9:97–113
Osborne J (2010) Improving your data transformation: applying the Box-Cox transformation. Pr Assess Res Eval 15:1–9
Ostadan F, Centeno C, Daloze J et al (2016) Changes in corticospinal excitability during consolidation predict acute exercise-induced off-line gains in procedural memory. Neurobiol Learn Mem 136:196–203. https://doi.org/10.1016/j.nlm.2016.10.009
Papathanasiou G, Georgoudis G, Georgakopoulos D et al (2010) Criterion-related validity of the short International Physical Activity Questionnaire against exercise capacity in young adults. Eur J Cardiovasc Prev Rehabil 17:380–386
Poh E, Carroll TJ, Taylor JA (2016) Effect of coordinate frame compatibility on the transfer of implicit and explicit learning across limbs. J Neurophysiol 116:1239–1249. https://doi.org/10.1152/jn.00410.2016
Poh E, Carroll TJ, de Rugy A (2017) Distinct coordinate systems for adaptations of movement direction and extent. J Neurophysiol 118:2670–2686. https://doi.org/10.1152/jn.00326.2016
Rajab AS, Crane DE, Middleton LE et al (2014) A single session of exercise increases connectivity in sensorimotor-related brain networks: a resting-state fMRI study in young healthy adults. Front Hum Neurosci 8:625. https://doi.org/10.3389/fnhum.2014.00625
Roig M, Skriver K, Lundbye-Jensen J et al (2012) A single bout of exercise improves motor memory. PLoS One 7:e44594. https://doi.org/10.1371/journal.pone.0044594
Saijo N, Gomi H (2010) Multiple motor learning strategies in visuomotor rotation. PLoS One. https://doi.org/10.1371/journal.pone.0009399
Sainburg RL, Wang J (2002) Interlimb transfer of visuomotor rotations: Independence of direction and final position information. Exp Brain Res 145:437–447. https://doi.org/10.1007/s00221-002-1140-7
Scheeres K, Knoop H, Meer VDJ, Bleijenberg G (2009) Clinical assessment of the physical activity pattern of chronic fatigue syndrome patients: a validation of three methods. Heal Qual Life Outcomes 7:1–7. https://doi.org/10.1186/1477-7525-7-29
Schmidt RA, Zelaznik H, Hawkins B et al (1979) Motor-output variability: a theory for the accuracy of rapid motor acts. Psychol Rev 47:415–451
Shabbott BA, Sainburg RL (2009) On-line corrections for visuomotor errors. Exp Brain Res 195:59–72. https://doi.org/10.1007/s00221-009-1749-x
Shadmehr R (2004) Generalization as a behavioral window to the neural mechanisms of learning internal models. Hum Mov Sci 23:543–568. https://doi.org/10.1016/j.humov.2004.04.003
Shadmehr R, Brashers-Krug T (1997) Functional stages in the formation of human long-term motor memory. J Neurosci 17:409–419
Shadmehr R, Mussa-Ivaldi FA (1994) Adaptive representation of dynamics during learning of a motor task. J Neurosci 14:3208–3224
Singh AM, Duncan RE, Neva JL, Staines WR (2014a) Aerobic exercise modulates intracortical inhibition and facilitation in a nonexercised upper limb muscle. BMC Sports Sci Med Rehabil 6:23. https://doi.org/10.1186/2052-1847-6-23
Singh AM, Neva JL, Staines WR (2014b) Acute exercise enhances the response to paired associative stimulation-induced plasticity in the primary motor cortex. Exp Brain Res 232:3675–3685. https://doi.org/10.1007/s00221-014-4049-z
Singh AM, Neva JL, Staines WR (2015) Aerobic exercise enhances neural correlates of motor skill learning. Behav Brain Res 301:19–26. https://doi.org/10.1016/j.bbr.2015.12.020
Skriver K, Roig M, Lundbye-Jensen J et al (2014) Acute exercise improves motor memory: exploring potential biomarkers. Neurobiol Learn Mem 116:46–58. https://doi.org/10.1016/j.nlm.2014.08.004
Smith AE, Goldsworthy MR, Garside T et al (2014) The influence of a single bout of aerobic exercise on short-interval intracortical excitability. Exp brain Res 232:1875–1882. https://doi.org/10.1007/s00221-014-3879-z
Spampinato D, Celnik P (2018) Deconstructing skill learning and its physiological mechanisms. Cortex 104:90–102
Spampinato DA, Block HJ, Celnik PA (2017) Cerebellar–M1 connectivity changes associated with motor learning are somatotopic specific. J Neurosci 37:2377–2386. https://doi.org/10.1523/JNEUROSCI.2511-16.2017
Statton MA, Encarnacion M, Celnik P, Bastian AJ (2015) A single bout of moderate aerobic exercise improves motor skill acquisition. PLoS One 10:1–13. https://doi.org/10.1371/journal.pone.0141393
Stavrinos E, Coxon J (2017) High-intensity interval exercise promotes motor cortex disinhibition and early motor skill consolidation. J Cogn Neurosci 29:593–604. https://doi.org/10.1162/jocn
Swinnen SP (2002) Intermanual coordination: from behavioural principles to neural-network interactions. Nat Rev Neurosci 3:348–359. https://doi.org/10.1038/nrn807
Taylor JA, Krakauer JW, Ivry RB (2014) Explicit and implicit contributions to learning in a sensorimotor adaptation task. J Neurosci 34:3023–3032. https://doi.org/10.1523/JNEUROSCI.3619-13.2014
Thomas R, Beck MM, Lind RR et al (2016) Acute exercise and motor memory consolidation: the role of exercise timing. Neural Plast 2016:1–11. https://doi.org/10.1155/2016/6205452
Thoroughman KA, Shadmehr R (1999) Electromyographic correlates of learning an internal model of reaching movements. J Neurosci 19:8573–8588
Tong C, Flanagan JR (2003) Task-specific internal models for kinematic transformations. J Neurophysiol 90:578–585. https://doi.org/10.1152/jn.01087.2002
Ungerleider LG, Doyon J, Karni A (2002) Imaging brain plasticity during motor skill learning. Neurobiol Learn Mem 78:553–564. https://doi.org/10.1006/nlme.2002.4091
Wang J, Lei Y (2015) Direct-effects and after-effects of visuomotor adaptation with one arm on subsequent performance with the other arm. J Neurophysiol 114:468–473. https://doi.org/10.1152/jn.00298.2015
Wang J, Sainburg RL (2003) Mechanisms underlying interlimb transfer of visuomotor rotations. Exp Brain Res 149:520–526. https://doi.org/10.1007/s00221-006-0543-2
Wang J, Sainburg RL (2004) Limitations in interlimb transfer of visuomotor rotations. Exp Brain Res 155:1–8. https://doi.org/10.1007/s00221-003-1691-2
Wang J, Sainburg RL (2005) Adaptation to visuomotor rotations remaps movement vectors, not final positions. J Neurosci 25:4024–4030. https://doi.org/10.1523/JNEUROSCI.5000-04.2005
Wang J, Lei Y, Binder J (2015) Performing a reaching task with one arm while adapting to a visuomotor rotation with the other can lead to complete transfer of motor learning across the arms. J Neurophysiol 113:109–113. https://doi.org/10.1016/j.neulet.2016.12.028
Wolpert DM, Miall RC, Kawato M (1998) Internal models in the cerebellum. Trends Cogn Sci 2:338–347. https://doi.org/10.1016/S1364-6613(98)01221-2
Yanagisawa H, Dan I, Tsuzuki D et al (2010) Acute moderate exercise elicits increased dorsolateral prefrontal activation and improves cognitive performance with Stroop test. Neuroimage 50:1702–1710. https://doi.org/10.1016/j.neuroimage.2009.12.023
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The authors would like to thank Natalie Wong for participant recruitment and data collection assistance.
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This work was funded by the Natural Sciences and Engineering Research Council of Canada (NSERC; RGPIN 401890-11 to LAB). JLN receives funding support from the Michael Smith Foundation for Health Research (MSFHR) and the Canadian Institutes of Health Research (CIHR). MPB is supported by a postdoctoral fellowship, a grant for a long-term research abroad, and research grants from the Research Foundation-Flanders (FWO; 1501018N).
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JLN conceived the study, primarily collected, processed and interpreted the data, wrote and edited the manuscript and contributed to data analysis. JAM contributed to data collection, processing, and edited the manuscript. DO contributed to data analysis and edited the manuscript. MPB primarily analyzed the data, contributed to interpretation of the results, and to writing and editing the manuscript. LAB contributed to the interpretation of data, and to writing and editing the manuscript.
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Neva, J.L., Ma, J.A., Orsholits, D. et al. The effects of acute exercise on visuomotor adaptation, learning, and inter-limb transfer. Exp Brain Res 237, 1109–1127 (2019). https://doi.org/10.1007/s00221-019-05491-5
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DOI: https://doi.org/10.1007/s00221-019-05491-5