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The effects of acute exercise on visuomotor adaptation, learning, and inter-limb transfer

  • Jason L. NevaEmail author
  • Jennifer A. Ma
  • Dan Orsholits
  • Matthieu P. Boisgontier
  • Lara A. Boyd
Research Article

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.

Keywords

Exercise Visuomotor adaptation Inter-limb transfer Motor adaptation Retention 

Notes

Acknowledgements

The authors would like to thank Natalie Wong for participant recruitment and data collection assistance.

Author contributions

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.

Funding

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).

References

  1. Ainsworth BE, Haskell WL, Whitt MC et al (2000) Compendium of Physical Activities: an MET intensities. Med Sci Sport Exerc 32:S498–S516CrossRefGoogle Scholar
  2. Baayen R, Davidson D, Bates D (2008) Mixed-effects modeling with crossed random effects for subjects and items. J Mem Lang 59:390–412CrossRefGoogle Scholar
  3. 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 CrossRefGoogle Scholar
  4. 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 CrossRefGoogle Scholar
  5. 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 doiCrossRefGoogle Scholar
  6. 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 CrossRefGoogle Scholar
  7. 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 CrossRefGoogle Scholar
  8. Booth M (2000) Assessment of physical activity: an international perspective. Res Q Exerc Sport 71:S114–S120CrossRefGoogle Scholar
  9. Borg G (1998) Borg’s perceived exertion and pain scales. Human Kinetics, Champaign, IL, USAGoogle Scholar
  10. Box G, Cox D (1964) An analysis of transformations. J R Stat Soc Ser B Stat Methodol 26:211–252Google Scholar
  11. 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 CrossRefGoogle Scholar
  12. Cardoso de Oliveira S (2002) The neuronal basis of bimanual coordination: recent neurophysiological evidence and functional models. Acta Psychol (Amst) 110:139–159CrossRefGoogle Scholar
  13. 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 CrossRefGoogle Scholar
  14. Core Team R (2017) R: a language and environment for statistical computing. R Found. Stat. Comput. Vienna, AuGoogle Scholar
  15. Craig C, Marshall A, Sjostrom M et al (2003) International physical activity questionnaire: 12-country reliability and validity. Med Sci Sport Exerc 35:1381–1395CrossRefGoogle Scholar
  16. 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 CrossRefGoogle Scholar
  17. 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 CrossRefGoogle Scholar
  18. 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 CrossRefGoogle Scholar
  19. 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 CrossRefGoogle Scholar
  20. 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 CrossRefGoogle Scholar
  21. 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 8:637–648CrossRefGoogle Scholar
  22. 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 34:218–245CrossRefGoogle Scholar
  23. Doyon J, Penhune V, Ungerleider LG (2003) Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning. Neuropsychologia 41:252–262CrossRefGoogle Scholar
  24. 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 CrossRefGoogle Scholar
  25. Elliott D, Roy EA (1981) Interlimb transfer after adaptation to visual displacement: patterns predicted from the functional closeness of limb neural control centres. Perception 10:383–387CrossRefGoogle Scholar
  26. 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 CrossRefGoogle Scholar
  27. 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 CrossRefGoogle Scholar
  28. 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 CrossRefGoogle Scholar
  29. 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 CrossRefGoogle Scholar
  30. 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 CrossRefGoogle Scholar
  31. 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 CrossRefGoogle Scholar
  32. 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 CrossRefGoogle Scholar
  33. 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 103:54–69CrossRefGoogle Scholar
  34. Kagerer F, Contreras-Vidal J, Stelmach G (1997) Adaptation to gradual as compared with sudden visuo-motor distortions. Exp Brain Res 115:557–561CrossRefGoogle Scholar
  35. 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 CrossRefGoogle Scholar
  36. 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 CrossRefGoogle Scholar
  37. 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 CrossRefGoogle Scholar
  38. Krakauer JW, Pine ZM, Ghilardi MF, Ghez C (2000) Learning of visuomotor transformations for vectorial planning of reaching trajectories. J Neurosci 20:8916–8924CrossRefGoogle Scholar
  39. 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 CrossRefGoogle Scholar
  40. 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 CrossRefGoogle Scholar
  41. Laszlo J, Baguley R, Bairstow P (1970) Bilateral transfer in tapping skill in the absence of peripheral information. J Mot Behav 2:261–271CrossRefGoogle Scholar
  42. 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 CrossRefGoogle Scholar
  43. 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 CrossRefGoogle Scholar
  44. 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 CrossRefGoogle Scholar
  45. 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 CrossRefGoogle Scholar
  46. 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 CrossRefGoogle Scholar
  47. 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 CrossRefGoogle Scholar
  48. 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 CrossRefGoogle Scholar
  49. 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 Google Scholar
  50. 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 Google Scholar
  51. 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 CrossRefGoogle Scholar
  52. Mattar AG, Gribble PL (2005) Motor learning by observing. Neuron 46:153–160.  https://doi.org/10.1016/j.neuron.2005.02.009 CrossRefGoogle Scholar
  53. 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 CrossRefGoogle Scholar
  54. 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 CrossRefGoogle Scholar
  55. 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 CrossRefGoogle Scholar
  56. 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 CrossRefGoogle Scholar
  57. 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 CrossRefGoogle Scholar
  58. 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 Google Scholar
  59. Oldfield R (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia Mar 9:97–113CrossRefGoogle Scholar
  60. Osborne J (2010) Improving your data transformation: applying the Box-Cox transformation. Pr Assess Res Eval 15:1–9Google Scholar
  61. 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 CrossRefGoogle Scholar
  62. 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 17:380–386CrossRefGoogle Scholar
  63. 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 CrossRefGoogle Scholar
  64. 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 CrossRefGoogle Scholar
  65. 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 CrossRefGoogle Scholar
  66. 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 CrossRefGoogle Scholar
  67. Saijo N, Gomi H (2010) Multiple motor learning strategies in visuomotor rotation. PLoS One.  https://doi.org/10.1371/journal.pone.0009399 Google Scholar
  68. 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 CrossRefGoogle Scholar
  69. 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 CrossRefGoogle Scholar
  70. Schmidt RA, Zelaznik H, Hawkins B et al (1979) Motor-output variability: a theory for the accuracy of rapid motor acts. Psychol Rev 47:415–451CrossRefGoogle Scholar
  71. 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 CrossRefGoogle Scholar
  72. 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 CrossRefGoogle Scholar
  73. Shadmehr R, Brashers-Krug T (1997) Functional stages in the formation of human long-term motor memory. J Neurosci 17:409–419CrossRefGoogle Scholar
  74. Shadmehr R, Mussa-Ivaldi FA (1994) Adaptive representation of dynamics during learning of a motor task. J Neurosci 14:3208–3224CrossRefGoogle Scholar
  75. 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 CrossRefGoogle Scholar
  76. 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 CrossRefGoogle Scholar
  77. 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 CrossRefGoogle Scholar
  78. 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 CrossRefGoogle Scholar
  79. 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 CrossRefGoogle Scholar
  80. Spampinato D, Celnik P (2018) Deconstructing skill learning and its physiological mechanisms. Cortex 104:90–102CrossRefGoogle Scholar
  81. 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 CrossRefGoogle Scholar
  82. 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 Google Scholar
  83. 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 CrossRefGoogle Scholar
  84. Swinnen SP (2002) Intermanual coordination: from behavioural principles to neural-network interactions. Nat Rev Neurosci 3:348–359.  https://doi.org/10.1038/nrn807 CrossRefGoogle Scholar
  85. 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 CrossRefGoogle Scholar
  86. 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 CrossRefGoogle Scholar
  87. Thoroughman KA, Shadmehr R (1999) Electromyographic correlates of learning an internal model of reaching movements. J Neurosci 19:8573–8588CrossRefGoogle Scholar
  88. 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 CrossRefGoogle Scholar
  89. 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 CrossRefGoogle Scholar
  90. 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 CrossRefGoogle Scholar
  91. 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 CrossRefGoogle Scholar
  92. 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 CrossRefGoogle Scholar
  93. 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 CrossRefGoogle Scholar
  94. 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 Google Scholar
  95. 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 CrossRefGoogle Scholar
  96. 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 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Jason L. Neva
    • 1
    Email author
  • Jennifer A. Ma
    • 1
  • Dan Orsholits
    • 2
  • Matthieu P. Boisgontier
    • 1
    • 3
  • Lara A. Boyd
    • 1
  1. 1.Department of Physical Therapy, Brain Behavior Laboratory, Faculty of MedicineUniversity of British ColumbiaVancouverCanada
  2. 2.University of Geneva, Swiss NCCR ‘LIVES—Overcoming Vulnerability: Life Course Perspectives’GenevaSwitzerland
  3. 3.Department of Movement SciencesKU LeuvenLeuvenBelgium

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