Table of Contents Author Guidelines Submit a Manuscript
Neural Plasticity
Volume 2016 (2016), Article ID 6205452, 11 pages
http://dx.doi.org/10.1155/2016/6205452
Research Article

Acute Exercise and Motor Memory Consolidation: The Role of Exercise Timing

1Department of Nutrition, Exercise and Sports, University of Copenhagen, 2200 Copenhagen, Denmark
2Department of Neuroscience & Pharmacology, University of Copenhagen, 2200 Copenhagen, Denmark
3Department of Neurological Surgery, The Miami Project to Cure Paralysis, University of Miami, Miami, FL 33136, USA
4Memory and Motor Rehabilitation Laboratory (MEMORY-LAB), Jewish Rehabilitation Hospital, Montreal Center for Interdisciplinary Research in Rehabilitation (CRIR), Montréal, QC, Canada H7V 1R2
5School of Physical & Occupational Therapy, Faculty of Medicine, McGill University, Montreal, QC, Canada H3G 1Y5

Received 28 January 2016; Accepted 14 April 2016

Academic Editor: Terry McMorris

Copyright © 2016 Richard Thomas et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. E. M. Robertson, “Skill learning: putting procedural consolidation in context,” Current Biology, vol. 14, no. 24, pp. R1061–R1063, 2004. View at Publisher · View at Google Scholar · View at Scopus
  2. M.-H. Monfils, E. J. Plautz, and J. A. Kleim, “In search of the motor engram: motor map plasticity as a mechanism for encoding motor experience,” Neuroscientist, vol. 11, no. 5, pp. 471–483, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. Y. Dudai, “The restless engram: consolidations never end,” Annual Review of Neuroscience, vol. 35, pp. 227–247, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. Y. Dudai, “The neurobiology of consolidations, or, how stable is the engram?” Annual Review of Psychology, vol. 55, pp. 51–86, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. S. E. Criscimagna-Hemminger and R. Shadmehr, “Consolidation patterns of human motor memory,” Journal of Neuroscience, vol. 28, no. 39, pp. 9610–9618, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. J. W. Krakauer and R. Shadmehr, “Consolidation of motor memory,” Trends in Neurosciences, vol. 29, no. 1, pp. 58–64, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. R. Shadmehr and T. Brashers-Krug, “Functional stages in the formation of human long-term motor memory,” The Journal of Neuroscience, vol. 17, no. 1, pp. 409–419, 1997. View at Google Scholar · View at Scopus
  8. M. P. Walker, R. Stickgold, D. Alsop, N. Gaab, and G. Schlaug, “Sleep-dependent motor memory plasticity in the human brain,” Neuroscience, vol. 133, no. 4, pp. 911–917, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. M. P. Walker, T. Brakefield, J. Seidman, A. Morgan, J. A. Hobson, and R. Stickgold, “Sleep and the time course of motor skill learning,” Learning and Memory, vol. 10, no. 4, pp. 275–284, 2003. View at Publisher · View at Google Scholar · View at Scopus
  10. J. L. Jensen, P. C. D. Marstrand, and J. B. Nielsen, “Motor skill training and strength training are associated with different plastic changes in the central nervous system,” Journal of Applied Physiology, vol. 99, no. 4, pp. 1558–1568, 2005. View at Publisher · View at Google Scholar · View at Scopus
  11. W. Muellbacher, U. Zlemann, J. Wissel et al., “Early consolidation in human primary motor cortex,” Nature, vol. 415, no. 6872, pp. 640–644, 2002. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Roig, R. Thomas, C. S. Mang et al., “Time-dependent effects of cardiovascular exercise on memory,” Exercise & Sport Sciences Reviews, vol. 44, no. 2, pp. 81–88, 2016. View at Publisher · View at Google Scholar · View at Scopus
  13. K. Skriver, M. Roig, J. Lundbye-Jensen et al., “Acute exercise improves motor memory: exploring potential biomarkers,” Neurobiology of Learning and Memory, vol. 116, pp. 46–58, 2014. View at Publisher · View at Google Scholar · View at Scopus
  14. E. M. Robertson, A. Pascual-Leone, and D. Z. Press, “Awareness modifies the skill-learning benefits of sleep,” Current Biology, vol. 14, no. 3, pp. 208–212, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. M. A. Statton, M. Encarnacion, P. Celnik, and A. J. Bastian, “A single bout of moderate aerobic exercise improves motor skill acquisition,” PLoS ONE, vol. 10, no. 10, article e0141393, 2015. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Roig, S. Nordbrandt, S. S. Geertsen, and J. B. Nielsen, “The effects of cardiovascular exercise on human memory: a review with meta-analysis,” Neuroscience & Biobehavioral Reviews, vol. 37, no. 8, pp. 1645–1666, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Roig, K. Skriver, J. Lundbye-Jensen, B. Kiens, and J. B. Nielsen, “A single bout of exercise improves motor memory,” PLoS ONE, vol. 7, no. 9, article e44594, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. R. Thomas, L. Korsgaard Johnsen, S. S. Geertsen, L. Christiansen, M. Roig, and J. Lundbye-Jensen, “Acute exercise and motor memory consolidation: the role of exercise intensity and timing,” in Proceedings of the 45th Annual Meeting Society for Neuroscience, Chicago, Ill, USA, 2015.
  19. C. S. Mang, N. J. Snow, K. L. Campbell, C. J. D. Ross, and L. A. Boyd, “A single bout of high-intensity aerobic exercise facilitates response to paired associative stimulation and promotes sequence-specific implicit motor learning,” Journal of Applied Physiology, vol. 117, no. 11, pp. 1325–1336, 2014. View at Publisher · View at Google Scholar · View at Scopus
  20. A. M. Singh, R. E. Duncan, J. L. Neva, and W. R. Staines, “Aerobic exercise modulates intracortical inhibition and facilitation in a nonexercised upper limb muscle,” BMC Sports Science, Medicine and Rehabilitation, vol. 6, no. 1, article 23, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. A. E. Smith, M. R. Goldsworthy, T. Garside, F. M. Wood, and M. C. Ridding, “The influence of a single bout of aerobic exercise on short-interval intracortical excitability,” Experimental Brain Research, vol. 232, no. 6, pp. 1875–1882, 2014. View at Publisher · View at Google Scholar · View at Scopus
  22. S. Tunovic, D. Z. Press, and E. M. Robertson, “A physiological signal that prevents motor skill improvements during consolidation,” The Journal of Neuroscience, vol. 34, no. 15, pp. 5302–5310, 2014. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Taubert, A. Villringer, and N. Lehmann, “Endurance exercise as an ‘endogenous’ neuro-enhancement strategy to facilitate motor learning,” Frontiers in Human Neuroscience, vol. 9, article 692, 2015. View at Publisher · View at Google Scholar · View at Scopus
  24. N. J. Snow, C. S. Mang, M. Roig et al., “The effect of an acute bout of moderate-intensity aerobic exercise on motor learning of a continuous tracking task,” PLoS ONE, vol. 11, no. 2, article e0150039, 2016. View at Publisher · View at Google Scholar
  25. J. Lundbye-Jensen, T. H. Petersen, J. C. Rothwell, and J. B. Nielsen, “Interference in ballistic motor learning: specificity and role of sensory error signals,” PLoS ONE, vol. 6, no. 3, Article ID e17451, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. G. Cantarero, B. Tang, R. O'Malley, R. Salas, and P. Celnik, “Motor learning interference is proportional to occlusion of LTP-like plasticity,” The Journal of Neuroscience, vol. 33, no. 11, pp. 4634–4641, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. R. Fonseca, U. V. Nägerl, R. G. M. Morris, and T. Bonhoeffer, “Competing for memory: hippocampal LTP under regimes of reduced protein synthesis,” Neuron, vol. 44, no. 6, pp. 1011–1020, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. R. L. Redondo and R. G. M. Morris, “Making memories last: the synaptic tagging and capture hypothesis,” Nature Reviews Neuroscience, vol. 12, no. 1, pp. 17–30, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. U. Frey and R. G. M. Morris, “Weak before strong: dissociating synaptic tagging and plasticity-factor accounts of late-LTP,” Neuropharmacology, vol. 37, no. 4-5, pp. 545–552, 1998. View at Publisher · View at Google Scholar · View at Scopus
  30. J. Siette, A. C. Reichelt, and R. F. Westbrook, “A bout of voluntary running enhances context conditioned fear, its extinction, and its reconsolidation,” Learning & Memory, vol. 21, no. 2, pp. 73–81, 2014. View at Publisher · View at Google Scholar · View at Scopus
  31. T. Xu, X. Yu, A. J. Perlik et al., “Rapid formation and selective stabilization of synapses for enduring motor memories,” Nature, vol. 462, no. 7275, pp. 915–919, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. A. R. Luft and M. M. Buitrago, “Stages of motor skill learning,” Molecular Neurobiology, vol. 32, no. 3, pp. 205–216, 2005. View at Publisher · View at Google Scholar · View at Scopus
  33. D. Borota, E. Murray, G. Keceli et al., “Post-study caffeine administration enhances memory consolidation in humans,” Nature Neuroscience, vol. 17, no. 2, pp. 201–203, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. R. C. Oldfield, “The assessment and analysis of handedness: the Edinburgh inventory,” Neuropsychologia, vol. 9, no. 1, pp. 97–113, 1971. View at Publisher · View at Google Scholar · View at Scopus
  35. R. J. Vallerand, L. G. Pelletier, M. R. Blais, N. M. Briere, C. Senecal, and E. F. Vallieres, “The academic motivation scale: a measure of intrinsic, extrinsic, and amotivation in education,” Educational and Psychological Measurement, vol. 52, no. 4, pp. 1003–1017, 1992. View at Publisher · View at Google Scholar
  36. J. Duda, L. Chi, and M. Newton, “Psychometric characteristics of the TEOSQ,” in Proceedings of the Annual Meeting of the North American Society for the Psychology of Sport and Physical Activity, University of Houston, 1990.
  37. M. Hagströmer, P. Oja, and M. Sjöström, “The International Physical Activity Questionnaire (IPAQ): a study of concurrent and construct validity,” Public Health Nutrition, vol. 9, no. 6, pp. 755–762, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Engeser and F. Rheinberg, “Flow, performance and moderators of challenge-skill balance,” Motivation and Emotion, vol. 32, no. 3, pp. 158–172, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. A.-M. Elbe, K. Strahler, P. Krustrup, J. Wikman, and R. Stelter, “Experiencing flow in different types of physical activity intervention programs: three randomized studies,” Scandinavian Journal of Medicine & Science in Sports, vol. 20, no. 1, pp. 111–117, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. D. Watson and L. A. Clark, The PANAS-X: Manual for the Positive and Negative Affect Schedule Expanded Form, 1999.
  41. E. Hoddes, V. Zarcone, H. Smythe, R. Phillips, and W. C. Dement, “Quantification of sleepiness: a new approach,” Psychophysiology, vol. 10, no. 4, pp. 431–436, 1973. View at Publisher · View at Google Scholar · View at Scopus
  42. G. B. Moneta and M. Csikszentmihalyi, “The effect of perceived challenges and skills on the quality of subjective experience,” Journal of Personality, vol. 64, no. 2, pp. 275–310, 1996. View at Publisher · View at Google Scholar · View at Scopus
  43. F. Rheinberg and R. Vollmeyer, “Flow-Erleben in einem Computerspiel unter experimentell variierten Bedingungen,” Zeitschrift für Psychologie, vol. 211, no. 4, pp. 161–170, 2003. View at Publisher · View at Google Scholar
  44. R. M. Ryan, “Control and information in the intrapersonal sphere: an extension of cognitive evaluation theory,” Journal of Personality and Social Psychology, vol. 43, no. 3, pp. 450–461, 1982. View at Publisher · View at Google Scholar · View at Scopus
  45. T. H. Monk, C. F. Reynolds, D. J. Kupfer et al., “The Pittsburgh sleep diary,” Journal of Sleep Research, vol. 3, no. 2, pp. 111–120, 1994. View at Publisher · View at Google Scholar · View at Scopus
  46. J. Doyon, M. Korman, A. Morin et al., “Contribution of night and day sleep vs. simple passage of time to the consolidation of motor sequence and visuomotor adaptation learning,” Experimental Brain Research, vol. 195, no. 1, pp. 15–26, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. J. K. Wilson, B. Baran, E. F. Pace-Schott, R. B. Ivry, and R. M. C. Spencer, “Sleep modulates word-pair learning but not motor sequence learning in healthy older adults,” Neurobiology of Aging, vol. 33, no. 5, pp. 991–1000, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. P. Maquet, S. Schwartz, R. Passingham, and C. Frith, “Sleep-related consolidation of a visuomotor skill: brain mechanisms as assessed by functional magnetic resonance imaging,” The Journal of Neuroscience, vol. 23, no. 4, pp. 1432–1440, 2003. View at Google Scholar · View at Scopus
  49. A. W. Salmoni, R. A. Schmidt, and C. B. Walter, “Knowledge of results and motor learning: a review and critical reappraisal,” Psychological Bulletin, vol. 95, no. 3, pp. 355–386, 1984. View at Publisher · View at Google Scholar · View at Scopus
  50. B. Winter, C. Breitenstein, F. C. Mooren et al., “High impact running improves learning,” Neurobiology of Learning and Memory, vol. 87, no. 4, pp. 597–609, 2007. View at Publisher · View at Google Scholar · View at Scopus
  51. F. Grego, J.-M. Vallier, M. Collardeau, C. Rousseu, J. Cremieux, and J. Brisswalter, “Influence of exercise duration and hydration status on cognitive function during prolonged cycling exercise,” International Journal of Sports Medicine, vol. 26, no. 1, pp. 27–33, 2005. View at Publisher · View at Google Scholar · View at Scopus
  52. C. Cian, N. Koulmann, P. A. Barraud, C. Raphel, C. Jimenez, and B. Melin, “Influence of variations in body hydration on cognitive function: effect of hyperhydration, heat stress, and exercise-induced dehydration,” Journal of Psychophysiology, vol. 14, no. 1, pp. 29–36, 2000. View at Publisher · View at Google Scholar · View at Scopus
  53. G. A. V. Borg, “Psychophysical bases of perceived exertion,” Medicine & Science in Sports & Exercise, vol. 14, no. 5, pp. 377–381, 1982. View at Google Scholar · View at Scopus
  54. T. Hothorn, F. Bretz, and P. Westfall, “Simultaneous inference in general parametric models,” Biometrical Journal, vol. 50, no. 3, pp. 346–363, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. D. Bates, M. Mächler, B. M. Bolker, and S. C. Walker, “Fitting linear mixed-effects models using lme4,” Journal of Statistical Software, vol. 67, no. 1, 2015. View at Publisher · View at Google Scholar · View at Scopus
  56. M. P. Walker and R. Stickgold, “It's practice, with sleep, that makes perfect: implications of sleep-dependent learning and plasticity for skill performance,” Clinics in Sports Medicine, vol. 24, no. 2, pp. 301–317, 2005. View at Publisher · View at Google Scholar · View at Scopus
  57. T. Brashers-Krug, R. Shadmehr, and E. Bizzi, “Consolidation in human motor memory,” Nature, vol. 382, no. 6588, pp. 252–255, 1996. View at Publisher · View at Google Scholar · View at Scopus
  58. J. W. Krakauer, C. Ghez, and M. F. Ghilardi, “Adaptation to visuomotor transformations: consolidation, interference, and forgetting,” The Journal of Neuroscience, vol. 25, no. 2, pp. 473–478, 2005. View at Publisher · View at Google Scholar · View at Scopus
  59. E. M. Robertson, D. Z. Press, and A. Pascual-Leone, “Off-line learning and the primary motor cortex,” The Journal of Neuroscience, vol. 25, no. 27, pp. 6372–6378, 2005. View at Publisher · View at Google Scholar · View at Scopus
  60. N. Censor, M. A. Dimyan, and L. G. Cohen, “Modification of existing human motor memories is enabled by primary cortical processing during memory reactivation,” Current Biology, vol. 20, no. 17, pp. 1545–1549, 2010. View at Publisher · View at Google Scholar · View at Scopus
  61. J. Rhee, J. Chen, S. M. Riechman, A. Handa, S. Bhatia, and D. L. Wright, “An acute bout of aerobic exercise can protect immediate offline motor sequence gains,” Psychological Research, vol. 80, no. 4, pp. 518–531, 2016. View at Publisher · View at Google Scholar · View at Scopus
  62. M. A. Perez, J. Lundbye-Jensen, and J. B. Nielsen, “Changes in corticospinal drive to spinal motoneurones following visuo-motor skill learning in humans,” The Journal of Physiology, vol. 573, no. 3, pp. 843–855, 2006. View at Publisher · View at Google Scholar · View at Scopus
  63. M. Lotze, C. Braun, N. Birbaumer, S. Anders, and L. G. Cohen, “Motor learning elicited by voluntary drive,” Brain, vol. 126, no. 4, pp. 866–872, 2003. View at Publisher · View at Google Scholar · View at Scopus
  64. M.-S. Rioult-Pedotti, J. P. Donoghue, and A. Dunaevsky, “Plasticity of the synaptic modification range,” Journal of Neurophysiology, vol. 98, no. 6, pp. 3688–3695, 2007. View at Publisher · View at Google Scholar · View at Scopus
  65. M.-S. Rioult-Pedotti, D. Friedman, G. Hess, and J. P. Donoghue, “Strengthening of horizontal cortical connections following skill learning,” Nature Neuroscience, vol. 1, no. 3, pp. 230–234, 1998. View at Publisher · View at Google Scholar · View at Scopus
  66. T. McMorris, A. Turner, B. J. Hale, and J. Sproule, “Beyond the catecholamines hypothesis for an acute exercise-cognition interaction: a neurochemical perspective,” in Exercise-Cognition Interaction: Neuroscience Perspectives, T. McMorris, Ed., pp. 65–104, Academic Press, New York, NY, USA, 2016. View at Google Scholar
  67. T. McMorris, J. Sproule, A. Turner, and B. J. Hale, “Acute, intermediate intensity exercise, and speed and accuracy in working memory tasks: A meta-analytical comparison of effects,” Physiology and Behavior, vol. 102, no. 3-4, pp. 421–428, 2011. View at Publisher · View at Google Scholar · View at Scopus
  68. M. Takimoto and T. Hamada, “Acute exercise increases brain region-specific expression of MCT1, MCT2, MCT4, GLUT1, and COX IV proteins,” Journal of Applied Physiology, vol. 116, no. 9, pp. 1238–1250, 2014. View at Publisher · View at Google Scholar · View at Scopus
  69. M. Coco, G. Alagona, G. Rapisarda et al., “Elevated blood lactate is associated with increased motor cortex excitability,” Somatosensory and Motor Research, vol. 27, no. 1, pp. 1–8, 2010. View at Publisher · View at Google Scholar · View at Scopus
  70. E. M. Robertson and D. A. Cohen, “Understanding consolidation through the architecture of memories,” The Neuroscientist, vol. 12, no. 3, pp. 261–271, 2006. View at Publisher · View at Google Scholar · View at Scopus
  71. E. M. Robertson, A. Pascual-Leone, and R. C. Miall, “Current concepts in procedural consolidation,” Nature Reviews Neuroscience, vol. 5, no. 7, pp. 576–582, 2004. View at Publisher · View at Google Scholar · View at Scopus
  72. R. M. Brown, E. M. Robertson, and D. Z. Press, “Sequence skill acquisition and off-line learning in normal aging,” PLoS ONE, vol. 4, no. 8, Article ID e6683, 2009. View at Publisher · View at Google Scholar · View at Scopus
  73. S. Fischer, M. F. Nitschke, U. H. Melchert, C. Erdmann, and J. Born, “Motor memory consolidation in sleep shapes more effective neuronal representations,” The Journal of Neuroscience, vol. 25, no. 49, pp. 11248–11255, 2005. View at Publisher · View at Google Scholar · View at Scopus
  74. A. Karni, G. Meyer, C. Rey-Hipolito et al., “The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 3, pp. 861–868, 1998. View at Publisher · View at Google Scholar · View at Scopus
  75. G. Albouy, S. Fogel, B. R. King et al., “Maintaining vs. enhancing motor sequence memories: respective roles of striatal and hippocampal systems,” NeuroImage, vol. 108, pp. 423–434, 2015. View at Publisher · View at Google Scholar · View at Scopus
  76. J. Doyon, V. Penhune, and L. G. Ungerleider, “Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning,” Neuropsychologia, vol. 41, no. 3, pp. 252–262, 2003. View at Publisher · View at Google Scholar · View at Scopus
  77. J. Doyon and H. Benali, “Reorganization and plasticity in the adult brain during learning of motor skills,” Current Opinion in Neurobiology, vol. 15, no. 2, pp. 161–167, 2005. View at Publisher · View at Google Scholar · View at Scopus
  78. D. A. Cohen, A. Pascual-Leone, D. Z. Press, and E. M. Robertson, “Off-line learning of motor skill memory: a double dissociation of goal and movement,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 50, pp. 18237–18241, 2005. View at Publisher · View at Google Scholar · View at Scopus