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Association Between Fast and Slow Learning and Molecular Processes in Repetitive Practice: A Post Hoc Analysis

  • Tércio Apolinário-SouzaEmail author
  • Ana Flavia Santos-Almeida
  • Natália Lelis Torres
  • Juliana Otoni Parma
  • Lidiane Aparecida Fernandes
  • Grace Schenatto Pereira
  • Guilherme Menezes Lage
Conference paper
Part of the Communications in Computer and Information Science book series (CCIS, volume 1068)

Abstract

The explanations for the positive effects of less repetitive practice in learning, compared to more repetitive practice, converge towards an idea of a greater memory strengthening in less repetitive practice. These benefits are associated with the AMPA glutamate receptor. However, there are no studies in the literature that explain, in molecular terms, how memory processes during practice (or acquisition) are associated with these benefits. Overall, the process of memory strengthening in the acquisition of a motor skill has two distinct stages: a fast initial performance improvement followed by a gradual change associated with the memory state termed slow learning. Computational models, like the multi-rate learning model, help to identify these two distinct stages (fast and slow learning). This study aimed to investigate if the AMPA receptors are associated with the memory’s fast state (fast learning) and slow state (slow learning). Mice (n = 30) practiced the rotarod in two days of constant (one rotation frequency) or varied (three different rotation frequencies) practice. Animals were tested both 24 h and 10 days after acquisition. Two analyses were conducted, stepwise discriminant analysis and analysis of the difference between the predicted and observed values. Varied practice was more associated with the slow state. The findings of the present study advance in the explanations of the molecular mechanisms underpinning the greater memory strengthening proposed by behavioral hypotheses. Furthermore, we propose an alternative explanation for the explanations formulated at behavioral level, highlighting the role of the reference of the error that is produced trial-to-trial.

Keywords

Motor learning Practice schedule AMPA receptor Fast learning Slow learning 

Notes

Acknowledgments

This study was supported by Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) (grant APQ-03305-15) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES), finance Code 001.

References

  1. 1.
    Lee, T.D., Swanson, L.R., Hall, A.L.: What is repeated in a repetition? Effects of practice conditions on motor skill acquisition. Phys. Ther. 71, 150–156 (1991)CrossRefGoogle Scholar
  2. 2.
    Shea, C.H., Kohl, R., Indermill, C.: Contextual interference: contributions of practice. Acta Psychol. (Amst) 73, 145–157 (1990).  https://doi.org/10.1016/0001-6918(90)90076-RCrossRefGoogle Scholar
  3. 3.
    Moxley, S.E.E.: Schema: the variability of practice hypothesis. J. Mot. Behav. 11, 65–70 (1979)CrossRefGoogle Scholar
  4. 4.
    Shea, J.B., Morgan, R.L.: Contextual interference effects on the acquisition, retention, and transfer of a motor skill. J. Exp. Psychol. 5, 179–187 (1979)Google Scholar
  5. 5.
    Lee, T., Magill, R.: The locus of contextual interference in motor-skill acquisition. J. Exp. Psychol. Learn. Mem. Cogn. 9, 730–746 (1983)CrossRefGoogle Scholar
  6. 6.
    Apolinário-Souza, T., Santos Almeida, A.F., Lelis-Torres, N., Parma, J.O., Pereira, G.S., Lage, G.M.: Molecular mechanisms associated with the benefits of variable practice in motor learning. J. Mot. Behav. 51, 1–12 (2019).  https://doi.org/10.1080/00222895.2019.1649997CrossRefGoogle Scholar
  7. 7.
    Tabone, C.J., Ramaswami, M.: Is NMDA receptor-coincidence detection required for learning and memory? Neuron 74, 767–769 (2012).  https://doi.org/10.1016/j.neuron.2012.05.008CrossRefGoogle Scholar
  8. 8.
    Zito, K.: NMDA receptor function and physiological modulation. In: Encyclopedia of Neuroscience, pp. 1157–1164 (2009)CrossRefGoogle Scholar
  9. 9.
    Lisman, J.E.: Three Ca2+ levels affect plasticity differently: the LTP zone, the LTD zone and no man’s land. J. Physiol. 532, 285 (2001)CrossRefGoogle Scholar
  10. 10.
    Lisman, J., Yasuda, R., Raghavachari, S.: Mechanisms of CaMKII action in long-term potentiation. Nat. Rev. Neurosci. 6, 2166–2171 (2008).  https://doi.org/10.1038/nrn3192CrossRefGoogle Scholar
  11. 11.
    Rumpel, S., Ledoux, J., Zador, A., Malinow, R.: Postsynaptic receptor trafficking underlying a form of associative learning. Science 308, 83–88 (2005).  https://doi.org/10.1126/science.1103944CrossRefGoogle Scholar
  12. 12.
    Karni, A., et al.: The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex. Proc. Natl. Acad. Sci. 95, 861–868 (1998).  https://doi.org/10.1073/pnas.95.3.861CrossRefGoogle Scholar
  13. 13.
    Smith, M.A., Ghazizadeh, A., Shadmehr, R.: Interacting adaptive processes with different timescales underlie short-term motor learning. PLoS Biol. 4, 1035–1043 (2006).  https://doi.org/10.1371/journal.pbio.0040179CrossRefGoogle Scholar
  14. 14.
    Ungerleider, L., Doyon, J., Karni, A.: Imaging brain plasticity during motor skill learning. Neurobiol. Learn. Mem. 78, 553–564 (2002).  https://doi.org/10.1006/nlme.2002.4091CrossRefGoogle Scholar
  15. 15.
    Thoroughman, K.A., Shadmehr, R.: Learning of action trough adaptative combination of motor primitives. Nature 407, 742–747 (2000).  https://doi.org/10.1038/35037588.LearningCrossRefGoogle Scholar
  16. 16.
    Scheidt, R.A., Dingwell, J.B., Mussa-ivaldi, F.A., Robert, A., Dingwell, J.B., Ferdinando, A.: Learning to Move Amid Uncertainty. J. Neurophysiol. 86, 971–985 (2001). citeulike-article-id:406856CrossRefGoogle Scholar
  17. 17.
    Albert, S.T., Shadmehr, R.: Estimating properties of the fast and slow adaptive processes during sensorimotor adaptation. J. Neurophysiol. 119, 1367–1393 (2017).  https://doi.org/10.1152/jn.00197.2017CrossRefGoogle Scholar
  18. 18.
    Bradford, M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254 (1976).  https://doi.org/10.1016/0003-2697(76)90527-3CrossRefGoogle Scholar
  19. 19.
    Grosshans, D.R., Clayton, D.A., Coultrap, S.J., Browning, M.D.: LTP leads to rapid surface expression of NMDA but not AMPA receptors in adult rat CA1. Nat. Neurosci. 5, 27–33 (2002).  https://doi.org/10.1038/nn779CrossRefGoogle Scholar
  20. 20.
    Trewartha, K.M., Garcia, A., Wolpert, D.M., Flanagan, J.R.: Fast but fleeting: adaptive motor learning processes associated with aging and cognitive decline. J. Neurosci. 34, 13411–13421 (2014).  https://doi.org/10.1523/JNEUROSCI.1489-14.2014CrossRefGoogle Scholar
  21. 21.
    Schweighofer, N., et al.: Mechanisms of the contextual interference effect in individuals poststroke. J. Neurophysiol. 106, 2632–2641 (2011).  https://doi.org/10.1152/jn.00399.2011CrossRefGoogle Scholar
  22. 22.
    Lage, G.M., Vieira, M.M., Palhares, L., Ugrinowitsch, H., Benda, R.: Practice schedules and number of skills as contextual interference factors in the learning of positioning timing tasks. J. Hum. Mov. Stud. 50, 185–200 (2006)Google Scholar
  23. 23.
    Silva, A.B., Lage, G.M., Gonçalves, W., Palhares, L.R., Ugrinowitsch, R., Benda, H.: Contextual interference and manipulation of generalized motor programs and parameters in timing tasks. J. Sport Exerc. Psychol. 26, 173 (2004)Google Scholar
  24. 24.
    Schmidt, R.A.: A schema theory of discrete motor skill learning. Psychol. Rev. 82, 225–260 (1975)CrossRefGoogle Scholar
  25. 25.
    Shea, J.B., Zimny, S.T.: Context effects in memory and learning movement information. Mem. Control Action. 12, 345–365 (1983)CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Tércio Apolinário-Souza
    • 1
    • 2
    • 4
    Email author
  • Ana Flavia Santos-Almeida
    • 3
  • Natália Lelis Torres
    • 1
  • Juliana Otoni Parma
    • 1
  • Lidiane Aparecida Fernandes
    • 1
  • Grace Schenatto Pereira
    • 3
  • Guilherme Menezes Lage
    • 1
  1. 1.School of Physical Education, Physiotherapy and Occupational Therapy, NNeuroMUniversidade Federal de Minas GeraisBelo HorizonteBrazil
  2. 2.Department of Human Movement Sciences, GEPECOMUniversidade do Estado de Minas GeraisIbiritéBrazil
  3. 3.Institute of Biological Sciences, NNCUniversidade Federal de Minas GeraisBelo HorizonteBrazil
  4. 4.Belo HorizonteBrazil

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