Skip to main content
Log in

Short timescale modulation of cortical and cerebellar activity in the early phase of motor sequence learning: an fMRI study

  • Original Research
  • Published:
Brain Imaging and Behavior Aims and scope Submit manuscript

Abstract

Motor learning is a multi-stage process, in which the involvement of different brain regions is related to the specific stage. We aimed at characterising short timescale changes of brain activity induced by motor sequence learning. Twenty healthy volunteers performed a serial reaction time task during an MRI session in a 3 T scanner. The task consisted of two conditions: repeated and random, that were compared over the whole fMRI run, as well as within sections, to investigate brain activity modulating related to the learning stage. The whole fMRI run analysis showed a stronger response for the repeated condition in fronto-parietal regions, cerebellum and thalamus. The analysis on sections showed initially increased right cerebellar activity. In the subsequent phase, bilateral cerebellar activity was observed, while no increased activity was seen in the last phase, when the learning was established. At the neocortical level, the repeated condition showed stronger activity at first in fronto-parietal regions bilaterally, then lateralized to the right hemisphere in the last learning phase. This study showed short time scale brain activity modulation in cortical and cerebellar regions with involvement of different brain regions over the learning process not restricted to the motor circuit.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Basso, G., Magon, S., Reggiani, F., Capasso, R., Monittola, G., Yang, F.-J., & Miceli, G. (2013). Distinguishable neurofunctional effects of task practice and item practice in picture naming: A BOLD fMRI study in healthy subjects. Brain and Language, 126, 302–313.

    PubMed  Google Scholar 

  • Bates, D., Mächler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67, 1–48.

    Google Scholar 

  • Battistoni, E., Stein, T., & Peelen, M. V. (2017). Preparatory attention in visual cortex. Annals of the New York Academy of Sciences, 1396, 92–107.

    PubMed  Google Scholar 

  • Beckmann, C., Jenkinson, M., & Smith, S. M. (2003). General multi-level linear modelling for group analysis in FMRI. Neuroimage, 20, 1052–1063.

    PubMed  Google Scholar 

  • Bernard, J. A., & Seidler, R. D. (2013). Cerebellar contributions to visuomotor adaptation and motor sequence learning: An ALE meta-analysis. Frontiers in Human Neuroscience, 7, 27.

    PubMed  PubMed Central  Google Scholar 

  • Bo, J., & Seidler, R. D. (2009). Visuospatial working memory capacity predicts the organization of acquired explicit motor sequences. Journal of Neurophysiology, 101, 3116–3125.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Buckner, R. L., Krienen, F. M., Castellanos, A., Diaz, J. C., & Yeo, B. T. T. (2011). The organization of the human cerebellum estimated by intrinsic functional connectivity. Journal of Neurophysiology, 02138, 2322–2345.

    Google Scholar 

  • Caspers, S. (2015). Posterior parietal cortex: Structural and functional diversity. Brain Mapping: An Encyclopedic Reference,  317-323

  • Cavanna, A. E., & Trimble, M. R. (2006). The precuneus: A review of its functional anatomy and behavioural correlates. Brain, 129, 564–583.

    PubMed  Google Scholar 

  • Clower, D. M., West, R. A., Lynch, J. C., & Strick, P. L. (2001). The inferior parietal lobule is the target of output from the superior colliculus, hippocampus, and cerebellum. The Journal of Neuroscience, 21, 6283–6291.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Coynel, D., Marrelec, G., Perlbarg, V., Pélégrini-Issac, M., Van de Moortele, P.-F., Ugurbil, K., Doyon, J., Benali, H., & Lehéricy, S. (2010). Dynamics of motor-related functional integration during motor sequence learning. Neuroimage, 49, 759–766.

    PubMed  Google Scholar 

  • Dayan, E., & Cohen, L. G. (2011). Review neuroplasticity subserving motor skill learning. Neuron, 72, 443–454.

    CAS  PubMed  PubMed Central  Google Scholar 

  • de Schotten, M. T., Dell’Acqua, F., Forkel, S. J., Simmons, A., Vergani, F., Murphy, D. G. M., & Catani, M. (2011). A lateralized brain network for visuospatial attention. Nature Neuroscience, 14, 1245–1246.

    Google Scholar 

  • Desikan, R. S., Ségonne, F., Fischl, B., Quinn, B. T., Dickerson, B. C., Blacker, D., Buckner, R. L., Dale, A. M., Maguire, R. P., Hyman, B. T., Albert, M. S., & Killiany, R. J. (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage, 31, 968–980.

    PubMed  Google Scholar 

  • Diedrichsen, J., Balsters, J. H., Flavell, J., Cussans, E., & Ramnani, N. (2009). A probabilistic MR atlas of the human cerebellum. Neuroimage, 46, 39–46.

    PubMed  Google Scholar 

  • Doyon, J., Bellec, P., Amsel, R., Penhune, V., Monchi, O., Carrier, J., Lehéricy, S., & Benali, H. (2009). Contributions of the basal ganglia and functionally related brain structures to motor learning. Behavioural Brain Research, 199, 61–75.

    PubMed  Google Scholar 

  • Doyon, J., Penhune, V., & Ungerleider, L. G. (2003). Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning. Neuropsychologia, 41, 252–262.

    PubMed  Google Scholar 

  • Doyon J, Ungerleider LG (2002) Functional anatomy of motor skill Learninig. In: Neuropsychology of Memory, 3rd ed. (Squire LR, Schacter DL, eds). The Guilford Press.

  • Fletcher, P. C., Frith, C. D., Grasby, P. M., Shallice, T., Frackowiak, R. S., & Dolan, R. J. (1995). Brain systems for encoding and retrieval of auditory-verbal memory. An in vivo study in humans. Brain, 118(Pt 2), 401–416.

    PubMed  Google Scholar 

  • Floyer-Lea, A., & Matthews, P. M. (2005). Distinguishable brain activation networks for short- and long-term motor skill learning. Journal of Neurophysiology, 94, 512–518.

    CAS  PubMed  Google Scholar 

  • Gasquoine, P. G. (2013). Localization of function in anterior cingulate cortex: From psychosurgery to functional neuroimaging. Neuroscience and Biobehavioral Reviews, 37, 340–348.

    PubMed  Google Scholar 

  • Gobel, E. W., Parrish, T. B., & Reber, P. J. (2011). Neural correlates of skill acquisition: Decreased cortical activity during a serial interception sequence learning task. Neuroimage, 58, 1150–1157.

    PubMed  Google Scholar 

  • Goodale, M. A., Westwood, D. A., & Milner, A. D. (2004). Two distinct modes of control for object-directed action. Progress in Brain Research, 144, 131–144.

    PubMed  Google Scholar 

  • Grafton, S. T., Hazeltine, E., & Ivry, R. B. (2002). Motor sequence learning with the nondominant left hand: A PET functional imaging study. Experimental Brain Research, 146, 369–378.

    PubMed  Google Scholar 

  • Greger, B., & Norris, S. (2005). Simple spike firing in the posterior lateral cerebellar cortex of macaque Mulatta was correlated with success-failure during a visually guided reaching task. Experimental Brain Research, 167, 660–665.

    PubMed  Google Scholar 

  • Hanakawa, T., Dimyan, M. A., & Hallett, M. (2008). Motor planning, imagery, and execution in the distributed motor network: A time-course study with functional MRI. Cerebral Cortex, 18, 2775–2788.

    PubMed  PubMed Central  Google Scholar 

  • Hervé, P.-Y., Zago, L., Petit, L., Mazoyer, B., & Tzourio-Mazoyer, N. (2013). Revisiting human hemispheric specialization with neuroimaging. Trends in Cognitive Sciences, 17, 69–80.

    PubMed  Google Scholar 

  • Hikosaka, O., Nakamura, K., Sakai, K., & Nakahara, H. (2002). Central mechanisms of motor skill learning. Current Opinion in Neurobiology, 12, 217–222.

    CAS  PubMed  Google Scholar 

  • Hopfinger, J. B., Buonocore, M. H., & Mangun, G. R. (2000). The neural mechanisms of top- down attentional control. Nature Neuroscience, 3, 284–291.

    CAS  PubMed  Google Scholar 

  • Imamizu, H., Kuroda, T., Miyauchi, S., Yoshioka, T., & Kawato, M. (2003). Modular organization of internal models of tools in the human cerebellum. Proceedings of the National Academy of Sciences of the United States of America, 100, 5461–5466.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Imamizu, H., Miyauchi, S., Tamada, T., Sasaki, Y., Takino, R., Pütz, B., Yoshioka, T., & Kawato, M. (2000). Human cerebellar activity reflecting an acquired internal model of a new tool. Nature, 403, 192–195.

    CAS  PubMed  Google Scholar 

  • Jubault, T., Ody, C., & Koechlin, E. (2007). Serial organization of human behavior in the inferior parietal cortex. The Journal of Neuroscience, 27, 11028–11036.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jueptner, M., Stephan, K. M., Frith, C. D., Brooks, D. J., Frackowiak, R. S., & Passingham, R. E. (1997). Anatomy of motor learning. I. Frontal cortex and attention to action. J Neurophysiol, 77, 1313–1324.

    CAS  PubMed  Google Scholar 

  • Karni, A., Meyer, G., Rey-Hipolito, C., Jezzard, P., Adams, M. M., Turner, R., & Ungerleider, L. G. (1998). 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, 95, 861–868.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kelly, R. M., & Strick, P. L. (2003). Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate. The Journal of Neuroscience, 23, 8432–8444.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lara, A. H., & Wallis, J. D. (2015). The role of prefrontal cortex in working memory: A mini review. Frontiers in Systems Neuroscience, 9, 173.

    PubMed  PubMed Central  Google Scholar 

  • Lohse, K. R., Wadden, K., Boyd, L. A., & Hodges, N. J. (2014). Motor skill acquisition across short and long time scales: A meta-analysis of neuroimaging data. Neuropsychologia, 59, 130–141.

    CAS  PubMed  Google Scholar 

  • Ma, L., Narayana, S., Robin, D. A., Fox, P. T., & Xiong, J. (2011). Changes occur in resting state network of motor system during 4 weeks of motor skill learning. Neuroimage, 58, 226–233.

    PubMed  Google Scholar 

  • Magon, S., Donath, L., Gaetano, L., Thoeni, A., Radue, E.-W., Faude, O., & Sprenger, T. (2016). Striatal functional connectivity changes following specific balance training in elderly people: fMRI results of a randomized controlled pilot study. Gait & Posture, 49, 334–339.

  • Margulies, D. S., Vincent, J. L., Kelly, C., Lohmann, G., Uddin, L. Q., Biswal, B. B., Villringer, A., Castellanos, F. X., Milham, M. P., & Petrides, M. (2009). Precuneus shares intrinsic functional architecture in humans and monkeys. Proceedings of the National Academy of Sciences of the United States of America, 106, 20069–20074.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Maus, B., Van Breukelen, G. J. P., Goebel, R., & Berger, M. P. F. (2010). Optimization of block designs in fMRI studies. Psychometrika, 75, 373–390.

    Google Scholar 

  • Medina, J. F., & Lisberger, S. G. (2009). Encoding and decoding of learned smooth-pursuit eye movements in the floccular complex of the monkey cerebellum. Journal of Neurophysiology, 102, 2039–2054.

    PubMed  PubMed Central  Google Scholar 

  • Miall, R. C., & Jenkinson, E. W. (2005). Functional imaging of changes in cerebellar activity related to learning during a novel eye-hand tracking task. Experimental Brain Research, 166, 170–183.

    CAS  PubMed  Google Scholar 

  • Nissen, M. J., & Bullemer, P. (1987). Attention requirements of learning: Evidence from performance measures. Cognitive Psychology, 19, 1–32.

    Google Scholar 

  • Oldfield, R. C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9, 97–113.

    CAS  PubMed  Google Scholar 

  • Penhune, V. B., & Doyon, J. (2005). Cerebellum and M1 interaction during early learning of timed motor sequences. Neuroimage, 26, 801–812.

    CAS  PubMed  Google Scholar 

  • Puttemans, V., Wenderoth, N., & Swinnen, S. P. (2005). Changes in brain activation during the acquisition of a multifrequency bimanual coordination task: From the cognitive stage to advanced levels of automaticity. The Journal of Neuroscience, 25, 4270–4278.

    CAS  PubMed  PubMed Central  Google Scholar 

  • R Core Team. (2017). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

    Google Scholar 

  • Ramnani, N. (2012). Frontal lobe and posterior parietal contributions to the Cortico-cerebellar. Cerebellum, 11, 366–383.

  • Seidler, R. D., Bo, J., & Anguera, J. A. (2012). Neurocognitive contributions to motor skill learning: The role of working memory. Journal of Motor Behavior, 44, 445–453.

    PubMed  Google Scholar 

  • Shallice, T., Fletcher, P., Frith, C. D., Grasby, P., Frackowiak, R. S., & Dolan, R. J. (1994). Brain regions associated with acquisition and retrieval of verbal episodic memory. Nature, 368, 633–635.

    CAS  PubMed  Google Scholar 

  • Shum, M., Shiller, D. M., Baum, S. R., & Gracco, V. L. (2011). Sensorimotor integration for speech motor learning involves the inferior parietal cortex. The European Journal of Neuroscience, 34, 1817–1822.

    PubMed  PubMed Central  Google Scholar 

  • Soetedjo, R., & Fuchs, A. F. (2006). Complex spike activity of purkinje cells in the oculomotor vermis during behavioral adaptation of monkey saccades. The Journal of Neuroscience, 26, 7741–7755.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stoodley C.J., & Schmahmann J.D. (2018). Functional topography of the human cerebellum. Handb Clin Neurol., 154, 59-70

  • Sun, F. T., Miller, L. M., Rao, A. A., & D’Esposito, M. (2007). Functional connectivity of cortical networks involved in bimanual motor sequence learning. Cerebral Cortex, 17, 1227–1234.

    PubMed  Google Scholar 

  • Talairach J, & Tournoux P (1988) Co-planar stereotaxic atlas of the human brain : 3-dimensional proportional system: An approach to cerebral imaging. Thieme Publishing Group

  • Torchiano M (2017) Effsize: Efficient effect size computation. R Packag version 071.

  • Trinkler, I., King, J. A., Doeller, C. F., Rugg, M. D., & Burgess, N. (2009). Neural bases of autobiographical support for episodic recollection of faces. Hippocampus, 19, 718–730.

    PubMed  Google Scholar 

  • van den Heuvel, M. P., & Sporns, O. (2013). Network hubs in the human brain. Trends in Cognitive Sciences, 17, 683–696.

    PubMed  Google Scholar 

  • van Mier, H. I., Perlmutter, J. S., & Petersen, S. E. (2004). Functional changes in brain activity during acquisition and practice of movement sequences. Motor Control, 8, 500–520.

    PubMed  Google Scholar 

  • Wenderoth, N., Debaere, F., Sunaert, S., & Swinnen, S. P. (2005). The role of anterior cingulate cortex and precuneus in the coordination of motor behaviour. The European Journal of Neuroscience, 22, 235–246.

    PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank all participants without whom this study could not have been completed.

Funding

Financial support was partially provided by the Swiss Multiple Sclerosis Society (research proposal 2013).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stefano Magon.

Ethics declarations

All procedures performed in this study were in accordance with the ethical standards of the Swiss Ethic Committee on research involving humans (http://www.swissethics.ch) and with the 1964 Helsinki declaration and its later amendments.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Conflict of interest

All authors declare that they have no conflicts of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Magon, S., Pfister, A., Laura, G. et al. Short timescale modulation of cortical and cerebellar activity in the early phase of motor sequence learning: an fMRI study. Brain Imaging and Behavior 14, 2159–2175 (2020). https://doi.org/10.1007/s11682-019-00167-8

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-019-00167-8

Keywords

Navigation