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.
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.
Bates, D., Mächler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67, 1–48.
Battistoni, E., Stein, T., & Peelen, M. V. (2017). Preparatory attention in visual cortex. Annals of the New York Academy of Sciences, 1396, 92–107.
Beckmann, C., Jenkinson, M., & Smith, S. M. (2003). General multi-level linear modelling for group analysis in FMRI. Neuroimage, 20, 1052–1063.
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.
Bo, J., & Seidler, R. D. (2009). Visuospatial working memory capacity predicts the organization of acquired explicit motor sequences. Journal of Neurophysiology, 101, 3116–3125.
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.
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.
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.
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.
Dayan, E., & Cohen, L. G. (2011). Review neuroplasticity subserving motor skill learning. Neuron, 72, 443–454.
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.
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.
Diedrichsen, J., Balsters, J. H., Flavell, J., Cussans, E., & Ramnani, N. (2009). A probabilistic MR atlas of the human cerebellum. Neuroimage, 46, 39–46.
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.
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.
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.
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.
Gasquoine, P. G. (2013). Localization of function in anterior cingulate cortex: From psychosurgery to functional neuroimaging. Neuroscience and Biobehavioral Reviews, 37, 340–348.
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.
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.
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.
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.
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.
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.
Hikosaka, O., Nakamura, K., Sakai, K., & Nakahara, H. (2002). Central mechanisms of motor skill learning. Current Opinion in Neurobiology, 12, 217–222.
Hopfinger, J. B., Buonocore, M. H., & Mangun, G. R. (2000). The neural mechanisms of top- down attentional control. Nature Neuroscience, 3, 284–291.
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.
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.
Jubault, T., Ody, C., & Koechlin, E. (2007). Serial organization of human behavior in the inferior parietal cortex. The Journal of Neuroscience, 27, 11028–11036.
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.
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.
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.
Lara, A. H., & Wallis, J. D. (2015). The role of prefrontal cortex in working memory: A mini review. Frontiers in Systems Neuroscience, 9, 173.
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.
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.
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.
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.
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.
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.
Nissen, M. J., & Bullemer, P. (1987). Attention requirements of learning: Evidence from performance measures. Cognitive Psychology, 19, 1–32.
Oldfield, R. C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9, 97–113.
Penhune, V. B., & Doyon, J. (2005). Cerebellum and M1 interaction during early learning of timed motor sequences. Neuroimage, 26, 801–812.
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.
R Core Team. (2017). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
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.
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.
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.
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.
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.
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.
van den Heuvel, M. P., & Sporns, O. (2013). Network hubs in the human brain. Trends in Cognitive Sciences, 17, 683–696.
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.
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.
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
Corresponding author
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
About this article
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
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11682-019-00167-8