Prior Somatic Stimulation Improves Performance of Acquired Motor Skill by Facilitating Functional Connectivity in Cortico-Subcortical Motor Circuits

DOI: 10.4236/jbbs.2012.23039   PDF   HTML     4,702 Downloads   8,047 Views   Citations


Once people have a well-trained motor skill, their performance becomes stabilized and achieving substantial improvement is difficult. Recently, we have shown that even a plateaued hand motor skill can be upgraded with short-period electrical stimulation to the hand prior to the task. Here, we identify the neuronal substrates underlying the improvement of the plateaued skill by examining the enhanced functional connectivity in the sensory-motor regions that are associated with motor learning. We measured brain activity using functional magnetic resonance imaging and performed psychophysiological interaction analysis. We recruited seven right-handed very-well trained participants, whose motor performance of continuously rotating two balls with their right hands became stabilized at higher performance levels. We prepared two experiments, in each of which they repeated an experimental run 16 times. In each run, they performed this cyclic rotation as many times as possible in 16 s. In the thenar-stimulation experiment, we applied 60-s stimulation to the thenar muscle before each of the 5th - 12th runs, and the others were preceded by ineffective sham stimulation. In the control experiment, the sham was always provided. Thenar stimulation enabled the participants to perform the movements at higher cycles. In association with this performance improvement, we found enhanced activity couplings between the primary motor cortex and the sensorimotor territory of the putamen and between the cerebellum and the primary sensorimotor cortices, without any quantitative activity increase. Neither behavioral change nor these increased activity couplings were observed in the control.Thus, in contrast to the stable neuronal states in the cortico-subcortical motor circuits when the well-learned task is repeated at the later stages of motor skill learning, plastic changes in the motor circuits seem to be required when the plateaued skill is upgraded, and the stimulation may entail a state of readiness for the plastic change that allows subsequent performance improvement.

Share and Cite:

S. Uehara, I. Nambu, M. Matsumura, S. Kakei and E. Naito, "Prior Somatic Stimulation Improves Performance of Acquired Motor Skill by Facilitating Functional Connectivity in Cortico-Subcortical Motor Circuits," Journal of Behavioral and Brain Science, Vol. 2 No. 3, 2012, pp. 343-356. doi: 10.4236/jbbs.2012.23039.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] W. Bryan and N. Harter, “Studies in the Physiology and Psychology of Telegraphic Language,” Psychological Review, Vol. 4, No. 1, 1897, pp. 27-53. doi:10.1037/h0073806
[2] H. H. Yin, S. P. Mulcare, M. R. F. Hilario, E. Clouse, T. Holloway, M. I. Davis, A. C. Hansson, D. M. Lovinger and R. M. Costa, “Dynamic Reorganization of Striatal Circuits during the Acquisition and Consolidation of a Skill,” Nature Neuroscience, Vol. 12, No. 3, 2009, pp. 333-341. doi:10.1038/nn.2261
[3] S. Uehara, I. Nambu, S. Tomatsu, J. Lee, S. Kakei and E. Naito, “Improving Human Plateaued Motor Skill with Somatic Stimulation,” PLoS One, Vol. 6, No. 10, 2011, e25670. doi:10.1371/journal.pone.0025670
[4] L. G. Ungerleider, J. Doyon and A. Karni, “Imaging Brain Plasticity during Motor Skill Learning,” Neurobiology of Learning and Memory, Vol. 78, No. 3, 2002, pp. 553-564. doi:10.1006/nlme.2002.4091
[5] E. Naito, T. Nakashima, T. Kito, Y. Aramaki, T. Okada and N. Sadato, “Human Limb-Specific and Non-Limb-Specific Brain Representations during Kinesthetic Illusory Movements of the Upper and Lower Extremities,” European Journal of Neuroscience, Vol. 25, No. 11, 2007, pp. 3476-3487. doi:10.1111/j.1460-9568.2007.05587.x
[6] I. Toni, J. Rowe, K. E. Stephan and R. E. Passingham, “Changes of Cortico-Striatal Effective Connectivity during Visuomotor Learning,” Cerebral Cortex, Vol. 12, No. 10, 2002, pp. 1040-1047. doi:10.1093/cercor/12.10.1040
[7] F. T. Sun, L. M. Miller, A. A. Rao and M. D’Esposito, “Functional Connectivity of Cortical Networks Involved in Bimanual Motor Sequence Learning,” Cerebral Cortex, Vol. 17, No. 5, 2007, pp. 1227-1234. doi:10.1093/cercor/bhl033
[8] T. Wu, P. Chan and M. Hallett, “Modifications of the Interactions in the Motor Networks When a Movement Becomes Automatic,” Journal of Physiology, Vol. 586, No. 17, 2008, 4295-4304. doi:10.1113/jphysiol.2008.153445
[9] T. Wu, P. Chan and M. Hallett, “Effective Connectivity of Neural Networks in Automatic Movements in Parkinson’s Disease,” NeuroImage, Vol. 49, No. 3, 2010, pp. 2581-2587. doi:10.1016/j.neuroimage.2009.10.051
[10] R. C. Oldfield, “The Assessment and Analysis of Handedness: The Edinburgh Inventory,” Neuropsychologia, Vol. 9, No. 1, 1971, pp. 97-113. doi:10.1016/0028-3932(71)90067-4
[11] R. Kawashima, M. Matsumura, N. Sadato, E. Naito, A. Waki, S. Nakamura, K. Matsunami, H. Fukuda and Y. Yonekura, “Regional Cerebral Blood Flow Changes in Human Brain Related to Ipsilateral and Contralateral Complex Hand Movements—A PET Study,” European Journal of Neuroscience, Vol. 10, No. 7, 1998, pp. 2254-2260. doi:10.1046/j.1460-9568.1998.00237.x
[12] M. Matsumura, N. Sadato, T. Kochiyama, S. Nakamura, E. Naito, K. Matsunami, R. Kawashima, H. Fukuda and Y. Yonekura, “Role of the Cerebellum in Implicit Motor Skill Learning: A PET Study,” Brain Research Bulletin, Vol. 63, No. 6, 2004, pp. 471-483. doi:10.1016/j.brainresbull.2004.04.008
[13] U. Proske, D. L. Morgan and J. E. Gregory, “Thixotropy in Skeletal Muscle and in Muscle Spindles: A Review,” Progress in Neurobiology, Vol. 41, No. 6, 1993, pp. 705-721. doi:10.1016/0301-0082(93)90032-N
[14] E. Naito, F. Scheperjans, S. B. Eickhoff, K. Amunts, P. E. Roland, K. Zilles and H. H. Ehrsson, “Human Superior Parietal Lobule Is Involved in Somatic Perception of Bimanual Interaction with an External Object,” Journal of Neurophysiology, Vol. 99, No. 2, 2008, pp. 695-703. doi:10.1152/jn.00529.2007
[15] K. J. Friston, C. Buechel, G. R. Fink, J. Morris, E. Rolls and R. J. Dolan, “Psychophysiological and Modulatory Interactions in Neuroimaging,” NeuroImage, Vol. 6, No. 3, 1997, pp. 218-229. doi:10.1006/nimg.1997.0291
[16] N. Hagura, Y. Oouchida, Y. Aramaki, T. Okada, M. Matsumura, N. Sadato and E. Naito, “Visuokinesthetic Perception of Hand Movement Is Mediated by Cerebro-Cerebellar Interaction between the Left Cerebellum and Right Parietal Cortex,” Cerebral Cortex, Vol. 19, No. 1, 2009, pp. 176-186. doi:10.1093/cercor/bhn068
[17] Y. Yamakawa, R. Kanai, M. Matsumura and E. Naito, “Social Distance Evaluation in Human Parietal Cortex,” PLoS One, Vol. 4, No. 2, 2009, e4360. doi:10.1371/journal.pone.0004360
[18] E. Naito, P. E. Roland and H. H. Ehrsson, “I Feel My Hand Moving: A New Role of the Primary Motor Cortex in Somatic Perception of Limb Movement,” Neuron, Vol. 36, No. 36, 2002, pp. 979-988. doi:10.1016/S0896-6273(02)00980-7
[19] T. Talairach and P. Tournoux, “Co-Planar Stereotaxic At- las of the Human Brain,” Thieme, New York, 1988.
[20] J. D. Schmahmann, J. Doyon, A. W. Toga, M. Petrides and A. C. Evans, “MRI Atlas of the Human Cerebellum,” Academic Press, San Diego, 2000.
[21] S. B. Eickhoff, K. E. Stephan, H. Mohlberg, C. Grefkes, G. R. Fink, K. Amunts and K. Zilles, “A New SPM Toolbox for Combining Probabilistic Cytoarchitectonic Maps and Functional Imaging Data,” NeuroImage, Vol. 25, No.4, 2005, pp. 1325-1335. doi:10.1016/j.neuroimage.2004.12.034
[22] E. Naito and H. H. Ehrsson, “Somatic Sensation of Hand-Object Interactive Movement Is Associated with Activity in the Left Inferior Parietal Cortex,” Journal of Neuroscience, Vol. 26, No. 14, 2006, pp. 3783-379. doi:10.1523/JNEUROSCI.4835-05.2006
[23] N. Sadato, V. Ibanez, M. P. Deiber, G. Campbell, M. Leonardo and M. Hallett, ”Frequency-Dependent Changes of Regional Cerebral Blood Flow during Finger Movements,” Journal of Cerebral Blood Flow & Metabolism, Vol. 16, No. 1, 1996, pp. 23-33. doi:10.1097/00004647-199601000-00003
[24] R. S. Turner, S. T. Grafton, J. R. Votaw, M. R. Delong and J. M. Hoffman, “Motor Subcircuits Mediating the Control of Movement Velocity: A PET Study,” Journal of Neurophysiology, Vol. 80, No. 4, 1998, pp. 2162-2176.
[25] S. Lehericy, E. Bardinet, L. Tremblay, P. F. Van de Moortele, J. B. Pochon, D. Dormont, D. S. Kim, J. Yelnik and K. Ugurbil, “Motor Control in Basal Ganglia Circuits Using fMRI and Brain Atlas Approaches,” Cerebral Cortex, Vol. 16, No. 2, 2006, pp. 149-161. doi:10.1093/cercor/bhi089
[26] S. Lehericy, M. Ducros, A. Krainik, C. Francois, P. F. Van de Moortele, K. Ugurbil and D. S. Kim, “3-D Diffusion Tensor Axonal Tracking Shows Distinct SMA and Pre-SMA Projections to the Human Striatum,” Cerebral Cortex, Vol. 14, No. 12, 2004, pp. 1302-1309. doi:10.1093/cercor/bhh091
[27] S. Lehericy, M. Ducros, P. F. Van de Moortele, C. Francois, L. Thivard, C. Poupon, N. Swindale, K. Ugurbil and D. S. Kim, “Diffusion Tensor Fiber Tracking Shows Distinct Corticostriatal Circuits in Humans,” Annals of Neurology, Vol. 55, No. 4, 2004, pp. 522-529. doi:10.1002/ana.20030
[28] E. Naito, “Sensing Limb Movements in the Motor Cortex: How Humans Sense Limb Movement,” Neuroscientist, Vol. 10, No. 1, 2004, pp. 73-82. doi:10.1177/1073858403259628
[29] R. Fuentes, P. Petersson, W. B. Siesser, M. G. Caron and M. A. Nicolelis, “Spinal Cord Stimulation Restores Locomotion in Animal Models of Parkinson’s Disease,” Science, Vol. 323, No. 5921, 2009, pp. 1578-1582. doi:10.1126/science.1164901
[30] R. Fuentes, P. Petersson and M. A. Nicolelis, “Restoration of Locomotive Function in Parkinson’s Disease by Spinal Cord Stimulation: Mechanistic Approach,” European Journal of Neuroscience, Vol. 32, No. 7, 2010, pp. 1100-1108. doi:10.1111/j.1460-9568.2010.07417.x
[31] M. R. De Long, M. D. Crutcher and A. P. Georgopoulous, “Primate Globus Pallidus and Subthalamic Nucleus: Functional Organization,” Journal of Neurophysiology, Vol. 53, No. 2, 1985, pp. 530-543.
[32] A. R. Luft, M. U. Manto and N. O. Ben Taib, “Modulation of Motor Cortex Excitability by Sustained Peripheral Stimulation: The Interaction between the Motor Cortex and the Cerebellum,” Cerebellum, Vol. 4, No. 2, 2005, pp. 90-96. doi:10.1080/14734220410019084
[33] J. A. Kleim, T. M. Hogg, P. M. VandenBerg, N. R. Cooper, R. Bruneau and M. Remple, “Cortical Synaptogenesis and Motor Map Reorganization Occur during Late, But Not Early, Phase of Motor Skill Learning,” The Journal of Neuroscience, Vol. 24, No. 3, 2004, pp. 628-633. doi:10.1523/JNEUROSCI.3440-03.2004
[34] K. Rosenkranz, A. Kacar and J. C. Rothwell, “Differential Modulation of Motor Cortical Plasticity and Excitability in Early and Late Phases of Human Motor Learning,” Journal of Neuroscience, Vol. 27, No. 44, 2007, pp. 12058-12066. doi:10.1523/JNEUROSCI.2663-07.2007
[35] T. H. Xu, X. Z. Yu, A. J. Perlik, W. F. Tobin, J. A. Zweig, K. Tennant, T. Jones and Y. Zuo, “Rapid Formation and Selective Stabilization of Synapses for Enduring Motor Memories,” Nature, Vol. 462, No. 7275, 2009, pp. 915-919. doi:10.1038/nature08389
[36] A. Pascual-Leone, J. Grafman and M. Hallett, “Modulation of Motor Output Maps during Development of Implicit and Explicit Knowledge,” Science, Vol. 263, No. 5151, 1994, pp. 1287-1289. doi:10.1126/science.8122113
[37] A. Pascual-Leone, N. Dang, L. G. Cohen, J. P. BrasilNeto, A. Cammarota and M. Hallett, “Modulation of Muscle Responses Evoked by Transcranial Magnetic Stimulation during the Acquisition of New Fine Motor Skills,” Journal of Neurophysiology, Vol. 74, No. 3, 1995, pp. 1037-1045.
[38] A. Karni, G. Meyer, P. Jezzard, M. M. Adams, R. Turner and L. G. Ungerleider, “Functional MRI Evidence for Adult Motor Cortex Plasticity during Motor Skill Learning,” Nature, Vol. 377, No. 6545, 1995, pp. 155-158. doi:10.1038/377155a0
[39] W. Muellbacher, U. Ziemann, J. Wissel, N. Dang, M. Kofler, S. Facchini, B. Boroojerdi, W. Poewe and M. Hallett, “Early Consolidation in Human Primary Motor Cortex,” Nature, Vol. 415, No. 6872, 2002, pp. 640-644. doi:10.1038/nature712
[40] J. Reis, H. M. Schambra, L. G. Cohen, E. R. Buch, B. Fritsch, E. Zarahn, P. A. Celnik and J. W. Krakauer, “Noninvasive Cortical Stimulation Enhances Motor Skill Acquisition over Multiple Days through and Effect on Consolidataion,” Proceedings of the National Academy of Sciences of USA, Vol. 106, No. 5, 2009, pp. 1290-1295. doi:10.1073/pnas.0805413106
[41] P. D. Cheney and E. E. Fetz, “Functional Classes of Primate Corticomotoneuronal Cells and Their Relation to Active Force,” Journal of Neurophysiology, Vol. 44, No. 4, 1980, pp. 773-791.
[42] C. Dettmers, G. R. Fink, R. N. Lemon, K. M. Stephan, R. E. Passingham, D. Silbersweig, A. Holmes, M. C. Ridding, D. J. Brooks and R. S. Frackowiak, “Relation between Cerebral Activity and Force in the Motor Areas of the Human Brain,” Journal of Neurophysiology, Vol. 74, No. 2, 1995, pp. 802-815.
[43] O. Hikosaka, K. Nakamura, K. Sakai and H. Nakahara, “Central Mechanisms of Motor Skill Learning,” Current Opinion in Neurobiology, Vol. 12, No. 2, 2002, pp. 217-222. doi:10.1016/S0959-4388(02)00307-0
[44] 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, 2005, pp. 161-167. doi:10.1016/j.conb.2005.03.004
[45] K. Debas, J. Carrier, P. Orban, M. Barakat, O. Lungu, G. Vandewalle, A. H. Tahar, P. Bellec, A. Karni, L. G. Ungerleider, H. Benali and J. Doyon, “Brain Plasticity Related to the Consolidation of Motor Sequence Learning and Motor Adaptation,” Proceedings of the National Academy of Sciences of USA, Vol. 107, No. 41, 2010, pp. 17839-17844. doi:10.1073/pnas.1013176107
[46] O. Hikosaka, H. Nakahara, M. K. Rand, K. Sakai K, X. F. Lu, K. Nakamura, S. Miyachi and K. Doya, “Parallel Neural Networks for Learning Sequential Procedures,” Trends in Neurosciences, Vol. 22, No. 10, 1999, pp. 464-471. doi:10.1016/S0166-2236(99)01439-3
[47] S. Lehericy, H. Benali, P. F. Van de Moortele, M. Pelegrini-Issac, T. Waechter, K. Ugurbil and J. Doyon, “Distinct Basal Ganglia Territories Are Engaged in Early and Advanced Motor Sequence Learning,” Proceedings of the National Academy of Sciences of USA, Vol. 102, No. 35, 2005, pp. 12566-12571. doi:10.1073/pnas.0502762102
[48] D. Coynel, G. Marrelec, V. Perlbarq, M. Peleqrini-Issac, P. F. Van de Moortele, K. Ugurbil, J. Doyon, H. Benali and S. Lehericy, “Dynamics of Motor-Related Functional Integration during Motor Sequence Learning,” NeuroImage, Vol. 49, No. 1, 2010, pp. 759-766. doi:10.1016/j.neuroimage.2009.08.048
[49] S. Miyachi, O. Hikosaka, K. Miyashita, Z. Karadi and M. K. Rand, “Differential Roles of Monkey Striatum in Learning of Sequential Hand Movement,” Experimental Brain Research, Vol. 115, No. 1, 1997, pp. 1-5. doi:10.1007/PL00005669
[50] G. E. Alexander and M. D. Crutcher, “Functional Architecture of Basal Ganglia Circuits: Neural Substrates of Parallel Processing,” Trends in Neurosciences, Vol. 13, No. 7, 1990, pp. 266-271. doi:10.1016/0166-2236(90)90107-L
[51] J. W. Mink, “The Basal Ganglia: Focused Selection and Inhibition of Competing Motor Programs,” Progress in Neurobiology, Vol. 50, No. 4, 1996, pp. 381-425. doi:10.1016/S0301-0082(96)00042-1
[52] L. A. Boyd, J. D. Edwards, C. S. Sienqsukon, E. D. Vidoni, B. D. Wessel and M. A. Linsdell, “Motor Sequence Chunking Is Impaired by Basal Ganglia Stroke,” Neurobiology of Learning and Memory, Vol. 92, No. 1, 2009, pp. 35-44. doi:10.1016/j.nlm.2009.02.009
[53] K. Takakusaki, K. Saitoh, H. Harada and M. Kashiwayanagi, “Role of Basal Ganglia-Brainstem Pathways in the Control of Motor Behaviors,” Neuroscience Research, Vol. 50, No. 2, 2004, pp. 137-151. doi:10.1016/j.neures.2004.06.015
[54] P. L. Strick, R. P. Dum and J. A. Fiez, “Cerebellum and Nonmotor Function,” Annual Review of Neuroscience, Vol. 32, 2009, pp. 413-434. doi:10.1146/annurev.neuro.31.060407.125606
[55] K. A. Coffman, R. P. Dum and P. L. Strick, “Cerebellar Vermis Is a Target of Projections from the Motor Areas in the Cerebral Cortex,” Proceedings of the National Academy of Sciences of USA, Vol. 108, No. 38, 2011, pp. 16068-16073. doi:10.1073/pnas.1107904108
[56] M. Manto, J. M. Bower, A. B. Conforto, J. M. Delgado-Garcia, S. N. da Guarda, M. Gerwig, C. Habas, N. Hagura, R. B. Ivry, P. Marien, M. Molinari, E. Naito, D. A. Nowak, N. Oulad Ben Taib, D. Pelisson, C. D. Tesche, C. Tilikete and D. Timmann, “Roles of the Cerebellum in Motor Control—The Diversity of Ideas on Cerebellar Involvement in Movement,” Cerebellum, Vol. 11, No. 2, 2012, pp. 457-487.

comments powered by Disqus

Copyright © 2020 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.