fMRI Investigation of Cortical and Subcortical Networks in the Learning of Abstract and Effector-Specific Representations of Motor Sequences

Bapi, Dr. Raju S. and Miyapuram, Mr. K. P. and Graydon, Dr. F. X. and Doya, Dr. Kenji (2006) fMRI Investigation of Cortical and Subcortical Networks in the Learning of Abstract and Effector-Specific Representations of Motor Sequences. [Journal (Paginated)]

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A visuomotor sequence can be learned as a series of visuo-spatial cues or as a sequence of effector movements. Earlier imaging studies have revealed that a network of brain areas is activated in the course of motor sequence learning. However these studies do not address the question of the type of representation being established at various stages of visuomotor sequence learning. In an earlier behavioral study, we demonstrated that acquisition of visuo-spatial sequence representation enables rapid learning in the early stage and progressive establishment of somato-motor representation helps speedier execution by the late stage. We conducted functional magnetic resonance imaging (fMRI) experiments wherein subjects learned and practiced the same sequence alternately in normal and rotated settings. In one rotated setting (visual), subjects learned a new motor sequence in response to an identical sequence of visual cues as in normal. In another rotated setting (motor), the display sequence was altered as compared to normal, but the same sequence of effector movements were used to perform the sequence. Comparison of different rotated settings revealed analogous transitions both in the cortical and subcortical sites during visuomotor sequence learning  a transition of activity from parietal to parietal-premotor and then to premotor cortex and a concomitant shift was observed from anterior putamen to a combined activity in both anterior and posterior putamen and finally to posterior putamen. These results suggest a putative role for engagement of different cortical and subcortical networks at various stages of learning in supporting distinct sequence representations.

Item Type:Journal (Paginated)
Additional Information:Citation Information: Neuroimage. 2006 Aug 15;32(2):714-27
Keywords:Sequence representation, Anterior striatum, Posterior striatum, DLPFC, pre-SMA, SMA
Subjects:Neuroscience > Brain Imaging
ID Code:5114
Deposited By:Miyapuram, Mr Krishna
Deposited On:01 Sep 2006
Last Modified:11 Mar 2011 08:56

References in Article

Select the SEEK icon to attempt to find the referenced article. If it does not appear to be in cogprints you will be forwarded to the paracite service. Poorly formated references will probably not work.

Alexander, G.E., DeLong, M.R., Strick, P.L., 1986. Parallel Organization of functionally segregated circuits linking basal ganglia and cortex. Ann. Rev. Neurosci. 9, 357–381.

Bapi, R.S., Doya, K., Harner, A.M., 2000. Evidence for effector independent and effector dependent representations and their differential time course of acquisition during motor sequence learning. Exp. Brain Res. 132, 149–162.

Bland, J.M., Altman, D.G., 1994. Correlation, regression, and repeated data. BMJ 308, 896.

Bower, J., 1995. The cerebellum as a sensory acquisition controller. Hum. Brain Mapp. 2, 255–256.

Brett, M., Christoff, K., Cusack, R., Lancaster, J., 2001. Using the Talairach atlas with the MNI template. NeuroImage, 13, S85.

Caminiti, R., Ferraina, S., Mayer, A.B., 1998. Visuomotor transformations: Early cortical mechanisms of reaching. Curr. Opin. Neurobiol. 8, 753–761.

Doyon, J., Penhune, V., Ungerleider, L.G., 2003. Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning. Neuropsychologia 41(3), 252–262.

Fitts, P.M., (1964). Perceptual-motor skill learning. In A.W. Melton (ed), Categories of human learning. Academic Press, New York, pp 243--285.

Friston, K.J., Ashburner, J., Frith, C.D., Poline, J-B., Heather, J.D., Frackowiak, R.S. J., 1995a. Spatial registration and normalisation of images. Hum. Brain Mapp. 2, 165-189.

Friston, K.J., Holmes, A.P., Worsley, K.J., Poline, J-B., Frith, C.D., Frackowiak, R.S. J., 1995b. Statistical parametric maps in functional imaging: A general linear approach. Hum. Brain Mapp. 2, 189–210.

Grafton, S.T., Hazeltine, E., Ivry, R., 1995. Functional mapping of sequence learning in normal humans. J. Cog. Neurosci. 7, 497–510.

Grafton, S.T., Hazeltine, E., Ivry, R.B., 1998. Abstract and effector-specific representations of motor sequences identified with PET. J. Neurosci. 18, 9420–9428.

Harrington, D.L., Rao, S.M., Haaland, K.Y., Bobholz, J.A., Mayer, A.R., Binder, J.R., Cox, R.W., 2000. Specialized neural systems underlying representations of sequential movements. J. Cog. Neurosci. 12, 56-77.

Hikosaka, O., Rand, M.K., Miyachi, S., Miyashita, K., 1995. Learning of sequential movements in the monkey: Process of learning and retention of memory. J. Neurophysiol. 74, 1652–1661.

Hikosaka, O., Sakai, K., Miyauchi, S., Takino, R., Sasaki, Y., Putz, B., 1996. Activation of human presupplementary motor area in learning of sequential procedures: a functional MRI study. J. Neurophysiol. 76, 617–621.

Hikosaka, O., Nakahara, H., Rand, M.K., Sakai, K., Lu, X., Nakamura, K., Miyachi, S., Doya, K., 1999. Parallel neural networks for learning sequential procedures. Trends Neurosci. 22, 464–471.

Hikosaka, O., Nakamura, K., Sakai, K., & Nakahara, H., 2002. Central mechanisms of motor skill learning. Curr. Opin. Neurobiol. 12, 217–222.

Holmes, A.P., Friston, K.J., 1998. Generalisability, random effects and population inference. NeuroImage 7, S754.

Jenkins, I.H., Brooks, D.J., Nixon, P.D., Frackowiak, R.S., Passingham, R.E., 1994. Motor sequence learning: A study with positron emission tomography. J. Neurosci. 14, 3775–3790.

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

Jueptner, M., Frith, C.D., Brooks, D.J., Frackowiak, R.S.J., Passingham, R.E., 1997b. Anatomy of motor learning. II. Subcortical structures and learning by trial and error. J. Neurophysiol. 77, 1325–1337.

Jueptner, M., Weiller, C., 1998. A review of differences between basal ganglia and cerebellar control of movements as revealed by functional imaging studies. Brain 121, 1437–1449.

Karni, A., Meyer, G., Jezzard, P., Adams, M.M., Turner, R., Ungerleider, L.G., 1995. Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 377, 155–158.

Keele, S.W., Ivry, R., Mayr, U., Hazeltine, E., 2003. The cognitive and neural architecture of sequence representation. Psychol. Rev. 110(2), 316–339.

Lancaster, J.L., Woldorff, M.G., Parsons, L.M., Liotti, M., Freitas, C.S., Rainey, L., Kochunov, P.V., Nickerson, D., Mikiten, S.A., Fox, P.T., 2000. Automated Talairach atlas labels for functional brain mapping. Hum. Brain Mapp. 10, 120–131.

Maldjian, J.A., Laurienti, P.J., Kraft, R.A., Burdette, J.H., 2003. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fmri data sets. NeuroImage 19, 1233–1239.

Mishkin, M., Ungerleider, L.G., Macko, K.A., 1983. Object vision and spatial vision: Two cortical pathways. Trends Neurosci. 6, 414–417.

Nakahara, H., Doya, K., Hikosaka, O., 2001. Parallel cortico basal ganglia mechanisms for acquisition and execution of visuomotor sequences – a computational approach. J. Cog Neurosci. 13, 626–647.

Pammi, V. S. C., Miyapuram, K. P., Bapi, R. S., & Doya, K., 2004. Chunking Phenomenon in Complex Sequential Skill Learning in Humans. In Pal, N.R., Kasabov, N., Mudi, R.K., Pal, S., Parui, S.K. (Eds.), Lecture Notes in Computer Science, Springer-Verlag Heidelberg, 3316, 294– 299.

Penhune, V.B., Doyon, J., 2002. Dynamic cortical and subcortical networks in learning and delayed recall of timed motor sequences. J. Neurosci. 22(4), 1397–1406.

Penny, W.D., Holmes, A.P., Friston, K.J., 2003. Random effects analysis. In R.S.J. Frackowiak, K.J. Friston, C. Frith, R. Dolan, K.J. Friston, C.J. Price, S. Zeki, J. Ashburner, and W.D. Penny (ed), Human Brain Function. Academic Press, 2nd edition.

Rorden C, Brett M., 2000. Stereotaxic display of brain lesions. Behav Neurology 12(4), 191–200.

Sakai, K., Hikosaka, O., Miyauchi, S., Takino, R., Sasaki, Y., Putz, B., 1998. Transition of brain activation from frontal to parietal areas in visuomotor sequence learning. J. Neurosci. 18, 1827–1840.

Sakai, K., Hikosaka, O., Takino, R., Miyauchi, S., Nielsen, M., Tamada, T., 2000. What and when–parallel and convergent processing in motor control. J. Neurosci. 20, 2691–2700.

Sakai, K., Kitaguchi, K., & Hikosaka, O., 2003. Chunking during human visuomotor sequence learning. Exp. Brain Res., 132, 149–162.

Sanes, J.N., 2003. Neocortical mechanisms in motor learning. Curr. Opin. Neurobiol. 13, 225–231.

Shadmehr, R., Holcomb, H.H., 1997. Neural Correlates of Motor Memory Consolidation, Science, 277, 821-825.

Shima, K., Mushiake, H., Saito, N., Tanji, J., 1996. Role for cells in the presupplementary motor area in updating motor plans. Proc. Nat. Acad. Sci., USA 93(16), 8694–8698.

Smith, S.M., 2002. Fast robust automated brain extraction. Hum. Brain Mapp. 17(3), 143–155.

Talairach, J., Tournoux, P., 1988. Co-planar stereotaxic atlas of the human brain. New York: Thieme.

Tanji, J., Shima, K., 1994. Role of supplementary motor areas cells in planning several movements ahead. Nature 371, 413–416.

Tanji, J., 2001. Sequential organization of multiple movements: Involvement of cortical motor areas. Ann. Rev. Neurosci. 24, 631–651.

Toni, I., Krams, M., Turner, R., Passingham, R.E., 1998. The time course of changes during motor sequence learning: a whole-brain fMRI study. NeuroImage 8, 50–61.

Willingham, D.B., 1998. A neuropsychological theory of motor skill learning. Psychol. Rev. 105, 558–584.

Wise, S.P., Boussaoud, D., Johnson, P.B., Caminiti, R., 1997. Premotor and parietal cortex: Corticocortical connectivity and combinatorial computations. Ann. Rev. Neurosci. 20, 25–42.


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