Changes in Excitability of the Motor Cortex Associated with Internal Model Formation during Intrinsic Visuomotor Learning in the Upper Arm

Timothy Hunter, Paul Sacco, Duncan L. Turner

.

DOI: 10.4236/jbbs.2011.13019                

Abstract

Previous studies have shown that the primary motor cortex (M1) may drive part of the feed forward control of well learnt simple movements by specifying patterns of muscle activation. This study explored the role of the M1 in the feed forward control of newly formed movement patterns after motor adaptation. Ten healthy right-handed subjects performed planar, centre-out arm reaching movement trials with a robotic manipulandum in three phases: a null force field (baseline), a velocity-dependent force field (adaptation; 25 Nsm-1) and again in a null force field (deadaptation). Reaching error and voluntary EMG were recorded from the biceps and triceps before, during and after motor adaptation. We also explored the effects of motor adaptation on evoked responses to single and paired pulse Transcranial Magnetic Stimulation from the same muscles at different delays after a visual go command, but before the onset of voluntary muscle activity. After the force field was removed, subjects produced reaching overshoot characteristic of adaptive internal model formation. Following motor adaptation, there was a significant increase in corticospinal excitability, reduction in short interval intracortical inhibition and increase in short interval intracortical facilitation that was associated with a sustained increase in voluntary muscle activity in the biceps. The adaptation-driven increase in reaching overshoot coupled with the increase in voluntary activity, corticospinal and intracortical excitability in the biceps suggests that the M1 may specify some of the feed forward components of newly learnt internal models through the control of specific muscles.

Keywords

TMS, Internal Model Formation, Corticospinal Excitability

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	T. E. Milner and D. W. Franklin, “Impedance Control and Internal Model Use during the Initial Stage of Adaptation to Novel Dynamics in Humans,” The Journal of Physiology, Vol. 567, 2005, pp. 651-664. doi:10.1113/jphysiol.2005.090449
[2]	K.A. Thoroughman and R. Shadmehr, “Electromyographic Correlates of Learning an Internal Model of Reaching Movements,” The Journal of Neuroscience, Vol. 19, No. 19, 1999, pp. 8573-8588.
[3]	D. M. Wolpert, Z. Ghahramani and M. I. Jordan, “An Internal Model for Sensorimotor Integration,” Science, Vol. 269, No. 5232, 1995, pp. 1880-1882. http://dx.doi.org/10.1126/science.7569931
[4]	D. M. Wolpert and Z. Ghahramani, “Computational Principles of Movement Neuroscience,” Nature Neuroscience, Vol. 3, 2000, pp. 1212-1217. doi:10.1038/81497
[5]	C. Padoa-Schioppa, C. S. Li and E. Bizzi, “Neuronal Correlates of Kinematics-to-Dynamics Transformation in the Supplementary Motor Area,” Neuron, Vol. 36, No. 4, 2002, pp. 751-765. doi:10.1016/S0896-6273(02)01028-0
[6]	C. S. Li, C. Padoa-Schioppa and E. Bizzi, “Neuronal Correlates of Motor Performance and Motor Learning in the Primary Motor Cortex of Monkeys Adapting to an External Force Field,” Neuron, Vol. 30, No. 2, 2001, pp. 593-607. doi:10.1016/S0896-6273(01)00301-4
[7]	M. Nikolova, N. Pondev, L. Christova, W. Wolf and A. R. Kossev, “Motor Cortex Excitability Changes Preceding Voluntary Muscle Activity in Simple Reaction Time Task,” European Journal of Applied Physiology, Vol. 98, No. 2, 2006, pp. 212-219. doi:10.1007/s00421-006-0265-y
[8]	C. D. MacKinnon and J. C. Rothwell, “Time-Varying Changes in Corticospinal Excitability Accompanying the Triphasic EMG Pattern in Humans,” The Journal of Physiology, Vol. 528, No. 3, 2000, pp. 633-645. doi:10.1111/j.1469-7793.2000.00633.x
[9]	E. Palmer, E. Cafarelli and P. Ashby, “The Processing of Human Ballistic Movements Explored by Stimulation Over the Cortex,” The Journal of Physiology, Vol. 481, No. 2, 1994, pp. 509-520.
[10]	R. Shadmehr and F. A. Mussa-Ivaldi, “Adaptive Representation of Dynamics during Learning of a Motor Task,” The Journal of Neuroscience, Vol. 14, No. 5, 1994, pp. 3208-3224.
[11]	T. Hunter, P. Sacco and D. L. Turner, “Corticospinal and EMG Correlates of Internal Model Formation during Force Field Motor Adaptation,” Society for Neuroscience Annual Meeting, 2008.
[12]	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
[13]	P. M. Rossini, A. T. Barker, A. Berardelli, M. D. Caramia, G. Caruso, R. R.Cracco and M. R. Dimitrijevic, “Non- Invasive Electrical and Magnetic Stimulation of the Brain, Spinal Cord and Roots: Basic Principles and Procedures for Routine Clinical Application. Report of an Ifcn Committee,” Electroencephalography and Clinical Neurophysiology, Vol. 91, No. 2, 1994, pp. 79-92. doi:10.1016/0013-4694(94)90029-9
[14]	A.R. Kossev, S. Siggelkow, R. Dengler and J. D. Rollnik, “Intracortical Inhibition and Facilitation in Paired-Pulse Transcranial Magnetic Stimulation: Effect of Conditioning Stimulus Intensity on Sizes and Latencies of Motor Evoked Potentials,” Journal of Clinical Neurophysiology, Vol. 20, No. 1, 2003, pp. 54-58. doi:10.1097/00004691-200302000-00007
[15]	R. Osu, E. Burdet, D. W. Franklin, T. E. Milner and M. Kawato, “Different Mechanisms Involved in Adaptation to Stable and Unstable Dynamics,” Journal of Neurophysiology, Vol. 90, No. 5, 2003, pp. 3255-3269. doi:10.1152/jn.00073.2003
[16]	S. McMillan, V. Nougier and W. D. Byblow, “Human Corticospinal Excitability during a Precued Reaction Time Paradigm,” Experimental Brain Research, Vol. 156, No. 1, 2004, pp. 80-87. doi:10.1007/s00221-003-1772-2
[17]	B. L. Day, J. C. Rothwell, P. D. Thompson, N. A. Maertens, K. Nakashima, K. Shannon and C. D. Marsden, “Delay in the Execution of Voluntary Movement by Electrical or Magnetic Brain Stimulation in Intact Man. Evidence for the Storage of Motor Programs in the Brain,” Brain, Vol. 112, No. 3, 1989, pp. 649-663. doi:10.1093/brain/112.3.649
[18]	R. Osu, D. W. Franklin, H. Kato, H. Gomi, K. Domen, T. Yoshioka and M. Kawato, “Short- and Long-Term Changes in Joint Co-Contraction Associated with Motor Learning as Revealed From Surface EMG,” Journal of Neurophysiology, Vol. 88, No. 2, 2002, pp. 991-1004.
[19]	D. W. Franklin, R. Osu, E. Burdet, M. Kawato and T. E. Milner, “Adaptation to Stable and Unstable Dynamics Achieved by Combined Impedance Control and Inverse Dynamics Model,” Journal of Neurophysiology, Vol. 90, No. 5, 2003, pp. 3270-3282. doi:10.1152/jn.01112.2002
[20]	C. Reynolds and P. Ashby, “Inhibition in the Human Motor Cortex Is Reduced Just before a Voluntary Contraction,” Neurology, Vol. 53, 1999, pp. 730-735.
[21]	W. Muellbacher, U. Ziemann, B. Boroojerdi, L. Cohen and M. Hallett, “Role of the Human Motor Cortex in Rapid Motor Learning,” Experimental Brain Research, Vol. 136, No. 4, 2001, pp. 431-438. doi:10.1007/s002210000614
[22]	C. L. Lim and C. Yiannikas, “Motor Evoked Potentials: A New Method of Controlled Facilitation Using Quantitative Surface EMG,” Electroencephalography and Clinical Neurophysiology, Vol. 85, No. 1, 1992, pp. 38-41. doi:10.1016/0168-5597(92)90099-W
[23]	C. G. Phillips and R. Porter, “The Pyramidal Projection to Motoneurones of Some Muscle Groups of the Baboon’s Forelimb,” Progress in Brain Research, Vol. 12, 1964, pp. 222-245. doi:10.1016/S0079-6123(08)60625-1
[24]	E. Palmer and P. Ashby, “Corticospinal Projections to Upper Limb Motoneurones in Humans,” The Journal of Physiology, Vol. 448, 1992, pp. 397-412.
[25]	J. C. Rothwell, P. D. Thompson, B. L. Day, S. Boyd and, C. D. Marsden, “Stimulation of the Human Motor Cortex through the Scalp,” Experimental Physiology, Vol. 76, No. 2, 1991, pp. 159-200.
[26]	J. Valls-Sole, A. Pascual-Leone, E. M. Wassermann and M. Hallett, “Human Motor Evoked Responses to Paired Transcranial Magnetic Stimuli,” Electroencephalography and Clinical Neurophysiology, Vol. 85, No. 6, 1992, pp. 355-364. doi:10.1016/0168-5597(92)90048-G
[27]	T. Kujirai, M. D. Caramia, J. C. Rothwell, B. L. Day, P. D. Thompson, A. Ferbert, S. Wroe, P. Asselman and C. D. Marsden, “Corticocortical Inhibition In Human Motor Cortex,” The Journal of Physiology, Vol. 471, No. 1, 1993, pp. 501-519.
[28]	V. Di Lazzaro, A. Oliviero, P. Profice, A. Insola, P. Mazzone, P. Tonali and J. C. Rothwell, “Direct Recordings of Descending Volleys after Transcranial Magnetic and Electric Motor Cortex Stimulation in Conscious Humans,” Electroencephalography and Clinical Neurophysiology, Supplement, Vol. 51, 1999, pp. 120-126.
[29]	M. C. Ridding, J. L. Taylor and J. C. Rothwell, “The Effect of Voluntary Contraction on Cortico-Cortical Inhibition In Human Motor Cortex,” The Journal of Physiology, Vol. 487, No. 2, 1995, pp. 541-548.
[30]	M. A. Perez, B. K. Lungholt, K. Nyborg and J. B. Nielsen, “Motor Skill Training Induces Changes in the Excitability of the Leg Cortical Area in Healthy Humans,” Experimental Brain Research, Vol. 159, No. 2, 2004, pp. 197-205. doi:10.1007/s00221-004-1947-5
[31]	A. Floyer-Lea, M. Wylezinska, T. Kincses and P. M. Matthews, “Rapid Modulation of GABA Concentration in Human Sensorimotor Cortex during Motor Learning,” Journal of Neurophysiology, Vol. 95, No. 3, 2006, pp. 1639-1644. doi:10.1152/jn.00346.2005
[32]	U. Ziemann, “Pharmacology of TMS,” Supplements to Clinical Neurophysiology, Vol. 56, 2003, pp. 226-231. doi:10.1016/S1567-424X(09)70226-0
[33]	J. Liepert, J. Classen, L. G. Cohen and M. Hallett, “Task- Dependent Changes of Intracortical Inhibition,” Experimental Brain Research, Vol. 118, No. 3, 1998, pp. 421- 426. doi:10.1007/s002210050296
[34]	Z. J. Daskalakis, B. K. Christensen, R. Chen, P. B. Fitzgerald, R. B. Zipursky and S. Kapur, “Evidence for Impaired Cortical Inhibition in Schizophrenia Using Transcranial Magnetic Stimulation,” Archives of General Psychiatry, Vol. 59, 2002, pp. 347-354. doi:10.1001/archpsyc.59.4.347
[35]	L. Roshan, G. O. Paradiso and R. Chen, “Two Phases of Short-Interval Intracortical Inhibition,” Experimental Brain Research, Vol. 151, No. 2, 2003, pp. 330-337. doi:10.1007/s00221-003-1502-9
[36]	F. Gandolfo, C. Li, B. J. Benda and C. P. Schioppa, E. Bizzi, “Cortical Correlates of Learning in Monkeys Adapting to a New Dynamical Environment,” Proceedings of the National Academy of Sciences of the U S A, Vol. 97, No. 5, 2000, pp. 2259-2263. doi:10.1073/pnas.040567097
[37]	T. Hunter, P. Sacco, M. A. Nitsche and D. L. Turner, “Modulation of Internal Model Formation during Force Field-Induced Motor Learning by Anodal Transcranial Direct Current Stimulation of Primary Motor Cortex,” The Journal of Physiology, Vol. 587, No. 12, 2009, pp. 2949-2961. doi:10.1113/jphysiol.2009.169284
[38]	A. Hadipour-Niktarash, C. K. Lee, J. E. Desmond and R. Shadmehr, “Impairment of Retention But Not Acquisition of a Visuomotor Skill Through Time-Dependent Disruption of Primary Motor Cortex,” The Journal of Neuroscience, Vol. 27, No. 49, 2007, pp. 13413-13419. doi:10.1523/JNEUROSCI.2570-07.2007
[39]	J. Xiao, C. Padoa-Schioppa and E. Bizzi, “Neuronal Correlates of Movement Dynamics in the Dorsal and Ventral Premotor Area in the Monkey,” Experimental Brain Research, Vol. 168, No. , 2006, pp. 106-119. doi:10.1007/s00221-005-0074-2
[40]	L. E. Sergio, C. Hamel-Paquet and J. F. Kalaska, “Motor Cortex Neural Correlates of Output Kinematics and Kinetics during Isometric-Force and Arm-Reaching Tasks,” Journal of Neurophysiology, Vol. 94, No. 4, 2005, pp. 2353-2378. doi:10.1152/jn.00989.2004
[41]	J. A. Rathelot and P. L. Strick, “Subdivisions of Primary Motor Cortex Based on Cortico-Motoneuronal Cells,” Proceedings of the National Academy of Sciences of the U S A, Vol. 106, No. 3, 2009, pp. 918-923. doi:10.1073/pnas.0808362106
[42]	Y. Yanai, N. Adamit, Z. Israel, R. Harel and Y. Prut, “Coordinate Transformation Is First Completed Downstream of Primary Motor Cortex,” The Journal of Neuroscien, Vol. 28, No. 7, 2008, pp. 1728-1732. doi:10.1523/JNEUROSCI.4662-07.2008