Timing of motor cortical stimulation during planar robotic training differentially impacts neuroplasticity in older adults

Clinical Neurophysiology

Volumn 126, Issue 5, 2015, Pages 1024-1032

  Massie, Crystal L ^a,d   Kantak, Shailesh S ^a,b   Narayanan, Priya ^a   Wittenberg, George F ^a,c  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b MOSS REHABILITATION RESEARCH INSTITUTE   (United States)

^c BALTIMORE VA MEDICAL CENTER   (United States)

^d INDIANA UNIVERSITY   (United States)

Author keywords

Aging; Motor control; Neuroplasticity; Reaching; Rehabilitation; Transcranial magnetic stimulation

Indexed keywords

ADULT; AGED; AGING; ARTICLE; CEREBROVASCULAR ACCIDENT; CLINICAL ARTICLE; ELECTROMYOGRAM; EVOKED MUSCLE RESPONSE; EXTENSOR MUSCLE; FEMALE; FLEXOR MUSCLE; HUMAN; MALE; MOTOR CORTEX; MOTOR PERFORMANCE; MUSCLE CONTRACTION; NERVE CELL PLASTICITY; PRIORITY JOURNAL; REHABILITATION CARE; RESPONSE TIME; ROBOTIC EXOSKELETON; ROBOTICS; TIME; TRAINING; TRANSCRANIAL MAGNETIC STIMULATION; AGE; MOTOR EVOKED POTENTIAL; MOVEMENT (PHYSIOLOGY); PHYSIOLOGY; REACTION TIME; SKELETAL MUSCLE;

ADULT; AGE FACTORS; AGED; EVOKED POTENTIALS, MOTOR; FEMALE; HUMANS; MALE; MOTOR CORTEX; MOTOR SKILLS; MOVEMENT; MUSCLE, SKELETAL; NEURONAL PLASTICITY; REACTION TIME; ROBOTICS; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84926050326     PISSN: 13882457     EISSN: 18728952     Source Type: Journal    
DOI: 10.1016/j.clinph.2014.06.053     Document Type: Article

References (34)

1. Bütefisch C., Heger R., Schicks W., Seitz R., Netz J. Hebbian-type stimulation during robot-assisted training in patients with stroke. Neurorehabil Neural Repair 2011, 25:645-655.
2. Bütefisch C.M., Khurana V., Kopylev L., Cohen L.G. Enhancing encoding of a motor memory in the primary motor cortex by cortical stimulation. J Neurophysiol 2004, 91:2110-2116.
3. Chen R., Udupa K. Measurement and modulation of plasticity of the motor system in humans using transcranial magnetic stimulation. Motor Control 2009, 13:442-453.
4. Chen R., Yaseen Z., Cohen L.G., Hallett M. Time course of corticospinal excitability in reaction time and self-paced movements. Ann Neurol 1998, 44:317-325.
5. Churchland M.M., Cunningham J.P., Kaufman M.T., Ryu S.I., Shenoy K.V. Cortical preparatory activity: representation of movement or first cog in a dynamical machine?. Neuron 2010, 68:387-400.
6. Churchland M.M., Santhanam G., Shenoy K.V. Preparatory activity in premotor and motor cortex reflects the speed of the upcoming reach. J Neurophysiol 2006, 96:3130-3146.
7. Churchland M.M., Shenoy K.V. Delay of movement caused by disruption of cortical preparatory activity. J Neurophysiol 2007, 97:348-359.
8. Classen J., Liepert J., Wise S.P., Hallett M., Cohen L.G. Rapid plasticity of human cortical movement representation induced by practice. J Neurophysiol 1998, 79:1117-1123.
9. Cohen L.G., Ziemann U., Chen R., Classen J., Hallett M., Gerloff C., et al. Studies of neuroplasticity with transcranial magnetic stimulation. J Clin Neurophysiol 1998, 15:305-324.
10. Conroy S.S., Whitall J., Dipietro L., Jones-Lush L.M., Zhan M., Finley M.A., et al. Effect of gravity on robot-assisted motor training after chronic stroke: a randomized trial. Arch Phys Med Rehabil 2011, 92:1754-1761.
11. Gharabaghi A., Kraus D., Leao M.T., Spuler M., Walter A., Bogdan M., et al. Coupling brain-machine interfaces with cortical stimulation for brain-state dependent stimulation: enhancing motor cortex excitability for neurorehabilitation. Front Hum Neurosci 2014, 8:1-7.
12. Giacobbe V., Volpe B.T., Thickbroom G.W., Fregni F., Pascual-Leone A., Krebs H.I., et al. Reversal of TMS-induced motor twitch by training is associated with a reduction in excitability of the antagonist muscle. J Neuroeng Rehabil 2011, 8:1-8.
13. Gilio F., Iacovelli E., Conte A., Frasca V., Gabriele M., Giacomelli E., et al. Asymmetric responses to repetitive transcranial magnetic stimulation (rTMS) over the left and right primary motor cortex in a patient with lateralized progressive limb-kinetic apraxia. Neurosci Lett 2008, 437:125-129.
14. Jones-Lush L.M., Judkins T.N., Wittenberg G.F. Arm movement maps evoked by cortical magnetic stimulation in a robotic environment. Neuroscience 2010, 165:774-781.
15. Kantak S.S., Jones-Lush L.M., Narayanan P., Judkins T.N., Wittenberg G.F. Rapid plasticity of motor corticospinal system with robotic reach training. Neuroscience 2013, 5:55-64.
16. Karst G.M., Hasan Z. Timing and magnitude of electromyographic activity for two-joint arm movements in different directions. J Neurophysiol 1991, 66:1594-1604.
17. Kluger B.M., Triggs W.J. Use of transcranial magnetic stimulation to influence behavior. Curr Neurol Neurosci Rep 2007, 7:491-497.
18. Koganemaru S., Mima T., Thabit M.N., Ikkaku T., Shimada K., Kanematsu M., et al. Recovery of upper-limb function due to enhanced use-dependent plasticity in chronic stroke patients. Brain 2010, 133:3373-3384.
19. Krebs H.I., Hogan N., Aisen M.L., Volpe B.T. Robot-aided neurorehabilitation. IEEE Trans Rehabil Eng 1998, 6:75-87.
20. Krutky M.A., Perreault E.J. Motor cortical measures of use-dependent plasticity are graded from distal to proximal in the human upper limb. J Neurophysiol 2007, 98:3230-3241.
21. Kuo M.F., Unger M., Liebetanz D., Lang N., Tergau F., Paulus W., et al. Limited impact of homeostatic plasticity on motor learning in humans. Neuropsychologia 2008, 46:2122-2128.
22. Lewis G.N., Vandal A.C., McNair P.J. A method to monitor upper limb movement direction encoding in the corticomotor pathway. J Mot Behav 2012, 44:223-232.
23. Lo A.C., Guarino P.D., Richards L.G., Haselkorn J.K., Wittenberg G.F., Federman D.G., et al. Robot-assisted therapy for long-term upper-limb impairment after stroke. N Engl J Med 2010, 362:1772-1783.
24. MacClellan L.R., Bradham D.D., Whitall J., Volpe B., Wilson P.D., Ohlhoff J., et al. Robotic upper-limb neurorehabilitation in chronic stroke patients. J Rehabil Res Dev 2005, 42:717-722.
25. Massie C.L., Tracy B.L., Malcolm M.P. Functional repetitive transcranial magnetic stimulation increases motor cortex excitability in survivors of stroke. Clin Neurophysiol 2013, 124:371-378.
26. Massie C.L., Narayanan P., Kantak S.S., Jones-Lush L.M., Judkins T.N., Wittenberg G.F. Effects of motor cortical stimulation during planar reaching movement. J Rehabil Robotics 2013, 1:42-53.
27. Rogasch N.C., Dartnall T.J., Cirillo J., Nordstrom M.A., Semmler J.G. Corticomotor plasticity and learning of a ballistic thumb training task are diminished in older adults. J Appl Physiol 2009, 107:1874-1883.
28. Stefan K., Kunesch E., Cohen L.G., Benecke R., Classen J. Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 2000, 123:572-584.
29. Stein J., Krebs H.I., Frontera W.R., Fasoli S.E., Hughes R., Hogan N. Comparison of two techniques of robot-aided upper limb exercise training after stroke. Am J Phys Med Rehabil 2004, 83:720-728.
30. Taylor J.L., Martin P.G. Voluntary motor output Is altered by spike-timing-dependent changes in the human corticospinal pathway. J Neurosci 2009, 29:11708-11716.
31. Thabit M.N., Ueki Y., Koganemaru S., Fawi G., Fukuyama H., Mima T. Movement-related cortical stimulation can induce human motor plasticity. J Neurosci 2010, 30:11529-11536.
32. Vandenberghe A., Levin O., De Schutter J., Swinnen S., Jonkers I. Three-dimensional reaching tasks effect of reaching height and width on upper limb kinematics and muscle activity. Gait Posture 2010, 32:500-507.
33. Wu H.G., Miyamoto Y.R., Gonzalez Castro L.N., Ölveczky B.P., Smith M.A. Temporal structure of motor variability is dynamically regulated and predicts motor learning ability. Nat Neurosci 2014, 17:312-321.
34. Ziemann U., Iliac T.V., Pauli C., Meintzschel F., Ruge D. Learning modifies subsequent induction of long-term potentiation-like and long-term depression-like plasticity in human motor cortex. J Neurosci 2004, 24:1666-1672.