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Repetitive TMS of the Motor Cortex Improves Ipsilateral Sequential Simple Finger Movements

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Repetitive TMS of the Motor Cortex Improves Ipsilateral Sequential Simple Finger Movements Repetitive TMS of the motor cortex improves ipsilateral sequential simple finger movements M. Kobayashi, MD, PhD; S. Hutchinson, MD; H. Théoret, PhD; G. Schlaug, MD, PhD; and A. Pascual-Leone, MD, PhD Abstract—Background: Disruption of cortical function can improve behavior. Motor cortex (M1) transcallosal interactions are mainly inhibitory; after unilateral damage to M1, there is increased excitability of the unaffected M1. Repetitive transcranial magnetic stimulation (rTMS) of M1 produces a temporary reduction in cortical excitability in the same M1 that outlasts the duration of the rTMS train. The authors hypothesize that reducing cortical excitability of M1 by rTMS may improve motor performance in the ipsilateral hand by releasing the contralateral M1 from transcallosal inhibition. Methods: Sixteen healthy volunteers participated. Using a sequential key-pressing task with the index finger, motor performance was monitored before and after rTMS (1 Hz for 10 minutes with the intensity below motor threshold) applied to the ipsilateral M1, contralateral M1, ipsilateral premotor area, or vertex (Cz). Results: rTMS of M1 shortened execution time of the motor task with the ipsilateral hand without affecting performance with the contralateral hand. This effect outlasted rTMS by at least 10 minutes, was specific for M1 stimulation, and was associated with increased intracortical excitability in the unstimulated M1. Conclusions: The authors’ results support the concept of an interhemispheric “rivalry.” They demonstrate the utility of repetitive transcranial magnetic stimulation to explore the functional facilitation of the unstimulated counterpart motor cortex, presumably via suppression of activity in the stimulated motor cortex and transcallosal inhibition. NEUROLOGY 2004;62:91–98 The two cerebral hemispheres are functionally cou- tical inhibition is suppressed in the unaffected motor pled and balanced.1-3 Unilateral dysfunction disrupts cortex of patients who have had a cortical stroke, this balance and leads to the release of the unaf- and such suppression is associated with, and pre- fected hemisphere, which can result in a paradoxical sumably the result of, disrupted transcallosal inhibi- functional improvement.4,5 This phenomenon has tion.11 The interhemispheric interaction between been documented in the setting of hemispatial atten- primary motor areas (M1) is strong and effective,12 tion. For example, in normal subjects, suppression of although commissural fibers are relatively sparse.13 one parietal cortex by repetitive transcranial mag- Inhibitory and facilitatory interactions are postu- netic stimulation (rTMS) improves attention to tar- lated, but when TMS is applied to the hand motor gets in the ipsilateral visual field.3 In patients who area, the interaction appears to be mostly inhibitory have had a stroke, a subsequent disruption of the in humans.14-16 healthy hemisphere by another stroke6 or rTMS7 Low-frequency (1 Hz) rTMS of the motor cortex may lead to an improvement of attention. can suppress cortical excitability for seconds to min- Studies on stroke patients have also suggested the utes (depending on the duration of the stimulation) presence of such interhemispheric “rivalry” between and produce a transient virtual lesion in the targeted bihemispheric motor areas. Patients who have had cortical region, leading to measurable physiologic strokes involving the motor cortex have increased and behavioral effects.17-22 rTMS of motor cortex can cortical excitability and enlarged cortical motor out- also change the metabolic rate in the contralateral put maps in the unaffected motor cortex.8-11 Intracor- motor area and therefore may lead to behavioral or functional effects ipsilateral to the side of Additional material related to this article can be found on the Neurology stimulation.23-25 In the present study, we hypothe- Web site. Go to www.neurology.org and scroll down the Table of Con- tents for the January 13 issue to find the title link for this article. sized that suppression of the hand representation in one M1 by low-frequency rTMS would lead to a tran- From the Laboratory for Magnetic Brain Stimulation (Drs. Kobayashi, Hutchinson, Théoret, and Pascual-Leone) and Neuroimaging Laboratory (Drs. Hutchinson and Schlaug), Department of Neurology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA. This work was conducted at the Harvard-Thorndike General Clinical Research Center, supported by the National Center for Research Resources (MO1 RR01032). Support was also received from the NIH (RO1MH57980, RO1MH60734, RO1EY12091) and the Goldberg Foundation (A.P.L.); the Dana Foundation, Lawrence J. and Anne Rubenstein Foundation, and Doris Duke Charitable Foundation (G.S.); and the Uehara Memorial Foundation (M.K.). Dr. Hutchinson received support from the Clinical Investigator Training Program at Beth Israel Deaconess Medical Center and Harvard Medical School. Received February 20, 2003. Accepted in final form September 19, 2003. Address correspondence and reprint requests to Dr. Alvaro Pascual-Leone, Laboratory for Magnetic Brain Stimulation, Department of Neurology, Beth Israel Deaconess Medical Center, Harvard Medical School, 330 Brookline Avenue, KS452, Boston, MA 02215; e-mail: [email protected] Copyright © 2004 by AAN Enterprises, Inc. 91 scallosal disinhibition of the unstimulated motor cor- was defined as being 2.5 cm anterior to the optimal position tex and so to a facilitation of movements with the for FDI according to recent functional imaging studies.31 These positions were confirmed in four subjects by an image-guided fra- ipsilateral hand. A recent study in adult rats that meless stereotaxy system (Brainsight, Rogue Research, Montreal, demonstrated facilitation in motor skill learning Canada) to localize the sites of TMS of the hand motor area with the ipsilateral, unaffected forelimb after unilat- and the dorsolateral premotor cortex. The coil was held tangen- tially to the skull with the handle pointing 45° posterolaterally for eral sensorimotor cortex lesions appears to support stimulation of the M1 and premotor cortex or pointing posteriorly 26 this hypothesis. for Cz. Paired-pulse TMS. Paired-pulse TMS consisted of a condi- Subjects and methods. Subjects. Sixteen healthy volunteers tioning stimulus with an intensity of 80% MT and a test stimulus (12 men and 4 women; aged 25 to 35 years; mean age, 29.6 Ϯ 3.6 with approximately 120% MT that was adjusted to reproducibly years) were recruited. No subject had any psychiatric or major evoke MEPs of peak-to-peak amplitude of approximately 0.5 mV. medical history or any contraindications to TMS.27 All subjects The short (1, 2, and 3 ms) and long (9, 12, and 15 ms) interstimu- were strongly right-handed according to the 12-item Annett ques- lus intervals (ISIs) between conditioning and test stimulus were tionnaire.28 The study was approved by the local Institutional used to assess intracortical inhibition and facilitation.32 Ten MEPs Review Board, and all participants gave their written informed were recorded at each ISI and at conditioning and test stimulus consent. alone. The order of the trials was pseudorandomly varied using Motor task and behavioral measure. The motor task consisted the CED PC interface (Cambridge Electronic Device, Cam- of the serial rapid pressing of four horizontally arranged keys in a bridge, UK). given order sequence (figure 1A). The subjects were instructed to Experiment 1. The rTMS effects of ipsilateral and contralat- repeat the sequence 12 times as quickly and precisely as possible eral M1 on hand motor performance were tested in 12 subjects. using their right or left index finger while accuracy and execution rTMS was applied over one of three different scalp locations: ipsi- times were measured. The motor task was repeated five times lateral M1, contralateral M1, and Cz as a control site (see figure with a short pause of 30 seconds between the tasks to minimize 1A). On the first day of the experiment, subjects practiced exten- subjects’ fatigue (240 pressings in one block). Each block of the sively with the right or left hand until their motor performance motor task took approximately 5 minutes to complete. The thumb reached a plateau. On the following 3 days, each subject received and ring finger of the same hand were placed and fixed beside the a single, continuous train of 600 pulses of 1-Hz rTMS, and their number pad to prompt subjects to use only hand muscles, mini- motor performance was monitored before, immediately, and 10 mizing movements of the forearm and proximal arm. The height minutes after rTMS (figure 1B). The three rTMS sites were tested of the chair and keyboard were adjusted for subject comfort and on three separate days to avoid a carry-over effect of the preceding kept constant during all experiments. In each experiment, the rTMS. The order of the targeted sites of rTMS application was subject’s motor performance was recorded with a personal com- counterbalanced across subjects. After all three rTMS sessions for puter using SuperLab software (Cedrus Corp., Phoenix, AZ). The one hand were completed, the experiments for the other hand mean execution time, the interval between every two sequential were performed. Subjects learned the motor task with the other key presses, and error rate (pressing an incorrect key) were calcu- hand on the first day, and the rTMS sessions of the three sites lated for each block. were conducted on the subsequent 3 days. Half of 12 subjects The subjects practiced the motor task for more than 30 min- underwent the studies first for their right hand; the other 6 were utes on the day before each experiment so that all of them could studied first with the left hand. perform the task fluently with few mistakes. Their performance Experiment 2. In the second experiment, we examined the reached plateau after approximately 20 minutes (figure 1C). In duration of the effect of rTMS over the ipsilateral M1 on hand addition, before each experiment, the subjects performed 3 motor behavior in seven subjects, including six subjects from Ex- warm-up blocks, 720 key presses, with 3-minute rests between periment 1.
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