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Nausea as a complication of low-frequency repetitive transcranial magnetic stimulation of the posterior fossa
Clinical Neurophysiology 113 (2002) 1441–1443 www.elsevier.com/locate/clinph
Nausea as a complication of low-frequency repetitive transcranial magnetic stimulation of the posterior fossa Takeshi Satow a,b, Tatsuya Mima a, Hidemi Hara a, Tatsuhide Oga a,c, Akio Ikeda c, Nobuo Hashimoto a,b, Hiroshi Shibasaki a,c,* a
Department of Brain Pathophysiopathology, Human Brain Research Center, Kyoto University Graduate School of Medicine, 54 Kawahara-cho, Shogoin, Sakyo-ku, Kyoto 606-8507, Japan b Department of Neurosurgery, Kyoto University Graduate School of Medicine, 54 Kawahara-cho, Shogoin, Sakyo-ku, Kyoto 606-8507, Japan c Department of Neurology, Kyoto University Graduate School of Medicine, 54 Kawahara-cho, Shogoin, Sakyo-ku, Kyoto 606-8507, Japan Accepted 30 May 2002
Abstract Background: Transcranial magnetic stimulation (TMS) can non-invasively investigate the function of human brain. However, it can induce a focal pain at the stimulated site on the scalp or seizures when applied with high frequency (.1 Hz). Here we report an induction of nausea as a complication of low-frequency repetitive TMS (rTMS) of the cerebellum. Subjects and methods: Eight right-handed normal volunteers underwent low-frequency (0.9 Hz) rTMS of the right cerebellum. The stimulus intensity was set at 90% of the resting motor threshold determined by TMS to motor cortex. Results: Nausea lasted as long as 10 min after the end of rTMS without apparent neurological deficit in two subjects. This symptom was replicated when the same protocol was applied on a different day in the same subjects. Conclusions: Low-frequency rTMS of cerebellum is still a safe procedure, but the experimenters should keep in mind the possibility of inducing nausea. q 2002 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Repetitive transcranial magnetic stimulation; Low frequency; Cerebellum; Nausea; Complication
1. Introduction Transcranial magnetic stimulation (TMS) can induce an electric current in the brain, which enables the non-invasive investigation of cortical function in human. Although in clinical neurophysiology, a single pulse TMS has been conventionally used, recent advances in its therapeutic application exploited repetitive TMS (rTMS). While the rTMS with high frequency (.1 Hz) has been reported to be effective for treating depression (Klein et al., 1999), the low-frequency rTMS is potentially effective for writer’s cramp (Siebner et al., 1999), cerebellar ataxia in patients with spinocerebellar degeneration (SCD) (Shiga et al., 2002) and epilepsy (Tergau et al., 1999). The rTMS can modulate the neuronal excitability of the stimulated site beyond the period of stimulation, which makes it possible to investigate the function of the normal human brain. On the other hand, there are potential adverse effects of TMS ranging from discomfort of the stimulated scalp to the * Corresponding author. Tel.: 181-75-751-3601; fax: 181-75-751-3202. E-mail address: [email protected] (H. Shibasaki).
induction of seizures (Ho¨mberg and Netz; 1989; Hafnagel et al., 1990; Fauth et al., 1992; Classen et al., 1995), particularly when it is repetitively applied with high frequency (Dhuna et al., 1991; Pascual-Leone et al., 1993; Wassermann et al., 1996a). TMS of the posterior fossa has been used to study the role of cerebellum in motor control (Ugawa et al., 1995; Werhahn et al., 1996) or to treat the SCD patients (Shiga et al., 2002). However, the apparent adverse effects by possible cerebellar stimulation have never been reported. Here we report an induction of nausea after the application of low-frequency rTMS of posterior fossa in normal subjects, and call attention to a potential adverse effect of low-frequency rTMS of cerebellum.
2. Subjects and methods Eight right-handed normal volunteers (mean age ^ SD: 32.5 ^ 5.6 years, 6 males and two females) participated in the study applying low-frequency rTMS to the posterior fossa. All subjects gave a written informed consent accord-
1388-2457/02/$ - see front matter q 2002 Elsevier Science Ireland Ltd. All rights reserved. PII: S 1388-245 7(02)00187-6
CLINPH 2002062
1442
T. Satow et al. / Clinical Neurophysiology 113 (2002) 1441–1443
ing to the research protocol approved by the Committee of Medical Ethics, Graduate School of Medicine, Kyoto University (Clinical Research Protocol No. 267). A Magstim Super Rapid Magnetic Stimulator (Magstim Co., Whitland, Dyfed, UK), equipped with a 7 cm figureof-8 coil, was used to produce a focal stimulation of the brain through the skull. In order to prevent excessive heating of the coil, it was cooled by a specially designed aircooling device during rTMS. The coil was placed on the skin presumably overlying the right cerebellar hemisphere, 1 cm below and 3 cm right lateral to the inion (The´ oret et al., 2001). The coil handle was directed upwards and was parallel to the individual body midline, which could minimize the stimulus effect to the neck muscles. The resting motor threshold of the right first dorsal interosseous (FDI) muscle was determined as previously reported (Rossini et al., 1994). A train of rTMS consisted of 900 stimuli with the interstimulus interval of 1.1 s (stimulus frequency 0.9 Hz), which lasted approximately 15 min. The stimulus intensity was set at 90% of the resting motor threshold determined by TMS to motor cortex. Electromyograms (EMGs) were continuously monitored from the right FDI, extensor carpi radialis and biceps muscles throughout the experiment according to the proposed safety guidelines (Pascual-Leone et al., 1993 ,1994; Wassermann et al., 1996b, 1998).
3. Results Two out of 8 subjects complained of nausea during and after the rTMS. A 30-year-old male complained of nausea when approximately 400 stimuli were applied, and it lasted 10 min after the end of rTMS. Stimulus intensity was 78% of the maximum stimulator output. The nausea was relatively mild and he found it tolerable. Neurological examination during and after rTMS revealed no abnormalities including ocular movement and finger-to-nose test. No permanent deficits were observed. Approximately 1 month after the initial rTMS of the cerebellum, the same subject underwent the same protocol. The stimulus intensity was 76%. Again, he complained of nausea soon after the initiation of rTMS, which needed the reduction of stimulus intensity to 70%, resulting in the disappearance of the symptom. Neurologically, he was normal during and after rTMS. A 24-year-old female complained of nausea when approximately 200 stimuli were applied, and the symptom continued for 11 min after the end of rTMS. The stimulus intensity was 54%. Neurological examination demonstrated no abnormality. This subject also had the same experiment 1 month later, and developed mild but similar symptom. The stimulus intensity was 64%. On this occasion, nausea disappeared immediately after the end of rTMS without any neurological deficit. In the remaining 6 subjects, lowfrequency rTMS of cerebellum was well tolerated without any symptoms.
4. Discussion Transient nausea was seen in two out of 8 subjects (25%) of the present series, and this figure seems to be relatively high as a complication of rTMS with low frequency (0.9 Hz). Thus we should keep in mind the possibility of causing nausea in rTMS of the posterior fossa. Induction of nausea has never been reported as a complication of rTMS. The cerebellar rTMS has been applied to normal subjects (The´ oret et al., 2001) and SCD patients (Shiga et al., 2002), and none of those studies reported the induction of nausea. The´ oret et al. used 1 Hz rTMS for 5 min (the intensity: 90% motor threshold, which was the same as ours) with the figure-of-8 coil. Shiga et al. used the longer interstimulus interval (about 6 s) and the higher stimulus intensity (about 250% motor threshold) with the circular coil. The underlying mechanism of nausea induced by rTMS of the posterior fossa is uncertain. It is less likely that the magnetic pulses have activated the vestibulocerebellum (Voogt et al., 1996), because the subjects did not complain of vertigo. It is also possible that the stimulation can have an influence on the area postrema in the floor of the fourth ventricle directly or via propagation of currents through the cerebrospinal fluid (Miller and Leslie, 1994). Motion sickness due to repetitive neck movements is unlikely because neck movements were almost absent in those two subjects. Only one of 8 subjects had a painful sensation around the stimulated site, but the subject did not suffer from nausea by cerebellar rTMS. Thus, vaso-vagal reflex induced by pain at the posterior neck is unlikely. The possibility of psychological factors such as anxiety or fear cannot be completely excluded. In our institute, low-frequency rTMS has so far been applied to the primary sensorimotor area, premotor area and parietal cortex in a total of 13 normal subjects, including the present two subjects, on multiple occasions without any adverse effects. Hence, we can judge this complication as specific for the stimulation of the posterior fossa. Since it was not associated with seizures or any neurological sequelae, we believe that rTMS of the posterior fossa can be regarded as a safe protocol, if appropriately used.
Acknowledgements The authors thank Drs Kohara and Siebner for the helpful comments on this manuscript. This study was supported by Grants-in-Aid for Scientific Research on Priority area (C)Advanced Brain Science Project 12210012, (B2)-13470134, (C2)-13670460 from the Japan Ministry of Education, Culture, Sports, Science and Technology, Research for the Future Program from the Japan Society for the Promotion of Science JSPS-RFTF97L00201 and Grant-in-Aid for Encouragement of Young Scientists 13780634 from the Japan Society for the Promotion of Science.
T. Satow et al. / Clinical Neurophysiology 113 (2002) 1441–1443
References Classen J, Witte OW, Schlaug G, Seitz RJ, Holthausen H, Benecke R. Epileptic seizures triggered by focal transcranial magnetic stimulation. Electroenceph clin Neurophysiol 1995;94:19–25. Dhuna AK, Gates JR, Pascual-Leone A. Transcranial magnetic stimulation in patients with epilepsy. Neurology 1991;41:1067–1071. Fauth C, Meyer BU, Prosiegel M, Zihl J, Conrad B. Seizure induction and magnetic brain stimulation after stroke. Lancet 1992;339:362. Hafnagel MD, Elger CE, Durwen HF, Bo¨ ker DK, Entzian W. Activation of epileptic focus by transcranial magnetic stimulation. Ann Neurol 1990;27:49–60. Ho¨ mberg V, Netz J. Generalized seizure induced by transcranial magnetic stimulation of motor cortex. Lancet 1989;2:1223. Klein E, Kreinin I, Chistyakov A, Koren D, Mecz L, Marmur S, BenShachar D, Feinsod M. Therapeutic efficacy of right prefrontal slow repetitive transcranial magnetic stimulation in major depression: a double-blind controlled study. Arch Gen Psychiatry 1999;56:315– 320. Miller AD, Leslie RA. The area postrema and vomiting. Front Neuroendocrinol 1994;15:301–320. Pascual-Leone A, Houser CM, Reeves K, Shotland LI, Grafman J, Sato S, Valls-Sole´ J, Brasil-Neto JP, Wassermann EM, Cohen LG, Hallett M. Safety of rapid-rate transcranial magnetic stimulation in normal volunteers. Electroenceph clin Neurophysiol 1993;89:120–130. Pascual-Leone A, Valls-Sole´ J, Wassermann EM, Hallett M. Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain 1994;117:847–858. Rossini PM, Barker AT, Beradelli A, Caramia MD, Caruso G, Cracco RQ, Dimitrijevic´ MR, Hallett M, Katayama Y, Lu¨ cking CH, Maertens de Noordhout AL, Marsden CD, Murray NMF, Rothwell JC, Swash M, Tomberg C. Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine
1443
clinical application. Report of an IFCN committee. Electroenceph clin Neurophysiol 1994;91:79–92. Shiga Y, Tsuda T, Itoyama Y, Shimizu H, Miyazawa KI, Jin K, Yamazaki T. Transcranial magnetic stimulation alleviates truncal ataxia in spinocerebellar degeneration. J Neurol Neurosurg Psychiatry 2002;72:124– 126. Siebner HR, Tormos JM, Ceballos-Baumann AO, Auer C, Catala MD, Conrad B, Pascual-Leone A. Low-frequency repetitive transcranial magnetic stimulation of the motor cortex in writer’s cramp. Neurology 1999;52:529–537. Tergau F, Naumann U, Paulus W, Steinhoff BJ. Low-frequency repetitive transcranial magnetic stimulation improves intractable epilepsy. Lancet 1999;353:2209. The´ oret H, Haque J, Pascual-Leone A. Increased variability of paced finger tapping accuracy following repetitive magnetic stimulation of the cerebellum in humans. Neurosci Lett 2001;306:29–32. Ugawa Y, Uesaka Y, Terao Y, Hanajima R, Kanazawa I. Magnetic stimulation over the cerebellum in humans. Ann Neurol 1995;37:703–713. Voogt J, Gerrits NM, Ruigrok T. Organization of the vestibulocerebellum. Ann N Y Acad Sci 1996;781:553–579. Wassermann EM, Cohen LG, Flitman SS, Chen R, Hallett M. Seizures in healthy people with repeated ‘safe’ transcranial magnetic stimuli. Lancet 1996a;347:825–826. Wassermann EM, Grafman J, Berry C, Hollnagel C, Wild K, Clark K, Hallett M. Use and safety of a new transcranial magnetic stimulator. Electroenceph clin Neurophysiol 1996b;101:412–417. Wassermann EM. Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5– 7, 1996. Electroenceph clin Neurophysiol 1998;108:1–16. Werhahn KJ, Taylor J, Ridding M, Meyer BU, Rothwell JC. Effect of transcranial magnetic stimulation over the cerebellum on the excitability of human motor cortex. Electroenceph clin Neurophysiol 1996;101:58–66.
Nausea as a complication of low-frequency repetitive transcranial magnetic stimulation of the posterior fossa Takeshi Satow a,b, Tatsuya Mima a, Hidemi Hara a, Tatsuhide Oga a,c, Akio Ikeda c, Nobuo Hashimoto a,b, Hiroshi Shibasaki a,c,* a
Department of Brain Pathophysiopathology, Human Brain Research Center, Kyoto University Graduate School of Medicine, 54 Kawahara-cho, Shogoin, Sakyo-ku, Kyoto 606-8507, Japan b Department of Neurosurgery, Kyoto University Graduate School of Medicine, 54 Kawahara-cho, Shogoin, Sakyo-ku, Kyoto 606-8507, Japan c Department of Neurology, Kyoto University Graduate School of Medicine, 54 Kawahara-cho, Shogoin, Sakyo-ku, Kyoto 606-8507, Japan Accepted 30 May 2002
Abstract Background: Transcranial magnetic stimulation (TMS) can non-invasively investigate the function of human brain. However, it can induce a focal pain at the stimulated site on the scalp or seizures when applied with high frequency (.1 Hz). Here we report an induction of nausea as a complication of low-frequency repetitive TMS (rTMS) of the cerebellum. Subjects and methods: Eight right-handed normal volunteers underwent low-frequency (0.9 Hz) rTMS of the right cerebellum. The stimulus intensity was set at 90% of the resting motor threshold determined by TMS to motor cortex. Results: Nausea lasted as long as 10 min after the end of rTMS without apparent neurological deficit in two subjects. This symptom was replicated when the same protocol was applied on a different day in the same subjects. Conclusions: Low-frequency rTMS of cerebellum is still a safe procedure, but the experimenters should keep in mind the possibility of inducing nausea. q 2002 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Repetitive transcranial magnetic stimulation; Low frequency; Cerebellum; Nausea; Complication
1. Introduction Transcranial magnetic stimulation (TMS) can induce an electric current in the brain, which enables the non-invasive investigation of cortical function in human. Although in clinical neurophysiology, a single pulse TMS has been conventionally used, recent advances in its therapeutic application exploited repetitive TMS (rTMS). While the rTMS with high frequency (.1 Hz) has been reported to be effective for treating depression (Klein et al., 1999), the low-frequency rTMS is potentially effective for writer’s cramp (Siebner et al., 1999), cerebellar ataxia in patients with spinocerebellar degeneration (SCD) (Shiga et al., 2002) and epilepsy (Tergau et al., 1999). The rTMS can modulate the neuronal excitability of the stimulated site beyond the period of stimulation, which makes it possible to investigate the function of the normal human brain. On the other hand, there are potential adverse effects of TMS ranging from discomfort of the stimulated scalp to the * Corresponding author. Tel.: 181-75-751-3601; fax: 181-75-751-3202. E-mail address: [email protected] (H. Shibasaki).
induction of seizures (Ho¨mberg and Netz; 1989; Hafnagel et al., 1990; Fauth et al., 1992; Classen et al., 1995), particularly when it is repetitively applied with high frequency (Dhuna et al., 1991; Pascual-Leone et al., 1993; Wassermann et al., 1996a). TMS of the posterior fossa has been used to study the role of cerebellum in motor control (Ugawa et al., 1995; Werhahn et al., 1996) or to treat the SCD patients (Shiga et al., 2002). However, the apparent adverse effects by possible cerebellar stimulation have never been reported. Here we report an induction of nausea after the application of low-frequency rTMS of posterior fossa in normal subjects, and call attention to a potential adverse effect of low-frequency rTMS of cerebellum.
2. Subjects and methods Eight right-handed normal volunteers (mean age ^ SD: 32.5 ^ 5.6 years, 6 males and two females) participated in the study applying low-frequency rTMS to the posterior fossa. All subjects gave a written informed consent accord-
1388-2457/02/$ - see front matter q 2002 Elsevier Science Ireland Ltd. All rights reserved. PII: S 1388-245 7(02)00187-6
CLINPH 2002062
1442
T. Satow et al. / Clinical Neurophysiology 113 (2002) 1441–1443
ing to the research protocol approved by the Committee of Medical Ethics, Graduate School of Medicine, Kyoto University (Clinical Research Protocol No. 267). A Magstim Super Rapid Magnetic Stimulator (Magstim Co., Whitland, Dyfed, UK), equipped with a 7 cm figureof-8 coil, was used to produce a focal stimulation of the brain through the skull. In order to prevent excessive heating of the coil, it was cooled by a specially designed aircooling device during rTMS. The coil was placed on the skin presumably overlying the right cerebellar hemisphere, 1 cm below and 3 cm right lateral to the inion (The´ oret et al., 2001). The coil handle was directed upwards and was parallel to the individual body midline, which could minimize the stimulus effect to the neck muscles. The resting motor threshold of the right first dorsal interosseous (FDI) muscle was determined as previously reported (Rossini et al., 1994). A train of rTMS consisted of 900 stimuli with the interstimulus interval of 1.1 s (stimulus frequency 0.9 Hz), which lasted approximately 15 min. The stimulus intensity was set at 90% of the resting motor threshold determined by TMS to motor cortex. Electromyograms (EMGs) were continuously monitored from the right FDI, extensor carpi radialis and biceps muscles throughout the experiment according to the proposed safety guidelines (Pascual-Leone et al., 1993 ,1994; Wassermann et al., 1996b, 1998).
3. Results Two out of 8 subjects complained of nausea during and after the rTMS. A 30-year-old male complained of nausea when approximately 400 stimuli were applied, and it lasted 10 min after the end of rTMS. Stimulus intensity was 78% of the maximum stimulator output. The nausea was relatively mild and he found it tolerable. Neurological examination during and after rTMS revealed no abnormalities including ocular movement and finger-to-nose test. No permanent deficits were observed. Approximately 1 month after the initial rTMS of the cerebellum, the same subject underwent the same protocol. The stimulus intensity was 76%. Again, he complained of nausea soon after the initiation of rTMS, which needed the reduction of stimulus intensity to 70%, resulting in the disappearance of the symptom. Neurologically, he was normal during and after rTMS. A 24-year-old female complained of nausea when approximately 200 stimuli were applied, and the symptom continued for 11 min after the end of rTMS. The stimulus intensity was 54%. Neurological examination demonstrated no abnormality. This subject also had the same experiment 1 month later, and developed mild but similar symptom. The stimulus intensity was 64%. On this occasion, nausea disappeared immediately after the end of rTMS without any neurological deficit. In the remaining 6 subjects, lowfrequency rTMS of cerebellum was well tolerated without any symptoms.
4. Discussion Transient nausea was seen in two out of 8 subjects (25%) of the present series, and this figure seems to be relatively high as a complication of rTMS with low frequency (0.9 Hz). Thus we should keep in mind the possibility of causing nausea in rTMS of the posterior fossa. Induction of nausea has never been reported as a complication of rTMS. The cerebellar rTMS has been applied to normal subjects (The´ oret et al., 2001) and SCD patients (Shiga et al., 2002), and none of those studies reported the induction of nausea. The´ oret et al. used 1 Hz rTMS for 5 min (the intensity: 90% motor threshold, which was the same as ours) with the figure-of-8 coil. Shiga et al. used the longer interstimulus interval (about 6 s) and the higher stimulus intensity (about 250% motor threshold) with the circular coil. The underlying mechanism of nausea induced by rTMS of the posterior fossa is uncertain. It is less likely that the magnetic pulses have activated the vestibulocerebellum (Voogt et al., 1996), because the subjects did not complain of vertigo. It is also possible that the stimulation can have an influence on the area postrema in the floor of the fourth ventricle directly or via propagation of currents through the cerebrospinal fluid (Miller and Leslie, 1994). Motion sickness due to repetitive neck movements is unlikely because neck movements were almost absent in those two subjects. Only one of 8 subjects had a painful sensation around the stimulated site, but the subject did not suffer from nausea by cerebellar rTMS. Thus, vaso-vagal reflex induced by pain at the posterior neck is unlikely. The possibility of psychological factors such as anxiety or fear cannot be completely excluded. In our institute, low-frequency rTMS has so far been applied to the primary sensorimotor area, premotor area and parietal cortex in a total of 13 normal subjects, including the present two subjects, on multiple occasions without any adverse effects. Hence, we can judge this complication as specific for the stimulation of the posterior fossa. Since it was not associated with seizures or any neurological sequelae, we believe that rTMS of the posterior fossa can be regarded as a safe protocol, if appropriately used.
Acknowledgements The authors thank Drs Kohara and Siebner for the helpful comments on this manuscript. This study was supported by Grants-in-Aid for Scientific Research on Priority area (C)Advanced Brain Science Project 12210012, (B2)-13470134, (C2)-13670460 from the Japan Ministry of Education, Culture, Sports, Science and Technology, Research for the Future Program from the Japan Society for the Promotion of Science JSPS-RFTF97L00201 and Grant-in-Aid for Encouragement of Young Scientists 13780634 from the Japan Society for the Promotion of Science.
T. Satow et al. / Clinical Neurophysiology 113 (2002) 1441–1443
References Classen J, Witte OW, Schlaug G, Seitz RJ, Holthausen H, Benecke R. Epileptic seizures triggered by focal transcranial magnetic stimulation. Electroenceph clin Neurophysiol 1995;94:19–25. Dhuna AK, Gates JR, Pascual-Leone A. Transcranial magnetic stimulation in patients with epilepsy. Neurology 1991;41:1067–1071. Fauth C, Meyer BU, Prosiegel M, Zihl J, Conrad B. Seizure induction and magnetic brain stimulation after stroke. Lancet 1992;339:362. Hafnagel MD, Elger CE, Durwen HF, Bo¨ ker DK, Entzian W. Activation of epileptic focus by transcranial magnetic stimulation. Ann Neurol 1990;27:49–60. Ho¨ mberg V, Netz J. Generalized seizure induced by transcranial magnetic stimulation of motor cortex. Lancet 1989;2:1223. Klein E, Kreinin I, Chistyakov A, Koren D, Mecz L, Marmur S, BenShachar D, Feinsod M. Therapeutic efficacy of right prefrontal slow repetitive transcranial magnetic stimulation in major depression: a double-blind controlled study. Arch Gen Psychiatry 1999;56:315– 320. Miller AD, Leslie RA. The area postrema and vomiting. Front Neuroendocrinol 1994;15:301–320. Pascual-Leone A, Houser CM, Reeves K, Shotland LI, Grafman J, Sato S, Valls-Sole´ J, Brasil-Neto JP, Wassermann EM, Cohen LG, Hallett M. Safety of rapid-rate transcranial magnetic stimulation in normal volunteers. Electroenceph clin Neurophysiol 1993;89:120–130. Pascual-Leone A, Valls-Sole´ J, Wassermann EM, Hallett M. Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain 1994;117:847–858. Rossini PM, Barker AT, Beradelli A, Caramia MD, Caruso G, Cracco RQ, Dimitrijevic´ MR, Hallett M, Katayama Y, Lu¨ cking CH, Maertens de Noordhout AL, Marsden CD, Murray NMF, Rothwell JC, Swash M, Tomberg C. Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine
1443
clinical application. Report of an IFCN committee. Electroenceph clin Neurophysiol 1994;91:79–92. Shiga Y, Tsuda T, Itoyama Y, Shimizu H, Miyazawa KI, Jin K, Yamazaki T. Transcranial magnetic stimulation alleviates truncal ataxia in spinocerebellar degeneration. J Neurol Neurosurg Psychiatry 2002;72:124– 126. Siebner HR, Tormos JM, Ceballos-Baumann AO, Auer C, Catala MD, Conrad B, Pascual-Leone A. Low-frequency repetitive transcranial magnetic stimulation of the motor cortex in writer’s cramp. Neurology 1999;52:529–537. Tergau F, Naumann U, Paulus W, Steinhoff BJ. Low-frequency repetitive transcranial magnetic stimulation improves intractable epilepsy. Lancet 1999;353:2209. The´ oret H, Haque J, Pascual-Leone A. Increased variability of paced finger tapping accuracy following repetitive magnetic stimulation of the cerebellum in humans. Neurosci Lett 2001;306:29–32. Ugawa Y, Uesaka Y, Terao Y, Hanajima R, Kanazawa I. Magnetic stimulation over the cerebellum in humans. Ann Neurol 1995;37:703–713. Voogt J, Gerrits NM, Ruigrok T. Organization of the vestibulocerebellum. Ann N Y Acad Sci 1996;781:553–579. Wassermann EM, Cohen LG, Flitman SS, Chen R, Hallett M. Seizures in healthy people with repeated ‘safe’ transcranial magnetic stimuli. Lancet 1996a;347:825–826. Wassermann EM, Grafman J, Berry C, Hollnagel C, Wild K, Clark K, Hallett M. Use and safety of a new transcranial magnetic stimulator. Electroenceph clin Neurophysiol 1996b;101:412–417. Wassermann EM. Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5– 7, 1996. Electroenceph clin Neurophysiol 1998;108:1–16. Werhahn KJ, Taylor J, Ridding M, Meyer BU, Rothwell JC. Effect of transcranial magnetic stimulation over the cerebellum on the excitability of human motor cortex. Electroenceph clin Neurophysiol 1996;101:58–66.