MEP (%)
Chapter 5 Conclusions
Chapter 5
cortico-not been observed after cTBS-on-Sl. Lack of changes after cTBS-on-Sl demon strates that cTBS is a focal brain stimulation technique with a spatial sensitivity of at least two centimeters. Since no significant change on cortico-muscular coherence has been observed after cTBS-on-Sl, we can also speculate that SI does not primar ily modulate cortico-muscular coherence. Since we have measured the whole cortical activity, we found cTBS-on-Sl-specific changes of widespread cortical mechanisms by means of cortical power or cortico-cortical coherence. These effects outlasted the stimulation duration for two hours and highlights the sensitivity of the cortical activity to stimulation of sensory cortices.
Our study is the first study combining cTBS stimulation with quantitative analysis of EEG and EMG signals during isometric contraction task, thus providing the first evidence that cTBS can alter cortico -muscular/-cortical synchronized and oscillatory activity.
108
Acknowledgements
First of all, I would like to thank my thesis supervisor, Prof. Nobuki Murayama for accepting me in his laboratory for five years as a graduate student. Without his vision, support, patience and guidance, this work could not have been done. Second, yet foremost, I would like to acknowledge Prof. Yuki Hayashida. Not only for his scientific supervision and professional mentorship, I would like to thank him also for his encouragement and friendship for which I will always be grateful. I would like to thank other members of my committee: Prof. Takahiro Inoue and Prof. Tsuyoshi Usagawa. Next, I have to acknowledge Japanese Ministry of Education, Culture, Sports, Science and Technology (MEXT) for supporting me financially for the last five years. I would like to express my gratitude to Ms. Nornaili binti Mat Safri for her guidance as an excellent senior colleague. I would also like to thank Dr. Kaoru Matsunaga from Kinoh Hospital for collaborating with me in this research. I should also acknowledge Dr. Tomohiko Igasaki for teaching me various scientific tools in the lab. I would also like to thank all the present and former members of the Murayama and Hayashida Laboratories, for kindly participating in my experiments. I am also grateful to all the members of the Turkish community. Among them, I have to single
out Mr. Ugur Unal and Mr. Tolga 6z§en for their brotherhood during this long
journey. Here, I am not able to express how grateful I am to my girlfriend, Ozge.
Without her love and continuous support, every thing would be very difficult. Last but not least, I have to dedicate everything to my family: my mother, my father, my
Bibliography
K. R. Alper, E. R. John, J. Brodie, W. Gnther, R. Daruwala, and L. S. Prichep. Cor relation of pet and qeeg in normal subjects. Psychiatry Research - Neuroimaging, 146(3):271-282, 2006.
S. N. Baker, E. Olivier, and R. N. Lemon. Coherent oscillations in monkey mo tor cortex and hand muscle emg show task-dependent modulation. Journal of Physiology, 501(l):225-241, 1997.
A. Berardelli, M. Inghilleri, J. C. Rothwell, S. Romeo, A. Curr, F. Gilio, N. Mod-ugno, and M. Manfredi. Facilitation of muscle evoked responses after repetitive cortical stimulation in man. Experimental Brain Research, 122(1) :79-84, 1998.
B. H. Bland and S. D. Oddie. Theta band oscillation and synchrony in the hip-pocampal formation and associated structures: The case for its role in sensorimo-tor integration. Behavioural brain research, 127(1-2): 119-136, 2001.
J. P. Brasil-Neto, L. G. Cohen, M. Panizza, J. Nilsson, B. J. Roth, and M. Hallett.
Optimal focal transcranial magnetic activation of the human motor cortex: Effects of coil orientation, shape of the induced current pulse, and stimulus intensity.
Journal of Clinical Neurophysiology, 9(1):132-136, 1992.
D. Brignani, P. Manganotti, P. M. Rossini, and C. Miniussi. Modulation of cor tical oscillatory activity during transcranial magnetic stimulation. Human brain mapping, 29(5):603-612, 2008.
110
A. Brovelli, M. Ding, A. Ledberg, Y. Chen, R. Nakamura, and S. L. Bressler. Beta oscillations in a large-scale sensorimotor cortical network: Directional influences revealed by granger causality. Proceedings of the National Academy of Sciences of the United States of America, 101(26):9849-9854, 2004.
R. Chen, J. Classen, C. Gerloff, P. Celnik, E. M. Wassermann, M. Hallett, and L. G. Cohen. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology, 48(5):1398-1403, 1997.
R. Chen, B. Corwell, Z. Yaseen, , M. Hallett, and L. G. Cohen. Mechanisms of cortical reorganization in lower-limb amputees. Journal of Neuroscience, 18(9):
3443-3450, 1998.
W. . Chen, T. Mima, H. R. Siebner, T. Oga, H. Hara, T. Satow, T. Begum, T. Nagamine, and H. Shibasaki. Low-frequency rtms over lateral premotor cortex induces lasting changes in regional activation and functional coupling of cortical motor areas. Clinical Neurophysiology, 114(9): 1628-1637, 2003.
Y.. Chen, C. . Huang, and K. . Hsu. Time-dependent reversal of long-term potenti-ation by low-frequency stimulpotenti-ation at the hippocampal mossy fiber-ca3 synapses.
Journal of Neuroscience, 21(ll):3705-3714, 2001.
B. A. Conway, D. M. Halliday, S. F. Farmer, U. Shahani, P. Maas, A. I. Weir, and J. R. Rosenberg. Synchronization between motor cortex and spinal motoneuronai pool during the performance of a maintained motor task in man. Journal of Physiology, 489(3) :917-924, 1995.
R. Courtemanche and Y. Lamarre. Local field potential oscillations in primate cerebellar cortex: Synchronization with cerebral cortex during active and passive expectancy. Journal of neurophysiology, 93(4):2039-2052, 2005.
R. Courtemanche, J. . Pellerin, and Y. Lamarre. Local field potential oscillations
R. Courtemanche, N. Pujii, and A. M. Graybiel. Synchronous, focally modulated beta-band oscillations characterize local field potential activity in the striatum of awake behaving monkeys. Journal of Neuroscience, 23(37): 11741-11752, 2003.
V. Di Lazzaro, F. Pilato, E. Saturno, A. Oliviero, M. Dileone, P. Mazzone, A. Insola, P. A. Tonali, F. Ranieri, Y. Z. Huang, and J. C. Rothwell. Theta-burst repetitive transcranial magnetic stimulation suppresses specific excitatory circuits in the human motor cortex. Journal of Physiology, 565(3):945-950, 2005.
S. F. Farmer, D. M. Halliday, B. A. Conway, J. A. Stephens, and J. R. Rosenberg. A review of recent applications of cross-correlation methodologies to human motor unit recording. Journal of neuroscience methods, 74(2): 175-187, 1997.
P. B. Fitzgerald, T. L. Brown, Z. J. Daskalakis, R. Chen, and J. Kulkarni. Intensity-dependent effects of 1 hz rtms on human corticospinal excitability. Clinical Neu-rophysiology, 113(7):1136-1141, 2002.
P. B. Fitzgerald, S. Fountain, and Z. J. Daskalakis. A comprehensive review of the effects of rtms on motor cortical excitability and inhibition. Clinical Neurophysi-ology, 117(12):2584-2596, 2006.
P. Fuhr, L. G. Cohen, B. J. Roth, and M. Hallett. Latency of motor evoked po tentials to focal transcranial stimulation varies as a function of scalp positions stimulated. Electroencephalography and Clinical Neurophysiology - Electrvmyog-raphy and Motor Control, 81(2):81-89, 1991.
C. Gerloff, J. Richard, J. Hadley, A. E. Schulman, M. Honda, and M. Hallett.
Functional coupling and regional activation of human cortical motor areas during simple, internally paced and externally paced finger movements. Brain, 121(8):
1513-1531, 1998.
C. Gerloff, C. Braun, M. Staudt, Y. L. Hegner, J. Dichgans, and I. Krgeloh-Mann.
Coherent corticomuscular oscillations originate from primary motor cortex:
Ev-112
idence from patients with early brain lesions. Human brain mapping, 27(10):
789-798, 2006.
I. Griskova, O. Ruksenas, K. Dapsys, S. Herpertz, and J. Hopner. The effects of 10 hz repetitive transcranial magnetic stimulation on resting eeg power spectrum in healthy subjects. Neuroscience letters, 419(2): 162-167, 2007.
P. Grosse, R. Guerrini, L. Parmeggiani, P. Bonanni, A. Pogosyan, and P. Brown.
Abnormal corticomuscular and intermuscular coupling in high-frequency rhythmic myoclonus. Brain, 126(2) :326-342, 2003.
N. Grossheinrich, A. Rau, O. Pogarell, K. Hennig-Fast, M. Reinl, S. Karch, A. Dieler, G. Leicht, C. Mulert, A. Sterr, and F. Padberg. Theta burst stimulation of the prefrontal cortex: Safety and impact on cognition, mood, and resting electroen cephalogram. Biological psychiatry, 2008. Article in Press.
M. Hallett. Transcranial magnetic stimulation and the human brain. Nature, 406 (6792):147-150, 2000.
D. M. Halliday, J. R. Rosenberg, A. M. Amjad, P. Breeze, B. A. Conway, and S. F.
Farmer. A framework for the analysis of mixed time series/point process data - theory and application to the study of physiological tremor, single motor unit discharges and electromyograms. Progress in biophysics and molecular biology, 64 (2-3):237-278, 1995.
D. M. Halliday, B. A. Conway, S. F. Farmer, and J. R. Rosenberg. Using elec-troencephalography to study functional coupling between cortical activity and electromyograms during voluntary contractions in humans. Neuroscience letters, 241(l):5-8, 1998.
N. L. Hansen and J. B. Nielsen. The effect of transcranial magnetic stimulation and
G. Hess and J. P. Donoghue. Facilitation of long-term potentiation in layer ii/iii horizontal connections of rat motor cortex following layer i stimulation: Route of effect and cholinergic contributions. Experimental Brain Research, 127(3) :279-290, 1999.
Y. Z. Huang, M. J. Edwards, E. Rounis, K. P. Bhatia, and J. C. Rothwell. Theta burst stimulation of the human motor cortex. Neuron, 45(2):201-206, 2005.
Y. Z. Huang, R. S. Chen, J. C. Rothwell, and H. . Wen. The after-effect of human theta burst stimulation is nmda receptor dependent. Clinical Neurophysiology, 118(5):1028-1032, 2007.
Y. Z. Huang, J. C. Rothwell, M. J. Edwards, and R. S. Chen. Effect of physiological activity on an nmda-dependent form of cortical plasticity in human. Cerebral
Cortex, 18(3):563-570, 2008.
S. Ishikawa, K. Matsunaga, R. Nakanishi, K. Kawahira, N. Murayama, S. Tsuji, Y. Z. Huang, and J. C. Rothwell. Effect of theta burst stimulation over the hu man sensorimotor cortex on motor and somatosensory evoked potentials. Clinical Neurophysiology, 118(5): 1033-1043, 2007.
H. Jing and M. Takigawa. Observation of eeg coherence after repetitive transcranial magnetic stimulation. Clinical Neurophysiology, 111(9): 1620-1631, 2000.
S. H. Jung, J. E. Shin, Y. . Jeong, and H. . Shin. Changes in motor cortical ex citability induced by high-frequency repetitive transcranial magnetic stimulation of different stimulation durations. Clinical Neurophysiology, 119(1):71-79, 2008.
W. Klimesch. Eeg alpha and theta oscillations reflect cognitive and memory perfor mance: A review and analysis. Brain Research Reviews, 29(2-3): 169-195, 1999.
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. Journal of Physiology, 471:501-519, 1993.
114
F, Maeda, J. P. Keenan, J, M. Tormos, H. Topka, and A. Pascual-Leone. Modula tion of corticospinal excitability by repetitive transcranial magnetic stimulation.
Clinical Neurophysiology, 111(5) 1800-805, 2000.
P. Manganotti, C. Gerloff, C. Toro, H. Katsuta, N. Sadato, P. Zhuang, L. Leocani, and M. Hallett. Task-related coherence and task-related spectral power changes during sequential finger movements. Electroencephalography and Clinical Neuro physiology - Electmmyography and Motor Control, 109(1):50-62, 1998.
J. F. Marsden, P. Ashby, P. Limousin-Dowsey, J. C. Rothwell, and P. Brown. Coher ence between cerebellar thalamus, cortex and muscle in man. cerebellar thalamus interactions. Brain, 123(7): 1459-1470, 2000.
J. F. Marsden, P. Limousin-Dowsey, P. Ashby, P. Pollak, and P. Brown. Subthalamic nucleus, sensorimotor cortex and muscle interrelationships in parkinson's disease.
Brain, 124(2):378~388, 2001.
K. R. Mills, S. J. Boniface, and M. Schubert. Magnetic brain stimulation with a dou ble coil: The importance of coil orientation. Electroencephalography and Clinical Neurophysiology - Electromyography and Motor Control, 85(1):17-21, 1992.
T. Mima and M. Hallett. Electroencephalographic analysis of cortico-muscular co herence: reference effect, volume conduction and generator mechanism. Clinical Neurophysiology, 110(ll):1892-1899, 1999a.
T. Mima and M. Hallett. Corticomuscular coherence: A review. Journal of Clinical Neurophysiology, 16(6):501-511, 1999b.
T. Mima, T. Matsuoka, and M. Hallett. Functional coupling of human right and left cortical motor areas demonstrated with partial coherence analysis. Neuroscience letters, 287(2):9&-96, 2000a.
T. Mima, J. Steger, A. E. Schulman, C. Gerloff, and M. Hallett. Electroencephalo-graphic measurement of motor cortex control of muscle activity in humans. Clin ical Neurophysiology, lll(2):326-337, 2000b.
T. Mima, T. Matsuoka, and M. Hallett. Information flow from the sensorimotor cortex to muscle in humans. Clinical Neurophysiology, 112(1):122-126, 2001.
N. Murayama, Y. . Lin, S. Salenius, and R. Hari. Oscillatory interaction between human motor cortex and trunk muscles during isometric contraction. Neurolmage, 14(5):1206-1213, 2001.
V. N. Murthy and E. E. Fetz. Oscillatory activity in sensorimotor cortex of awake monkeys: Synchronization of local field potentials and relation to behavior. Jour-nal of neurophysiology, 76(6):3949-3967, 1996.
S. Ohara, T. Mima, K. Baba, A. Ikeda, T. Kunieda, R. Matsumoto, J. Yamamoto, M. Matsuhashi, T. Nagamine, K. Hirasawa, T. Hori, T. Mihara, N. Hashimoto, S. Salenius, and H. Shibasaki. Increased synchronization of cortical oscillatory activities between human supplementary motor and primary sensorimotor areas during voluntary movements. Journal of Neuroscience, 21(23):9377-9386, 2001.
H. Okamura, H. Jing, and M. Takigawa. Eeg modification induced by repetitive transcranial magnetic stimulation. Journal of Clinical Neurophysiology, 18(4):
318-325, 2001.
A. Oliviero, L. H. A. Strens, V. Lazzaro, P. A. Tonali, and P. Brown. Persistent effects of high frequency repetitive tms on the coupling between motor areas in the human. Experimental Brain Research, 149(1): 107-113, 2003.
A. Pascual-Leone, J. VaUs-Sole\ E. M. Wassermann, and M. Hallett. Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain, 117(4):847-858, 1994.
116
A. Peinemann, B. Reimer, C. Lor, A. Quartarone, A. Muchau, B. Conrad, and H. R. Siebner. Long-lasting increase in corticospinal excitability after 1800 pulses of subthreshold 5 hz repetitive tms to the primary motor cortex. Clinical Neuro-physiology, 115(7): 1519-1526, 2004.
I. Penfield and T. Rasmussen. The cerebral cortex of man: A clinical study of localization of function. Macmillan, New York, 1950.
F. Perrin, J. Pernier, O. Bertrand, and J. F. Echallier. Spherical splines for scalp potential and current density mapping. Electroencephalography and clinical neu-rophysiology, 72(2): 184-187, 1989.
G. Pfurtscheller, A. Stancak Jr., and Ch Neuper. Event-related synchronization (ers) in the alpha band - an electrophysiological correlate of cortical idling: A review. International Journal of Psychophysiology, 24(l-2):39-46, 1996.
G. Pfurtscheller, Ch Neuper, C. Andrew, and G. Edlinger. Foot and hand area mu rhythms. International Journal of Psychophysiology, 26(1-3):121-135, 1997.
C. Plewnia, A. J. Rilk, S. R. Soekadar, C. Arfeller, H. S. Huber, P. Sauseng, F. Hum mel, and C. Gerloff. Enhancement of long-range eeg coherence by synchronous bifocal transcranial magnetic stimulation. European Journal of Neuroscience, 27 (6):1577-1583, 2008.
M. Pohja and S. Salenius. Modulation of cortex-muscle oscillatory interaction by ischaemia-induced deafferentation. Neuroreport, 14(3):321-324, 2003.
J. R. Rosenberg, A. M. Amjad, P. Breeze, D. R. Brillinger, and D. M. Halliday. The fourier approach to the identification of functional coupling between neuronal spike trains. Progress in biophysics and molecular biology, 53(1):1-31, 1989.
N. Safri, N. Murayama, Y. Hayashida, and T. Igasaki. Eifects of concurrent visual
N. M. Safri, N. Murayama, T. Igasaki, and Y. Hayashida. Effects of visual stimu lation on corticospinal coherence during isometric hand contraction in humans.
International Journal of Psychophysiology, 61(2):288-293, 2006.
N.M. Safri. Effects of externally applied sensory stimulation on the motor cortex-muscle synchronization in humans. PhD thesis, Kumamoto University, 2005.
S. Salenius, R. Salmelin, C. Neuper, G. Pfurtscheller, and R, Hari. Human cortical
40 hz rhythm is closely related to emg rhythmicity. Neuroscience letters, 213(2):
75-78, 1996.
S. Salenius, K. Portin, M. Kajola, R. Salmelin, and R. Hari. Cortical control of hu man motoneuron firing during isometric contraction. Journal of neurophysiology, 77(6):3401-3405, 1997.
R. Salmelin and R. Hari. Spatiotemporal characteristics of sensorimotor neuromag-netic rhythms related to thumb movement. Neuroscience, 60(2):537-550, 1994.
J. Sarnthein and D. Jeanmonod. High thalamocortical theta coherence in patients with parkinson's disease. Journal of Neuroscience, 27(1): 124-131, 2007.
K. Schindler, T. Nyffeler, R. Wiest, M. Hauf, J. Mathis, Ch W. Hess, and R. Mui.
Theta burst transcranial magnetic stimulation is associated with increased eeg synchronization in the stimulated relative to unstimulated cerebral hemisphere.
Neuroscience letters, 436(l):31-34, 2008.
J.. Schoffelen, R. Oostenveld, and P. Pries. Imaging the human motor system's beta-band synchronization during isometric contraction. Neurolmage, 41(2):437-447, 2008.
H. R. Siebner, M. Peller, F. Willoch, S. Minoshima, H. Boecker, C. Auer, A. Drzezga, B. Conrad, and P. Bartenstein. Lasting cortical activation after repetitive tms of the motor cortex: A glucose metabolic study. Neurology, 54(4):956-963, 2000.
118
A. Siegel and H. N. Sapru. Essential Neuroscience, 1st Edition. Lippincott Williams Wilkins, 2006.
T. Silen, N. Forss, S. Salenius, T. Karjalainen, and R. Hari. Oscillatory cortical drive to isometrically contracting muscle in unverricht-lundborg type progressive myoclonus epilepsy (uld). Clinical Neurophysiology, 113(12): 1973-1979, 2002.
D. S. Soteropoulos and S. N. Baker. Cortico-cerebellar coherence during a precision grip task in the monkey. Journal of neurophysiology, 95(2) :1194-1206, 2006.
A. M. Speer, T. A. Kimbrell, E. M. Wassermann, J. D. Repella, M. W. Willis, P. Herscovitch, and R. M. Post. Opposite effects of high and low frequency rtms on regional brain activity in depressed patients. Biological psychiatry, 48(12):
1133-1141, 2000.
L. H. A. Strens, A. Oliviero, B. R. Bloem, W. Gerschlager, J. C. Rothweil, and P. Brown. The effects of subthreshold 1 hz repetitive tms on cortico-cortical and interhemispheric coherence. Clinical Neurophysiology, 113(8):1279-1285, 2002.
L. H. A. Strens, P. Asselman, A. Pogosyan, C. Loukas, A. J. Thompson, and P. Brown. Corticocortical coupling in chronic stroke: Its relevance to recovery.
Neurology, 63(3):475-484, 2004.
T. Touge, W. Gerschlager, P. Brown, and J. C. Rothweil. Are the after-effects of low-frequency rtms on motor cortex excitability due to changes in the efficacy of cortical synapses? Clinical Neurophysiology, 112(11):2138-2145, 2001.
J.G. Webster. Medical Instrumentation Application and Design. John Wiley Sons, 1998.
L. A. Wheaton, S. Bohlhalter, G. Nolte, H. Shibasaki, N. Hattori, E. Fridman, S. Vorbach, J. Grafman, and M. Hallett. Cortico-cortical networks in patients with