Long‐term effect of motor cortical repetitive transcranial magnetic stimulation induces

Repetitive transcranial magnetic stimulation (rTMS) recently has been assessed as a noninvasive treatment modality for movement and psychiatric disorders, whereas the mechanism underlying the therapeutic effects is not fully understood. Studies in rodents showed lasting functional changes in some selected regions, such as limbic‐associated structures, but unfocused brain stimulation did not clarify the regional effects. To address the topographical and temporal profiles of the effects on glucose metabolism in primate brain, we performed rTMS and repeated 18F‐fluorodeoxyglucose positron emission tomography (FDG‐PET) before, during, and up to 16 days after rTMS in anesthetized cynomologous monkeys. We delivered a total of 2,000 pulses of 5Hz‐rTMS over the right precentral gyrus using a small‐sized eight‐figured coil that induced a localized electrical field. Voxel‐based analysis in a standard space of the macaque brain showed statistically robust changes in FDG uptake: a decrease in the motor/premotor cortices and an increase in the limbic‐associated areas involving the anterior/posterior cingulate, and orbitofrontal cortices. Interestingly, these uptake changes continued for at least 8 days and the magnitude of the lasting effects in the limbic‐related areas was negatively correlated across subjects with those in the motor/premotor cortices. The results demonstrate that motor rTMS has a long‐term lasting effect on motor‐related regions and distant limbic‐related areas via functional connections.

[1]  M Hallett,et al.  Safety of different inter-train intervals for repetitive transcranial magnetic stimulation and recommendations for safe ranges of stimulation parameters. , 1997, Electroencephalography and clinical neurophysiology.

[2]  H. Fukuyama,et al.  Neuronal nitric oxide has a role as a perfusion regulator and a synaptic modulator in cerebellum but not in neocortex during somatosensory stimulation—An animal PET study , 2002, Neuroscience Research.

[3]  A. Drzezga,et al.  Continuous Transcranial Magnetic Stimulation during Positron Emission Tomography: A Suitable Tool for Imaging Regional Excitability of the Human Cortex , 2001, NeuroImage.

[4]  Richard F. Martin,et al.  Primate brain maps : structure of the macaque brain , 2000 .

[5]  P Mertens,et al.  Electrical stimulation of motor cortex for pain control: a combined PET-scan and electrophysiological study , 1999, PAIN.

[6]  H. Siebner,et al.  Imaging brain activation induced by long trains of repetitive transcranial magnetic stimulation , 1998, Neuroreport.

[7]  C. Cavada,et al.  The anatomical connections of the macaque monkey orbitofrontal cortex. A review. , 2000, Cerebral cortex.

[8]  Yoshikazu Ugawa,et al.  Endogenous dopamine release induced by repetitive transcranial magnetic stimulation over the primary motor cortex: an [11C]raclopride positron emission tomography study in anesthetized macaque monkeys , 2004, Biological Psychiatry.

[9]  G A Orban,et al.  Functional impact of cerebral connections. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[10]  P. Fitzgerald,et al.  Intensity-dependent effects of 1 Hz rTMS on human corticospinal excitability , 2002, Clinical Neurophysiology.

[11]  T. Ohnishi,et al.  Effects of 1-Hz repetitive transcranial magnetic stimulation on acute pain induced by capsaicin , 2004, Pain.

[12]  M. Segal,et al.  Long-Term Effects of Transcranial Magnetic Stimulation on Hippocampal Reactivity to Afferent Stimulation , 1999, The Journal of Neuroscience.

[13]  Alan C. Evans,et al.  Propofol anesthesia and cerebral blood flow changes elicited by vibrotactile stimulation: a positron emission tomography study. , 2001, Journal of neurophysiology.

[14]  Takuya Hayashi,et al.  A coil for magnetic stimulation of the macaque monkey brain. , 2003, Supplements to Clinical neurophysiology.

[15]  Karl J. Friston,et al.  Acute Remapping within the Motor System Induced by Low-Frequency Repetitive Transcranial Magnetic Stimulation , 2003, The Journal of Neuroscience.

[16]  Ichiro Kanazawa,et al.  0.2‐Hz repetitive transcranial magnetic stimulation has no add‐on effects as compared to a realistic sham stimulation in Parkinson's disease , 2003, Movement disorders : official journal of the Movement Disorder Society.

[17]  E. Lynd-Balta,et al.  The orbital and medial prefrontal circuit through the primate basal ganglia , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  G. V. Van Hoesen,et al.  Cingulate input to the primary and supplementary motor cortices in the rhesus monkey: Evidence for somatotopy in areas 24c and 23c , 1992, The Journal of comparative neurology.

[19]  R. Haier,et al.  Positron Emission Tomography Study of Regional Cerebral Metabolism in Humans during Isoflurane Anesthesia , 1997, Anesthesiology.

[20]  R. Racine,et al.  Long-term potentiation in the neocortex of the adult, freely moving rat. , 1998, Cerebral cortex.

[21]  H Scheich,et al.  LTD and LTP induced by transcranial magnetic stimulation in auditory cortex , 1996, Neuroreport.

[22]  N. Toschi,et al.  Long-Term Repetitive Transcranial Magnetic Stimulation Increases the Expression of Brain-Derived Neurotrophic Factor and Cholecystokinin mRNA, but not Neuropeptide Tyrosine mRNA in Specific Areas of Rat Brain , 2000, Neuropsychopharmacology.

[23]  T. Paus,et al.  Cerebral blood-flow changes induced by paired-pulse transcranial magnetic stimulation of the primary motor cortex. , 2001, Journal of neurophysiology.

[24]  Scott T. Grafton,et al.  Automated image registration: I. General methods and intrasubject, intramodality validation. , 1998, Journal of computer assisted tomography.

[25]  Pierre J Magistretti,et al.  GABA uptake into astrocytes is not associated with significant metabolic cost: Implications for brain imaging of inhibitory transmission , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[26]  R. Tovell,et al.  ANESTHESIA FOR ELECTROCONVULSIVE THERAPY , 1954, Anesthesiology.

[27]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[28]  C. Epstein,et al.  Magnetic brain stimulation and brain size: relevance to animal studies. , 1992, Electroencephalography and clinical neurophysiology.

[29]  Alan C. Evans,et al.  Dose-dependent reduction of cerebral blood flow during rapid-rate transcranial magnetic stimulation of the human sensorimotor cortex. , 1998, Journal of neurophysiology.

[30]  Philippe A. Chouinard,et al.  Modulating neural networks with transcranial magnetic stimulation applied over the dorsal premotor and primary motor cortices. , 2003, Journal of neurophysiology.

[31]  A. Jenny Commissural projections of the cortical hand motor area in monkeys , 1979, The Journal of comparative neurology.

[32]  Harumasa Takano,et al.  Functional connectivity revealed by single-photon emission computed tomography (SPECT) during repetitive transcranial magnetic stimulation (rTMS) of the motor cortex , 2003, Clinical Neurophysiology.

[33]  J Valls-Solé,et al.  Akinesia in Parkinson's disease. II. Effects of subthreshold repetitive transcranial motor cortex stimulation , 1994, Neurology.

[34]  C M Epstein,et al.  Repetitive transcranial magnetic stimulation activates specific regions in rat brain. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[36]  A Jon Stoessl,et al.  For Personal Use. Only Reproduce with Permission from the Lancet Publishing Group. Placebos and the Placebo Effect the Placebo Effect in Neurological Disorders , 2022 .

[37]  Á. Pascual-Leone,et al.  Rapid-rate transcranial magnetic stimulation of left dorsolateral prefrontal cortex in drug-resistant depression , 1996, The Lancet.

[38]  S. Leurgans,et al.  Objective changes in motor function during placebo treatment in PD , 2000, Neurology.

[39]  M. Hallett,et al.  Depression of motor cortex excitability by low‐frequency transcranial magnetic stimulation , 1997, Neurology.

[40]  B Conrad,et al.  Repetitive transcranial magnetic stimulation has a beneficial effect on bradykinesia in Parkinson's disease. , 1999, Neuroreport.

[41]  M Schulzer,et al.  Expectation and Dopamine Release: Mechanism of the Placebo Effect in Parkinson's Disease , 2001, Science.

[42]  Peter T. Fox,et al.  Imaging human intra‐cerebral connectivity by PET during TMS , 1997, Neuroreport.

[43]  E. Wassermann 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. , 1998, Electroencephalography and clinical neurophysiology.

[44]  S Minoshima,et al.  Lasting cortical activation after repetitive TMS of the motor cortex , 2000, Neurology.

[45]  Karl J. Friston,et al.  Rapid Assessment of Regional Cerebral Metabolic Abnormalities in Single Subjects with Quantitative and Nonquantitative [18F]FDG PET: A Clinical Validation of Statistical Parametric Mapping , 1999, NeuroImage.