Cortical hemoglobin-concentration changes under the coil induced by single-pulse TMS in humans: a simultaneous recording with near-infrared spectroscopy

We measured cortical hemoglobin-concentration changes under the coil induced by single-pulse transcranial magnetic stimulation (TMS) using a technique of simultaneous recording with near-infrared spectroscopy (NIRS). Single-pulse TMS was delivered over the hand area of the left primary motor cortex at an intensity of 100, 120, or 140% of the active motor threshold (AMT). NIRS recordings were also made during sham stimulation. These four different stimulation sessions (TMS at three intensities and sham stimulation) were performed both when the subject slightly contracted the right first dorsal interosseous muscle and when relaxed it (active and resting conditions). Under the active condition with TMS at 100% AMT, we observed a transient increase in oxy-hemoglobin (oxy-Hb), which was significantly larger than sham stimulation. Under the resting conditions with TMS at 120 and 140% AMT, we observed significant decreases in both deoxy-hemoglobin (deoxyHb) and total-hemoglobin (total-Hb) as compared to sham stimulation. We suggest that the increase of oxy-Hb concentration at 100% AMT under the active condition reflects an add-on effect by TMS to the active baseline and that decrease of deoxy-Hb and total-Hb concentrations at 120 and 140% AMT under the resting condition are due to reduced baseline firings of the corticospinal tract neurons induced by a lasting inhibition provoked by a higher intensity TMS.

[1]  Kuniyoshi L. Sakai,et al.  An event-related optical topography study of cortical activation induced by single-pulse transcranial magnetic stimulation , 2003, NeuroImage.

[2]  Hiroki Sato,et al.  Practicality of Wavelength Selection to Improve Signal-to-noise Ratio in Near-infrared Spectroscopy , 2003 .

[3]  Atsushi Maki,et al.  Non-invasive assessment of language dominance with near-infrared spectroscopic mapping , 1998, Neuroscience Letters.

[4]  John Rothwell,et al.  Effects of low frequency and low intensity repetitive paired pulse stimulation of the primary motor cortex , 2004, Clinical Neurophysiology.

[5]  A Villringer,et al.  Saccadic Suppression Induces Focal Hypooxygenation in the Occipital Cortex , 2000, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

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

[7]  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.

[8]  P. Ashby,et al.  Mechanism of the silent period following transcranial magnetic stimulation Evidence from epidural recordings , 1999, Experimental Brain Research.

[9]  T. Mima,et al.  Brain structures related to active and passive finger movements in man. , 1999, Brain : a journal of neurology.

[10]  J. L. Taylor,et al.  The effect of voluntary contraction on cortico‐cortical inhibition in human motor cortex. , 1995, The Journal of physiology.

[11]  J. Nielsen,et al.  Investigating human motor control by transcranial magnetic stimulation , 2003, Experimental Brain Research.

[12]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[13]  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.

[14]  G Laborde,et al.  Frameless Neuronavigation in Modern Neurosurgery , 1995, Minimally invasive neurosurgery : MIN.

[15]  R. Töpper,et al.  Localization of the motor hand area using transcranial magnetic stimulation and functional magnetic resonance imaging , 1999, Clinical Neurophysiology.

[16]  S Nioka,et al.  Comparison of time-resolved and -unresolved measurements of deoxyhemoglobin in brain. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[17]  R. Nelson,et al.  Cerebral near infrared spectroscopy: emitter-detector separation must be increased. , 1999, British journal of anaesthesia.

[18]  Klaus Funke,et al.  Effect of transcranial magnetic stimulation on single‐unit activity in the cat primary visual cortex , 2003, The Journal of physiology.

[19]  Per Lav Madsen,et al.  Near-infrared oximetry of the brain , 1999, Progress in Neurobiology.

[20]  A Berardelli,et al.  Silent period evoked by transcranial stimulation of the human cortex and cervicomedullary junction. , 1993, The Journal of physiology.

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

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

[23]  Jens Frahm,et al.  Subthreshold high-frequency TMS of human primary motor cortex modulates interconnected frontal motor areas as detected by interleaved fMRI-TMS , 2003, NeuroImage.

[24]  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.

[25]  C. Mathiesen,et al.  Temporal coupling between neuronal activity and blood flow in rat cerebellar cortex as indicated by field potential analysis , 2000, The Journal of physiology.

[26]  Walter Paulus,et al.  Complete suppression of voluntary motor drive during the silent period after transcranial magnetic stimulation , 1999, Experimental Brain Research.

[27]  A. Kleinschmidt,et al.  Simultaneous Recording of Cerebral Blood Oxygenation Changes during Human Brain Activation by Magnetic Resonance Imaging and Near-Infrared Spectroscopy , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[28]  A. Villringer,et al.  Near infrared spectroscopy (NIRS): A new tool to study hemodynamic changes during activation of brain function in human adults , 1993, Neuroscience Letters.

[29]  Ziad Nahas,et al.  A combined TMS/fMRI study of intensity-dependent TMS over motor cortex , 1999, Biological Psychiatry.

[30]  C. Marsden,et al.  Corticocortical inhibition in human motor cortex. , 1993, The Journal of physiology.

[31]  W. Hoefnagels,et al.  Simultaneous measurements of cerebral oxygenation changes during brain activation by near‐infrared spectroscopy and functional magnetic resonance imaging in healthy young and elderly subjects , 2002, Human brain mapping.

[32]  Robert Chen,et al.  Interactions between inhibitory and excitatory circuits in the human motor cortex , 2003, Experimental Brain Research.

[33]  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.

[34]  A Maki,et al.  Wavelength dependence of the precision of noninvasive optical measurement of oxy-, deoxy-, and total-hemoglobin concentration. , 2001, Medical physics.

[35]  Sergio Fantini,et al.  A haemodynamic model for the physiological interpretation of in vivo measurements of the concentration and oxygen saturation of haemoglobin. , 2002, Physics in medicine and biology.

[36]  C. Mathiesen,et al.  Modification of activity‐dependent increases of cerebral blood flow by excitatory synaptic activity and spikes in rat cerebellar cortex , 1998, The Journal of physiology.

[37]  A. Villringer,et al.  Cross talk in the Lambert-Beer calculation for near-infrared wavelengths estimated by Monte Carlo simulations. , 2002, Journal of biomedical optics.

[38]  Sergio Fantini,et al.  Bilateral near-infrared monitoring of the cerebral concentration and oxygen-saturation of hemoglobin during right unilateral electro-convulsive therapy , 2003, Brain Research.

[39]  Yoshikazu Ugawa,et al.  Long‐term effect of motor cortical repetitive transcranial magnetic stimulation induces , 2004 .

[40]  F. Jöbsis Noninvasive, infrared monitoring of cerebral and myocardial oxygen sufficiency and circulatory parameters. , 1977, Science.

[41]  Takashi Kusaka,et al.  Functional imaging of the brain in sedated newborn infants using near infrared topography during passive knee movement , 2001, Neuroscience Letters.

[42]  S. Bestmann,et al.  Functional MRI of cortical activations induced by transcranial magnetic stimulation (TMS) , 2001, Neuroreport.

[43]  E. Watanabe,et al.  Non-invasive functional mapping with multi-channel near infra-red spectroscopic topography in humans , 1996, Neuroscience Letters.

[44]  K. Sakai,et al.  Paired‐pulse magnetic stimulation of the human motor cortex: differences among I waves , 1998, The Journal of physiology.

[45]  David A. Boas,et al.  Factors affecting the accuracy of near-infrared spectroscopy concentration calculations for focal changes in oxygenation parameters , 2003, NeuroImage.

[46]  A. Berardelli,et al.  Cortical inhibition in Parkinson's disease. A study with paired magnetic stimulation. , 1996, Brain : a journal of neurology.

[47]  A Villringer,et al.  Functional magnetic resonance imaging shows localized brain activation during serial transcranial stimulation in man , 1996, Neuroreport.

[48]  E. Evarts TEMPORAL PATTERNS OF DISCHARGE OF PYRAMIDAL TRACT NEURONS DURING SLEEP AND WAKING IN THE MONKEY. , 1964, Journal of neurophysiology.

[49]  A. Grinvald,et al.  Interactions Between Electrical Activity and Cortical Microcirculation Revealed by Imaging Spectroscopy: Implications for Functional Brain Mapping , 1996, Science.

[50]  鯨井 隆 Corticocortical inhibition in human motor cortex , 1994 .

[51]  M. Hallett,et al.  Transcranial magnetic stimulation techniques in clinical investigation , 2002, Neurology.