Somatotopic blocking of sensation with navigated transcranial magnetic stimulation of the primary somatosensory cortex

We demonstrate that spatially accurate and selective stimulation is crucial when cortical functions are studied by the creation of temporary lesions with transcranial magnetic stimulation (TMS). Previously, the interpretation of the TMS results has been hampered by inaccurate knowledge of the site and strength of the induced electric current in the brain. With a Navigated Brain Stimulation (NBS) system, which provides real‐time magnetic resonance image (MRI)‐guided targeting of the TMS‐induced electric field, we found that TMS of a spatially restricted cortical S1 thenar area is sufficient to abolish sensation from a weak electric stimulation of the corresponding skin area. We demonstrate that with real‐time navigation, TMS can be repeatably directed at millimeter‐level precision to a target area defined on the MRI. The stimulation effect was temporally and spatially specific: the greatest inhibition of sensation occurred when TMS was applied 20 ms after the cutaneous test stimulus and the TMS effect was sensitive to 8–13 mm displacements of the induced electric field pattern. The results also indicate that TMS selectively to S1 is sufficient to abolish perception of cutaneous stimulation of the corresponding skin area. Hum Brain Mapp, 2005. © 2005 Wiley‐Liss, Inc.

[1]  A. Pertovaara,et al.  The movement-induced modulation in discriminability between cutaneous nonpainful stimuli depends on test stimulus intensity , 2004, Experimental Brain Research.

[2]  B LIBET,et al.  PRODUCTION OF THRESHOLD LEVELS OF CONSCIOUS SENSATION BY ELECTRICAL STIMULATION OF HUMAN SOMATOSENSORY CORTEX. , 1964, Journal of neurophysiology.

[3]  Y. Lamarre,et al.  Modulation of somatosensory evoked responses in the primary somatosensory cortex produced by intracortical microstimulation of the motor cortex in the monkey , 2004, Experimental Brain Research.

[4]  D. Rasmusson,et al.  Corticocortical inhibition of peripheral inputs within primary somatosensory cortex: the role of GABA(A) and GABA(B) receptors. , 2003, Journal of neurophysiology.

[5]  M Seyal,et al.  Suppression of cutaneous perception by magnetic pulse stimulation of the human brain. , 1992, Electroencephalography and clinical neurophysiology.

[6]  Justin A. Harris,et al.  Transient Storage of a Tactile Memory Trace in Primary Somatosensory Cortex , 2002, The Journal of Neuroscience.

[7]  J. Swets.  The Relative Operating Characteristic in Psychology , 1973, Science.

[8]  M. Hallett,et al.  Differentiation of sensorimotor neuronal structures responsible for induction of motor evoked potentials, attenuation in detection of somatosensory stimuli, and induction of sensation of movement by mapping of optimal current directions. , 1994, Electroencephalography and clinical neurophysiology.

[9]  C. E. Chapman,et al.  Time course and magnitude of movement-related gating of tactile detection in humans. I. Importance of stimulus location. , 1998, Journal of neurophysiology.

[10]  S. Gandevia,et al.  Reduction in perceived intensity of cutaneous stimuli during movement: a quantitative study , 2004, Experimental Brain Research.

[11]  Angel Nuñez,et al.  Primary somatosensory cortex modulation of tactile responses in nucleus gracilis cells of rats , 2004, The European journal of neuroscience.

[12]  M. Hallett,et al.  Optimal Focal Transcranial Magnetic Activation of the Human Motor Cortex: Effects of Coil Orientation, Shape of the Induced Current Pulse, and Stimulus Intensity , 1992, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[13]  John K. Chapin,et al.  Mapping the effects of motor cortex stimulation on somatosensory relay neurons in the rat thalamus: Direct responses and afferent modulation , 1990, Brain Research Bulletin.

[14]  Conrad V. Kufta,et al.  Attenuation in detection of somatosensory stimuli by transcranial magnetic stimulation. , 1991, Electroencephalography and clinical neurophysiology.

[15]  C. C. Wood,et al.  Human cortical potentials evoked by stimulation of the median nerve. I. Cytoarchitectonic areas generating short-latency activity. , 1989, Journal of neurophysiology.

[16]  Simona Temereanca,et al.  Functional Topography of Corticothalamic Feedback Enhances Thalamic Spatial Response Tuning in the Somatosensory Whisker/Barrel System , 2004, Neuron.

[17]  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.

[18]  Timothy S Miles,et al.  Magnetic stimulation of motor and somatosensory cortices suppresses perception of ulnar nerve stimuli. , 2003, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[19]  M. de Carvalho,et al.  A new method for reproducible coil positioning in transcranial magnetic stimulation mapping. , 1997, Electroencephalography and clinical neurophysiology.

[20]  A. Nakamura,et al.  Somatosensory Homunculus as Drawn by MEG , 1998, NeuroImage.

[21]  Seppo Kähkönen,et al.  The effect of stimulus intensity on brain responses evoked by transcranial magnetic stimulation , 2004, Human brain mapping.

[22]  R. Ilmoniemi,et al.  Modulation of electroencephalographic responses to transcranial magnetic stimulation: evidence for changes in cortical excitability related to movement , 2003, The European journal of neuroscience.

[23]  R. Ilmoniemi,et al.  Multichannel magnetic stimulation: improved stimulus targeting. , 1996 .

[24]  C. E. Chapman,et al.  Sensory perception during movement in man , 2004, Experimental Brain Research.

[25]  Juha Virtanen,et al.  Relationships between magnetic stimulation and MEG/EEG , 1996 .

[26]  B R Rosen,et al.  Stereotactic transcranial magnetic stimulation: correlation with direct electrical cortical stimulation. , 1997, Neurosurgery.

[27]  L. Garcia-Larrea,et al.  Timing and characteristics of perceptual attenuation by transcranial stimulation: a study using magnetic cortical stimulation and somatosensory-evoked potentials. , 1999, Psychophysiology.

[28]  Axel Thielscher,et al.  Linking Physics with Physiology in TMS: A Sphere Field Model to Determine the Cortical Stimulation Site in TMS , 2002, NeuroImage.

[29]  R J Ilmoniemi,et al.  Modeling of the stimulating field generation in TMS. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[30]  C C Wood,et al.  Human cortical potentials evoked by stimulation of the median nerve. II. Cytoarchitectonic areas generating long-latency activity. , 1989, Journal of neurophysiology.

[31]  Hyung-Cheul Shin,et al.  Mapping the effects of motor cortex stimulation on single neurons in the dorsal column nuclei in the rat: Direct responses and afferent modulation , 1989, Brain Research Bulletin.

[32]  J. Mattingley,et al.  Fast and slow parietal pathways mediate spatial attention , 2004, Nature Neuroscience.

[33]  K. A. Hadland,et al.  Role of the human medial frontal cortex in task switching: a combined fMRI and TMS study. , 2002, Journal of neurophysiology.

[34]  R Salmelin,et al.  The 3D topography of MEG source localization accuracy: effects of conductor model and noise , 2003, Clinical Neurophysiology.

[35]  Nick F. Ramsey,et al.  A stereotactic method for image-guided transcranial magnetic stimulation validated with fMRI and motor-evoked potentials , 2004, NeuroImage.

[36]  J. Sarvas.  Basic mathematical and electromagnetic concepts of the biomagnetic inverse problem. , 1987, Physics in medicine and biology.

[37]  R J Ilmoniemi,et al.  Transcranial magnetic stimulation as a tool for cognitive studies. , 2001, Scandinavian journal of psychology.

[38]  M. Seyal,et al.  Suppression of spatial localization of a cutaneous stimulus following transcranial magnetic pulse stimulation of the sensorimotor cortex. , 1997, Electroencephalography and clinical neurophysiology.