Column‐based model of electric field excitation of cerebral cortex

A model to explain the orientation selectivity of the neurophysiologic effects of electric‐field transients applied to cerebral cortex is proposed and supported with neuroimaging evidence. Although it is well known that transcranial magnetic stimulation (TMS) excites cerebral cortex in an orientation‐selective manner, a neurophysiologically compelling explanation of this phenomenon has been lacking. It is generally presumed that TMS‐induced excitation is mediated by horizontal fibers in the cortical surfaces nearest to the stimulating coil, i.e., at the gyral crowns. No evidence exists, however, that horizontal fibers are orientation selective either anatomically or physiologically. We used positron emission tomography to demonstrate that TMS‐induced cortical activation is selectively sulcal. This observation allows the well‐established columnar organization of cerebral cortex to be invoked to explain the observed orientation selectivity. In addition, Rushton's cosine principle can used to model stimulation efficacy for an electrical field applied at any cortical site at any intensity and in any orientation. Hum. Brain Mapp. 22:1–16, 2004. © 2004 Wiley‐Liss, Inc.

[1]  W. Rushton The effect upon the threshold for nervous excitation of the length of nerve exposed, and the angle between current and nerve , 1927, The Journal of physiology.

[2]  D. O. Rudin,et al.  THE ACTION POTENTIAL OF SPINAL AXONS IN VITRO , 1954, The Journal of general physiology.

[3]  C. G. Phillips,et al.  Unifocal and bifocal stimulation of the motor cortex , 1962, The Journal of physiology.

[4]  C. G. Phillips,et al.  Selective excitation of corticofugal neurones by surface‐anodal stimulation of the baboon's motor cortex , 1962, The Journal of physiology.

[5]  M. Clare,et al.  Site of excitation in stimulation of the motor cortex. , 1965, Journal of neurophysiology.

[6]  D. Purpura,et al.  INTRACELLULAR ACTIVITIES AND EVOKED POTENTIAL CHANGES DURING POLARIZATION OF MOTOR CORTEX. , 1965, Journal of neurophysiology.

[7]  A. Gorman,et al.  Differential patterns of activation of the pyramidal system elicited by surface anodal and cathodal cortical stimulation. , 1966, Journal of neurophysiology.

[8]  V E Amassian,et al.  An analysis of the activation of motor cortical neurons by surface stimulation. , 1967, Journal of neurophysiology.

[9]  J. B. Ranck,et al.  Which elements are excited in electrical stimulation of mammalian central nervous system: A review , 1975, Brain Research.

[10]  M. Carpenter The cerebral cortex , 1976 .

[11]  S P Wise,et al.  Size, laminar and columnar distribution of efferent cells in the sensory‐motor cortex of monkeys , 1977, The Journal of comparative neurology.

[12]  D H Hubel,et al.  Brain mechanisms of vision. , 1979, Scientific American.

[13]  M. Raichle,et al.  The role of cerebral cortex in the generation of voluntary saccades: a positron emission tomographic study. , 1985, Journal of neurophysiology.

[14]  C. Nicholson,et al.  A model for the polarization of neurons by extrinsically applied electric fields. , 1986, Biophysical journal.

[15]  M. Alexander,et al.  Principles of Neural Science , 1981 .

[16]  C. Nicholson,et al.  Modulation by applied electric fields of Purkinje and stellate cell activity in the isolated turtle cerebellum. , 1986, The Journal of physiology.

[17]  M. Raichle,et al.  Mapping human somatosensory cortex with positron emission tomography. , 1987, Journal of neurosurgery.

[18]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[19]  B. Day,et al.  Electric and magnetic stimulation of human motor cortex: surface EMG and single motor unit responses. , 1989, The Journal of physiology.

[20]  V E Amassian,et al.  A comparison of corticospinal activation by magnetic coil and electrical stimulation of monkey motor cortex. , 1990, Electroencephalography and clinical neurophysiology.

[21]  M Hallett,et al.  A theoretical calculation of the electric field induced in the cortex during magnetic stimulation. , 1991, Electroencephalography and clinical neurophysiology.

[22]  J C Mazziotta,et al.  Somatotopic mapping of the primary motor cortex in humans: activation studies with cerebral blood flow and positron emission tomography. , 1991, Journal of neurophysiology.

[23]  F. H. Lopes da Silva Neural mechanisms underlying brain waves: from neural membranes to networks. , 1991, Electroencephalography and clinical neurophysiology.

[24]  S. Boniface,et al.  Magnetic brain stimulation with a double coil: the importance of coil orientation. , 1992, Electroencephalography and clinical neurophysiology.

[25]  V. Amassian,et al.  Modelling magnetic coil excitation of human cerebral cortex with a peripheral nerve immersed in a brain-shaped volume conductor: the significance of fiber bending in excitation. , 1992, Electroencephalography and clinical neurophysiology.

[26]  M Hallett,et al.  Topographic mapping of the human motor cortex with magnetic stimulation: factors affecting accuracy and reproducibility. , 1992, Electroencephalography and clinical neurophysiology.

[27]  Jack L. Lancaster,et al.  A modality‐independent approach to spatial normalization of tomographic images of the human brain , 1995 .

[28]  R Kawashima,et al.  Activity in the human primary motor cortex related to arm and finger movements. , 1995, Neuroreport.

[29]  A. Schleicher,et al.  Two different areas within the primary motor cortex of man , 1996, Nature.

[30]  Mark Hallett,et al.  Locating the Motor Cortex on the MRI with Transcranial Magnetic Stimulation and PET , 1996, NeuroImage.

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

[32]  Alan C. Evans,et al.  Transcranial Magnetic Stimulation during Positron Emission Tomography: A New Method for Studying Connectivity of the Human Cerebral Cortex , 1997, The Journal of Neuroscience.

[33]  Christopher J. Thompson,et al.  Magnetic shielding requirements for PET detectors during transcranial magnetic stimulation , 1997 .

[34]  A P Rudell,et al.  Transcranial magnetic stimulation in study of the visual pathway. , 1998, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[35]  P. Fox,et al.  Global spatial normalization of human brain using convex hulls. , 1999, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[36]  Jack L. Lancaster,et al.  Accurate High-Speed Spatial Normalization Using an Octree Method , 1999, NeuroImage.

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

[38]  Connectivity of the human supplementary motor area (SMA) revealed by concurrent TMS-PET , 2001, NeuroImage.

[39]  Jack L. Lancaster,et al.  Positron emission tomography during transcranial magnetic stimulation does not require μ-metal shielding , 2003, NeuroImage.

[40]  M. Daube-Witherspoon,et al.  Intensity-dependent regional cerebral blood flow during 1-Hz repetitive transcranial magnetic stimulation (rTMS) in healthy volunteers studied with H2 15O positron emission tomography: i. effects of primary motor cortex rTMS , 2003, Biological Psychiatry.

[41]  Jae Sung Lee,et al.  Positron emission tomography during transcranial magnetic stimulation does not require mu-metal shielding. , 2003, NeuroImage.

[42]  Korbinian Brodmann,et al.  Brodmann's localization in the cerebral cortex : the principles of comparative localisation in the cerebral cortex based on cytoarchitectonics , 2006 .