Model of low-pass filtering of local field potentials in brain tissue.

Local field potentials (LFPs) are routinely measured experimentally in brain tissue, and exhibit strong low-pass frequency filtering properties, with high frequencies (such as action potentials) being visible only at very short distances (approximately 10 microm) from the recording electrode. Understanding this filtering is crucial to relate LFP signals with neuronal activity, but not much is known about the exact mechanisms underlying this low-pass filtering. In this paper, we investigate a possible biophysical mechanism for the low-pass filtering properties of LFPs. We investigate the propagation of electric fields and its frequency dependence close to the current source, i.e., at length scales in the order of average interneuronal distances. We take into account the presence of a high density of cellular membranes around current sources, such as glial cells. By considering them as passive cells, we show that under the influence of the electric source field, they respond by polarization. Because of the finite velocity of ionic charge movements, this polarization will not be instantaneous. Consequently, the induced electric field will be frequency-dependent, and much reduced for high frequencies. Our model establishes that this situation is analogous to an equivalent RC circuit, or better yet a system of coupled RC circuits. We present a number of numerical simulations of an induced electric field for biologically realistic values of parameters, and show the frequency filtering effect as well as the attenuation of extracellular potentials with distance. We suggest that induced electric fields in passive cells surrounding neurons are the physical origin of frequency filtering properties of LFPs. Experimentally testable predictions are provided allowing us to verify the validity of this model.

[1]  J. B. Ranck,et al.  Specific impedance of rabbit cerebral cortex. , 1963, Experimental neurology.

[2]  G. Shepherd,et al.  Theoretical reconstruction of field potentials and dendrodendritic synaptic interactions in olfactory bulb. , 1968, Journal of neurophysiology.

[3]  J. Christensen Doctoral thesis , 1970 .

[4]  Sanford L. Palay,et al.  The fine structure of the nervous system , 1976 .

[5]  W Rall,et al.  Computed potentials of cortically arranged populations of neurons. , 1977, Journal of neurophysiology.

[6]  B. Hille Ionic channels of excitable membranes , 2001 .

[7]  F W Sharbrough,et al.  Computer simulation of neuronal circuit models of rhythmic behavior in the electroencephalogram. , 1988, Computers in biology and medicine.

[8]  T. Bullock,et al.  Lateral coherence of the electrocorticogram: a new measure of brain synchrony. , 1989, Electroencephalography and clinical neurophysiology.

[9]  W. Singer,et al.  Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[10]  D. Apps,et al.  Ionic channels of excitable membranes (second edition) : By Bertil Hille; Sinauer Associates (distributed by W.H. Freeman); Sunderland, MA, 1992; xiv + 607 pages. £37.95. ISBN 0878933239 , 1992 .

[11]  P. Nunez,et al.  Neocortical Dynamics and Human EEG Rhythms , 1995 .

[12]  M. Steriade,et al.  Intracortical and corticothalamic coherency of fast spontaneous oscillations. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[13]  A. Destexhe Spike-and-Wave Oscillations Based on the Properties of GABAB Receptors , 1998, The Journal of Neuroscience.

[14]  Prof. Dr. Dr. Valentino Braitenberg,et al.  Cortex: Statistics and Geometry of Neuronal Connectivity , 1998, Springer Berlin Heidelberg.

[15]  Mnh,et al.  Histologie du Système Nerveux de Lʼhomme et des Vertébrés , 1998 .

[16]  P. Achermann,et al.  Coherence analysis of the human sleep electroencephalogram , 1998, Neuroscience.

[17]  S. J. Salon,et al.  Numerical Methods in Electromagnetism , 1999 .

[18]  D. Contreras,et al.  Spatiotemporal Analysis of Local Field Potentials and Unit Discharges in Cat Cerebral Cortex during Natural Wake and Sleep States , 1999, The Journal of Neuroscience.

[19]  L. Garey Cortex: Statistics and Geometry of Neuronal Connectivity, 2nd edn. By V. BRAITENBERG and A. SCHÜZ. (Pp. xiii+249; 90 figures; ISBN 3 540 63816 4). Berlin: Springer. 1998. , 1999 .

[20]  勇一 作村,et al.  Biophysics of Computation , 2001 .

[21]  C. Bédard,et al.  Modeling extracellular field potentials and the frequency-filtering properties of extracellular space. , 2003, Biophysical journal.

[22]  R. Eckhorn,et al.  Coherent oscillations: A mechanism of feature linking in the visual cortex? , 1988, Biological Cybernetics.

[23]  宁北芳,et al.  疟原虫var基因转换速率变化导致抗原变异[英]/Paul H, Robert P, Christodoulou Z, et al//Proc Natl Acad Sci U S A , 2005 .