Modeling the effect of dendritic input location on MEG and EEG source dipoles

The cerebral sources of magneto- and electroencephalography (MEG, EEG) signals can be represented by current dipoles. We used computational modeling of realistically shaped passive-membrane dendritic trees of pyramidal cells from the human cerebral cortex to examine how the spatial distribution of the synaptic inputs affects the current dipole. The magnitude of the total dipole moment vector was found to be proportional to the vertical location of the synaptic input. The dipole moment had opposite directions for inputs above and below a reversal point located near the soma. Inclusion of shunting-type inhibition either suppressed or enhanced the current dipole, depending on whether the excitatory and inhibitory synapses were on the same or opposite side of the reversal point. Relating the properties of the macroscopic current dipoles to dendritic current distributions can help to provide means for interpreting MEG and EEG data in terms of synaptic connection patterns within cortical areas.

[1]  K. Rockland,et al.  Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey , 1979, Brain Research.

[2]  Klas H. Pettersen,et al.  Amplitude variability and extracellular low-pass filtering of neuronal spikes. , 2008, Biophysical journal.

[3]  G. Stuart,et al.  Role of dendritic synapse location in the control of action potential output , 2003, Trends in Neurosciences.

[4]  John J. Foxe,et al.  The timing and laminar profile of converging inputs to multisensory areas of the macaque neocortex. , 2002, Brain research. Cognitive brain research.

[5]  Koji Inui,et al.  Temporal analysis of the flow from V1 to the extrastriate cortex in humans. , 2006, Journal of neurophysiology.

[6]  Michele Migliore,et al.  Realistic simulations of neuronal activity: A contribution to the debate on direct detection of neuronal currents by MRI , 2008, NeuroImage.

[7]  Stephen Perrig,et al.  Spatiotemporal scales and links between electrical neuroimaging modalities , 2011, Medical & Biological Engineering & Computing.

[8]  J. Allman,et al.  Dendritic architecture of the von Economo neurons , 2006, Neuroscience.

[9]  G. Shepherd,et al.  Emerging rules for the distributions of active dendritic conductances , 2002, Nature Reviews Neuroscience.

[10]  N. Spruston,et al.  Determinants of Voltage Attenuation in Neocortical Pyramidal Neuron Dendrites , 1998, The Journal of Neuroscience.

[11]  Herbert G. Vaughan,et al.  THE NEURAL ORIGINS OF HUMAN EVENT‐RELATED POTENTIALS * , 1980 .

[12]  I Segev,et al.  Signal delay and input synchronization in passive dendritic structures. , 1993, Journal of neurophysiology.

[13]  Karl J. Friston,et al.  The Dynamic Brain: From Spiking Neurons to Neural Masses and Cortical Fields , 2008, PLoS Comput. Biol..

[14]  R. Llinás The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. , 1988, Science.

[15]  Aina Puce,et al.  Category-sensitive excitatory and inhibitory processes in human extrastriate cortex. , 2002, Journal of neurophysiology.

[16]  Y. Okada,et al.  Contribution of Ionic Currents to Magnetoencephalography (MEG) and Electroencephalography (EEG) Signals Generated by Guinea‐Pig CA3 Slices , 2003, The Journal of physiology.

[17]  Mina Teicher,et al.  EEG generator--a model of potentials in a volume conductor. , 2009, Journal of neurophysiology.

[18]  Suzanne Tyč-Dumont,et al.  Electrical Dynamics of the Dendritic Space , 2010 .

[19]  I Segev,et al.  Untangling dendrites with quantitative models. , 2000, Science.

[20]  T. L. Hayes,et al.  Magnopyramidal neurons in the anterior motor speech region. Dendritic features and interhemispheric comparisons. , 1996, Archives of neurology.

[21]  Ivica Kostović,et al.  Perinatal growth of prefrontal layer III pyramids in Down syndrome. , 2002, Pediatric neurology.

[22]  Nicholas T. Carnevale,et al.  The NEURON Simulation Environment , 1997, Neural Computation.

[23]  T. Poggio,et al.  Nonlinear interactions in a dendritic tree: localization, timing, and role in information processing. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[24]  Bin Chen,et al.  Modeling neuronal current MRI signal with human neuron , 2011, Magnetic resonance in medicine.

[25]  Helen Barbas,et al.  The Prefrontal Cortex and Flexible Behavior , 2007, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[26]  Dominique L. Pritchett,et al.  Quantitative analysis and biophysically realistic neural modeling of the MEG mu rhythm: rhythmogenesis and modulation of sensory-evoked responses. , 2009, Journal of neurophysiology.

[27]  K. Svoboda,et al.  The subcellular organization of neocortical excitatory connections , 2009, Nature.

[28]  U. Mitzdorf Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. , 1985, Physiological reviews.

[29]  E. Halgren,et al.  Spatiotemporal dynamics of neocortical excitation and inhibition during human sleep , 2012, Proceedings of the National Academy of Sciences.

[30]  Karl J. Friston,et al.  A neural mass model for MEG/EEG: coupling and neuronal dynamics , 2003, NeuroImage.

[31]  Gaute T. Einevoll,et al.  Intrinsic dendritic filtering gives low-pass power spectra of local field potentials , 2010, Journal of Computational Neuroscience.

[32]  Bradley J. Roth,et al.  Is it possible to detect dendrite currents using presently available magnetic resonance imaging techniques? , 2012, Medical & Biological Engineering & Computing.

[33]  R. Lorente de Nó,et al.  Action potential of the motoneurons of the hypoglossus nucleus. , 1947, Journal of cellular and comparative physiology.

[34]  Idan Segev,et al.  Compartmental models of complex neurons , 1989 .

[35]  M. Häusser,et al.  Estimating the Time Course of the Excitatory Synaptic Conductance in Neocortical Pyramidal Cells Using a Novel Voltage Jump Method , 1997, The Journal of Neuroscience.

[36]  Erik De Schutter,et al.  Computational Modeling Methods for Neuroscientists , 2009 .

[37]  Vivien A. Casagrande,et al.  Biophysics of Computation: Information Processing in Single Neurons , 1999 .

[38]  S. J. Williamson,et al.  Spatial extent of coherent sensory-evoked cortical activity , 2004, Experimental Brain Research.

[39]  Dominique L. Pritchett,et al.  Neural Correlates of Tactile Detection: A Combined Magnetoencephalography and Biophysically Based Computational Modeling Study , 2007, The Journal of Neuroscience.

[40]  John D. Van Horn,et al.  Source cancellation profiles of electroencephalography and magnetoencephalography , 2012, NeuroImage.

[41]  J Rinzel,et al.  Branch input resistance and steady attenuation for input to one branch of a dendritic neuron model. , 1973, Biophysical journal.

[42]  Y. Okada,et al.  Genesis of MEG signals in a mammalian CNS structure. , 1997, Electroencephalography and clinical neurophysiology.

[43]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[44]  Seppo P. Ahlfors,et al.  Sensitivity of MEG and EEG to Source Orientation , 2010, Brain Topography.

[45]  William R. Holmes,et al.  Passive Cable Modeling , 2009 .

[46]  Ratko Magjarevic,et al.  Neurodynamic measures of functional connectivity and cognition , 2011, Medical & Biological Engineering & Computing.

[47]  Martin Burghoff,et al.  Neuronal current detection with low-field magnetic resonance: simulations and methods. , 2009, Magnetic resonance imaging.

[48]  H G Vaughan,et al.  THE NEURAL ORIGINS OF HUMAN EVENT‐RELATED POTENTIALS * , 1980, Annals of the New York Academy of Sciences.

[49]  Richard H. Bayford,et al.  A cable theory based biophysical model of resistance change in crab peripheral nerve and human cerebral cortex during neuronal depolarisation: implications for electrical impedance tomography of fast neural activity in the brain , 2012, Medical & Biological Engineering & Computing.

[50]  L. Cauller Layer I of primary sensory neocortex: where top-down converges upon bottom-up , 1995, Behavioural Brain Research.

[51]  Arjen van Ooyen,et al.  The effect of dendritic topology on firing patterns in model neurons , 2002, Network.

[52]  K Reinikainen,et al.  [Physical basis of the generation of neuromagnetic fields]. , 1985, Biofizika.

[53]  Y. Okada,et al.  Physiological origins of evoked magnetic fields and extracellular field potentials produced by guinea‐pig CA3 hippocampal slices , 2002, The Journal of physiology.

[54]  Adriaan van Oosterom,et al.  The inverse problem of bioelectricity: an evaluation , 2012, Medical & Biological Engineering & Computing.

[55]  M. Häusser,et al.  The single dendritic branch as a fundamental functional unit in the nervous system , 2010, Current Opinion in Neurobiology.

[56]  Andrew R. Mayer,et al.  Modelling the magnetic signature of neuronal tissue , 2007, NeuroImage.

[57]  W. J. Nowack Neocortical Dynamics and Human EEG Rhythms , 1995, Neurology.

[58]  Fernando H. Lopes da Silva Electrophysiological Basis of MEG Signals , 2010 .

[59]  E. Halgren,et al.  Cancellation of EEG and MEG signals generated by extended and distributed sources , 2009, Human brain mapping.

[60]  Matti Hämäläinen,et al.  Handbook of Neural Activity Measurement: MEG and EEG: source estimation , 2012 .

[61]  T. Sejnowski,et al.  [Letters to nature] , 1996, Nature.

[62]  N. Spruston Pyramidal neurons: dendritic structure and synaptic integration , 2008, Nature Reviews Neuroscience.

[63]  Eric Halgren,et al.  Magnetoencephalography ( Neuromagnetism ) , 2003 .

[64]  Gaute T. Einevoll,et al.  Frequency Dependence of Signal Power and Spatial Reach of the Local Field Potential , 2013, PLoS Comput. Biol..

[65]  William Sutherling,et al.  Current source-density and neuromagnetic analysis of the direct cortical response in rat cortex , 1988, Brain Research.

[66]  Y. Okada,et al.  Contributions of principal neocortical neurons to magnetoencephalography and electroencephalography signals , 2006, The Journal of physiology.

[67]  István Ulbert,et al.  Processing stages underlying word recognition in the anteroventral temporal lobe , 2006, NeuroImage.

[68]  Michael W. Reimann,et al.  A Biophysically Detailed Model of Neocortical Local Field Potentials Predicts the Critical Role of Active Membrane Currents , 2013, Neuron.

[69]  F. H. Lopes da Silva,et al.  Biophysical aspects of EEG and magnetoencephalogram generation , 1998 .

[70]  Seppo P. Ahlfors,et al.  Direction of magnetoencephalography sources associated with feedback and feedforward contributions in a visual object recognition task , 2015, Neuroscience Letters.

[71]  Michael L. Hines,et al.  The NEURON Book , 2006 .

[72]  W. Rall Cable theory for dendritic neurons , 1989 .