Spatial consistency of neural firing regulates long-range local field potential synchronization: A computational study

Local field potentials (LFPs) are thought to integrate neuronal processes within the range of a few millimeters of radius, which corresponds to the scale of multiple columns. In this study, the model of LFP in the visual cortex proposed by Mazzoni et al. (2008) was adapted to organize a network of two cortical areas, in which pyramidal neurons were divided into two sub-population modeling columns with spatially organized connections to neurons in other areas. Using the model enabled the relationship between neural firing and LFP to be evaluated, in addition to the LFP coherence between the two areas. Results showed that: (1) neurons in a particular sub-population generated the LFP in the area; (2) the spatial consistency of neural firing in the two areas was strongly correlated with LFP coherence; and (3) this consistency was capable of regulating LFP coherence in a lower frequency band, which was originally introduced to neurons in a particular sub-population. These results were derived from a winner-take-all operation in the columnar structure; thus, they are expected to be common in the cortex. It is suggested that the spatial consistency of neural firing is essential for regulating long-range LFP synchronization, which would facilitate neuronal integration processes over multiple cortical areas.

[1]  Michael E. Hasselmo,et al.  A Proposed Function for Hippocampal Theta Rhythm: Separate Phases of Encoding and Retrieval Enhance Reversal of Prior Learning , 2002, Neural Computation.

[2]  Manuel Schabus,et al.  Fronto-parietal EEG coherence in theta and upper alpha reflect central executive functions of working memory. , 2005, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[3]  M. Carandini,et al.  Local Origin of Field Potentials in Visual Cortex , 2009, Neuron.

[4]  M. Carandini,et al.  Stimulus contrast modulates functional connectivity in visual cortex , 2009, Nature Neuroscience.

[5]  N. Logothetis,et al.  Frequency-Band Coupling in Surface EEG Reflects Spiking Activity in Monkey Visual Cortex , 2009, Neuron.

[6]  Jeremy R. Manning,et al.  Broadband Shifts in Local Field Potential Power Spectra Are Correlated with Single-Neuron Spiking in Humans , 2009, The Journal of Neuroscience.

[7]  I. Fried,et al.  Coupling between Neuronal Firing Rate, Gamma LFP, and BOLD fMRI Is Related to Interneuronal Correlations , 2007, Current Biology.

[8]  P Rappelsberger,et al.  Long-range EEG synchronization during word encoding correlates with successful memory performance. , 2000, Brain research. Cognitive brain research.

[9]  Gustavo Deco,et al.  Optimal Information Transfer in the Cortex through Synchronization , 2010, PLoS Comput. Biol..

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

[11]  R. Traub,et al.  A mechanism for generation of long-range synchronous fast oscillations in the cortex , 1996, Nature.

[12]  Klas H. Pettersen,et al.  Modeling the Spatial Reach of the LFP , 2011, Neuron.

[13]  Xiao-Jing Wang,et al.  Erratum to: Effects of neuromodulation in a cortical network model of object working memory dominated by recurrent inhibition , 2014, Journal of Computational Neuroscience.

[14]  Naoyuki Sato,et al.  Theta synchronization networks emerge during human object–place memory encoding , 2007, Neuroreport.

[15]  Xiao-Jing Wang,et al.  What determines the frequency of fast network oscillations with irregular neural discharges? I. Synaptic dynamics and excitation-inhibition balance. , 2003, Journal of neurophysiology.

[16]  G. Ermentrout,et al.  Gamma rhythms and beta rhythms have different synchronization properties. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[17]  N. Logothetis,et al.  Phase-of-Firing Coding of Natural Visual Stimuli in Primary Visual Cortex , 2008, Current Biology.

[18]  N. Sato Fast entrainment of human electroencephalogram to a theta-band photic flicker during successful memory encoding , 2013, Front. Hum. Neurosci..

[19]  A. Aertsen,et al.  Beyond the Cortical Column: Abundance and Physiology of Horizontal Connections Imply a Strong Role for Inputs from the Surround , 2011, Front. Neurosci..

[20]  Ben H. Jansen,et al.  Electroencephalogram and visual evoked potential generation in a mathematical model of coupled cortical columns , 1995, Biological Cybernetics.

[21]  E. Brown,et al.  Thalamocortical model for a propofol-induced α-rhythm associated with loss of consciousness , 2010, Proceedings of the National Academy of Sciences.

[22]  F. Varela,et al.  Perception's shadow: long-distance synchronization of human brain activity , 1999, Nature.

[23]  Marcelo A. Montemurro,et al.  Spike-Phase Coding Boosts and Stabilizes Information Carried by Spatial and Temporal Spike Patterns , 2009, Neuron.

[24]  W. Newsome,et al.  The Variable Discharge of Cortical Neurons: Implications for Connectivity, Computation, and Information Coding , 1998, The Journal of Neuroscience.

[25]  Nicolas Brunel,et al.  Encoding of Naturalistic Stimuli by Local Field Potential Spectra in Networks of Excitatory and Inhibitory Neurons , 2008, PLoS Comput. Biol..

[26]  C. Koch,et al.  The origin of extracellular fields and currents — EEG, ECoG, LFP and spikes , 2012, Nature Reviews Neuroscience.

[27]  Nicolas Brunel,et al.  Author's Personal Copy Understanding the Relationships between Spike Rate and Delta/gamma Frequency Bands of Lfps and Eegs Using a Local Cortical Network Model , 2022 .

[28]  J. Pernier,et al.  Oscillatory γ-Band (30–70 Hz) Activity Induced by a Visual Search Task in Humans , 1997, The Journal of Neuroscience.

[29]  Arthur Gretton,et al.  Low-Frequency Local Field Potentials and Spikes in Primary Visual Cortex Convey Independent Visual Information , 2008, The Journal of Neuroscience.

[30]  G. Karmos,et al.  Entrainment of Neuronal Oscillations as a Mechanism of Attentional Selection , 2008, Science.

[31]  M. Tsodyks,et al.  Synaptic Theory of Working Memory , 2008, Science.

[32]  Xiao-Jing Wang Neurophysiological and computational principles of cortical rhythms in cognition. , 2010, Physiological reviews.

[33]  T. Poggio,et al.  Object Selectivity of Local Field Potentials and Spikes in the Macaque Inferior Temporal Cortex , 2006, Neuron.

[34]  P. Fries A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

[35]  R. Ilmoniemi,et al.  Magnetoencephalography-theory, instrumentation, and applications to noninvasive studies of the working human brain , 1993 .

[36]  R. Shapley,et al.  LFP power spectra in V1 cortex: the graded effect of stimulus contrast. , 2005, Journal of neurophysiology.

[37]  Kevan A. C. Martin,et al.  Canonical cortical circuits , 2010 .

[38]  J. Martinerie,et al.  The brainweb: Phase synchronization and large-scale integration , 2001, Nature Reviews Neuroscience.

[39]  R. Knight,et al.  The functional role of cross-frequency coupling , 2010, Trends in Cognitive Sciences.