Influence of spiking activity on cortical local field potentials

•  The intra‐cortical local field potential (LFP) reflects a variety of electrophysiological processes and is a fundamental signal used to enhance knowledge about neuroscience. •  For most investigations, spike‐free LFPs are mandatory for valid conclusions, but spikes can contaminate LFPs and falsify findings despite low‐pass filtering or other attempts to remove spiking activity from LFPs. The extent of this fundamental problem remains unclear. •  Using spikes recorded in the awake monkey, we revealed how spike amplitude, spike duration, firing rate and noise statistic influence the extent to which spikes contaminate LFPs. •  Contamination varies with these parameters and can affect LFPs down to around 10 Hz; below this it is theoretically possible but unlikely. LFP frequencies up to the (high‐) gamma band can remain unaffected, but signals above must always be carefully analysed. •  We propose a method to reveal modulations in spectrograms, which also allows the detection of spike contamination, and provide a systematic guide to assess spike contamination of intra‐cortical LFPs.

[1]  John P. Donoghue,et al.  Decoding 3-D Reach and Grasp Kinematics From High-Frequency Local Field Potentials in Primate Primary Motor Cortex , 2010, IEEE Transactions on Biomedical Engineering.

[2]  J. Maunsell,et al.  Different Origins of Gamma Rhythm and High-Gamma Activity in Macaque Visual Cortex , 2011, PLoS biology.

[3]  Stephen V. David,et al.  Decoupling Action Potential Bias from Cortical Local Field Potentials , 2010, Comput. Intell. Neurosci..

[4]  N. Logothetis,et al.  In Vivo Measurement of Cortical Impedance Spectrum in Monkeys: Implications for Signal Propagation , 2007, Neuron.

[5]  R P Lesser,et al.  Functional significance of the mu rhythm of human cortex: an electrophysiologic study with subdural electrodes. , 1993, Electroencephalography and clinical neurophysiology.

[6]  Paul Ferrari,et al.  Self-paced movements induce high-frequency gamma oscillations in primary motor cortex , 2008, NeuroImage.

[7]  Antonio Pesce Is Decoupling in action , 2015 .

[8]  José del R. Millán,et al.  Very high frequency oscillations (VHFO) as a predictor of movement intentions , 2006, NeuroImage.

[9]  Yali Amit,et al.  Single-unit stability using chronically implanted multielectrode arrays. , 2009, Journal of neurophysiology.

[10]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[11]  James P. Evans The Origin , 2009, Genetics in Medicine.

[12]  R. Quian Quiroga,et al.  Unsupervised Spike Detection and Sorting with Wavelets and Superparamagnetic Clustering , 2004, Neural Computation.

[13]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[14]  Christof Koch,et al.  The Spiking Component of Oscillatory Extracellular Potentials in the Rat Hippocampus , 2012, The Journal of Neuroscience.

[15]  Robert C. Liu,et al.  Predicting stimulus-locked single unit spiking from cortical local field potentials , 2010, Journal of Computational Neuroscience.

[16]  A. Schwartz,et al.  Recording from the same neurons chronically in motor cortex. , 2012, Journal of neurophysiology.

[17]  Gabriel Curio,et al.  Are high-frequency (600Hz) oscillations in human somatosensory evoked potentials due to phase-resetting phenomena? , 2012, Clinical Neurophysiology.

[18]  Alexander Kraskov,et al.  M1 Corticospinal Mirror Neurons and Their Role in Movement Suppression during Action Observation , 2013, Current Biology.

[19]  P. Nunez,et al.  Electric fields of the brain , 1981 .

[20]  E. Fetz,et al.  Compact movable microwire array for long-term chronic unit recording in cerebral cortex of primates. , 2007, Journal of neurophysiology.

[21]  N. Logothetis The Underpinnings of the BOLD Functional Magnetic Resonance Imaging Signal , 2003, The Journal of Neuroscience.

[22]  J.P. Donoghue,et al.  Reliability of signals from a chronically implanted, silicon-based electrode array in non-human primate primary motor cortex , 2005, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[23]  J. Haueisen,et al.  Multiplicity in the high-frequency signals during the short-latency somatosensory evoked cortical activity in humans , 2001, Clinical Neurophysiology.

[24]  E. Whitham,et al.  Scalp electrical recording during paralysis: Quantitative evidence that EEG frequencies above 20Hz are contaminated by EMG , 2007, Clinical Neurophysiology.

[25]  R. Schmidt,et al.  Cross-Frequency Phase–Phase Coupling between Theta and Gamma Oscillations in the Hippocampus , 2012, The Journal of Neuroscience.

[26]  Stavros Zanos,et al.  Relationships between spike-free local field potentials and spike timing in human temporal cortex. , 2012, Journal of neurophysiology.

[27]  J. Wolpaw,et al.  Decoding two-dimensional movement trajectories using electrocorticographic signals in humans , 2007, Journal of neural engineering.

[28]  G. Buzsáki,et al.  Intrinsic Circuit Organization and Theta–Gamma Oscillation Dynamics in the Entorhinal Cortex of the Rat , 2010, The Journal of Neuroscience.

[29]  C. Mehring,et al.  Inference of hand movements from local field potentials in monkey motor cortex , 2003, Nature Neuroscience.

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

[31]  E. Niebur,et al.  Neural Correlates of High-Gamma Oscillations (60–200 Hz) in Macaque Local Field Potentials and Their Potential Implications in Electrocorticography , 2008, The Journal of Neuroscience.

[32]  K. H. Britten,et al.  Power spectrum analysis of bursting cells in area MT in the behaving monkey , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  Max A. Little,et al.  Exploiting Nonlinear Recurrence and Fractal Scaling Properties for Voice Disorder Detection , 2007, Biomedical engineering online.

[34]  C. Braun,et al.  Hand Movement Direction Decoded from MEG and EEG , 2008, The Journal of Neuroscience.

[35]  Theodoros P. Zanos,et al.  Removal of spurious correlations between spikes and local field potentials. , 2011, Journal of neurophysiology.

[36]  C. Braun,et al.  A review on directional information in neural signals for brain-machine interfaces , 2009, Journal of Physiology-Paris.

[37]  Ernst Niebur,et al.  Effect of Stimulus Intensity on the Spike–Local Field Potential Relationship in the Secondary Somatosensory Cortex , 2008, The Journal of Neuroscience.

[38]  G. Pfurtscheller Functional Topography During Sensorimotor Activation Studied with Event‐Related Desynchronization Mapping , 1989, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.