Temporal coupling of field potentials and action potentials in the neocortex

Abstract

The local field potential (LFP) is an aggregate measure of group neuronal activity and is often correlated with the action potentials of single neurons. In recent years, investigators have found that action potential firing rates increase during elevations in power high-frequency band oscillations (50-200 Hz range). However, action potentials also contribute to the LFP signal itself, making the spike-LFP relationship complex. Here, we examine the relationship between spike rates and LFP in varying frequency bands in rat neocortical recordings. We find that 50-180 Hz oscillations correlate most consistently with high firing rates, but that other LFP bands also carry information relating to spiking, including in some cases anti-correlations. Relatedly, we find that spiking itself and electromyographic activity contribute to LFP power in these bands. The relationship between spike rates and LFP power varies between brain states and between individual cells. Finally, we create an improved oscillation-based predictor of action potential activity by specifically utilizing information from across the entire recorded frequency spectrum of LFP. The findings illustrate both caveats and improvements to be taken into account in attempts to infer spiking activity from LFP.

A causal role for pulvinar in coordinating task independent cortico-cortical interactions

“…Baseline firing rates of neurons in dPL were significantly reduced following muscimol injections (pre-injection: 10.69 ± 1.76 Hz; post-injection: 5.48 ± 1.06 Hz, mean ± s.e.m., n=8; p=0.04, Wilcoxon sign-rank test) but not after control injections (pre-injection: 4.33 ± 0.36 Hz; post-injection: 4.46 ± 0.29 Hz, mean ± s.e.m., n=7; p=0.81, Wilcoxon sign-rank test). We also examined high gamma activity (HGA, 60-90Hz), which is often interpreted as a surrogate for mulit-unit activity (Ray, 2008;Ray, 2011;Watson, 2018). Consistent with the reduction in spike rates, the power of HGA in dPL was significantly reduced, following muscimol injections compared to control sessions (p=0.04, Wilcoxon rank-sum test, 8 muscimol sessions, 7 control sessions).…”

Adaptive Spike-Artifact Removal from Local Field Potentials Uncovers Prominent Beta and Gamma Band Neuronal Synchronization

“…Prior biophysical modeling studies have shown that while spikelocked synaptic effects on the LFP rises sharply, they decay over longer ≥ 10 ms time windows than the duration of action potential repolarization (Schomburg et al, 2012). Furthermore, it is known that Na+ spikes of neurons working coherently, or in an asynchronous regime have afterpotentials that can last 2-20 ms (Fernandez et al, 2005), and spikes can trigger NMDA and Ca+ plateau potentials that are phase-locked to the spike time and prevail in the LFP Watson et al, 2018). These influences will account to different degrees for the slow, non-transient modulation that is visible in many raw spike-LFP triggered spectra.…”

“…see Figure 6, Suppl. 3 and 11 in (Watson et al, 2018)). This is a problem when considering that local cell-to-circuit interactions between neurons can be limited to a <150 µm diameter with spike triggered averages being essentially flat at larger distances of the neuron to the site of LFP recording (Fujisawa et al, 2008).…”

“…However, the close relationship of spiking activity to the LFP can be artifactual when the local field potential activity is contaminated by the action potentials of the spiking neurons themselves as opposed to be based on transmembrane currents from the local circuit Einevoll et al, 2013;Ray, 2015). Such contamination of the LFP can occur for spiking activity of neurons in the immediate surroundings (within ~200 µm) of a recorded neuron (Watson et al, 2018) and becomes evident as spike-bleed through artifacts in spike-triggered LFP averages or as artifactual spike-LFP synchrony, because the LFP phase of the spiking activity is contaminated by the spike itself and thus is not informative beyond the spike time itself. This spike bleed through effect is not only evident for the high frequencies at which the fast action potentials main power reside (around ~0.8-5 kHz), but it can dominate spike-LFP measurements down to ~100 Hz, with lower but discernible contributions for frequencies as low as 25Hz (Ardid et al, 2015;Ray, 2015;Schomburg et al, 2012;Zanos et al, 2011).…”

Interactions between motor thalamic field potentials and single unit spiking predict behavior in rats

“…High gamma power best correlated with 199 directionally selective unit activity, exhibiting roughly zero-lag between spiking and power 200 increases. Therefore, as in cortex, Mthal high gamma power may serve as a surrogate for multi-201 unit activity(Ray et al, 2008;Manning et al, 2009;Watson et al, 2018). 202Mthal single unit activity also showed a small correlation with delta power, which was 203 larger for directionally selective units.…”