Phase-locking of bursting neuronal firing to dominant LFP frequency components

Abstract

Neuronal firing in the hippocampal formation relative to the phase of local field potentials (LFP) has a key role in memory processing and spatial navigation. Firing can be in either tonic or burst mode. Although bursting neurons are common in the hippocampal formation, the characteristics of their locking to LFP phase are not completely understood. We investigated phase-locking properties of bursting neurons using simulations generated by a dual compartmental model of a pyramidal neuron adapted to match the bursting activity in the subiculum of a rat. The model was driven with stochastic input signals containing a power spectral profile consistent with physiologically relevant frequencies observed in LFP. The single spikes and spike bursts fired by the model were locked to a preferred phase of the predominant frequency band where there was a peak in the power of the driving signal. Moreover, the preferred phase of locking shifted with increasing burst size, providing evidence that LFP phase can be encoded by burst size. We also provide initial support for the model results by analysing example data of spontaneous LFP and spiking activity recorded from the subiculum of a single urethane-anaesthetised rat. Subicular neurons fired single spikes, two-spike bursts and larger bursts that locked to a preferred phase of either dominant slow oscillations or theta rhythms within the LFP, according to the model prediction. Both power-modulated phase-locking and gradual shift in the preferred phase of locking as a function of burst size suggest that neurons can use bursts to encode timing information contained in LFP phase into a spike-count code.

Bursting Neurons in the Hippocampal Formation Encode Features of LFP Rhythms

“…Three adult male Sprague Dawley rats and one adult male Wistar rat were used. The experimental procedures for recording from the subiculum have been described before in Constantinou et al (2015). The rats were anesthetized by intraperitoneal injection of 1.5 g/kg urethane.…”

“…Bursting activity was simulated using a two-compartment conductance-based model of a pyramidal neuron which has been used in previous studies (Kamondi et al, 1998; Kepecs et al, 2002; Kepecs and Lisman, 2003; Samengo and Montemurro, 2010; Constantinou et al, 2015). The model contains the minimal ionic conductances required to generate bursting activity (Kepecs and Wang, 2000) after being reduced from a 19-compartment model of a CA3 hippocampal neuron (Traub et al, 1991) to a two-compartment conductance-based model (Pinsky and Rinzel, 1994).…”

“…The input current I ( t ) was injected into a dendritic compartment (Supplementary Equation 1) and bursting activity was recorded from a somatic compartment (Supplementary Equation 2). We had previously adjusted the model parameters (Constantinou et al, 2015) so as to produce single spikes and bursts with the same probability as subicular neurons ( Figures 2A,C ). Burst production by entorhinal neurons was governed by a similar distribution, so we only modified the variance of the input current to adapt the model to entorhinal bursting neurons ( Figures 2B,D ).…”

“…The ~1 Hz rhythm under similar experimental conditions has also been referred to as hippocampal slow oscillations in the literature (Wolansky et al, 2006; Clement et al, 2008). We isolated the epochs with dominant delta rhythms as described in Constantinou et al (2015). In summary, based on the power spectra, the frequency bands for delta and theta rhythms were defined as 0.5–2.5 Hz and 2.5–5.0 Hz, respectively.…”

“…Recent evidence suggests that bursting pyramidal neurons can lock their firing to a preferred phase range of the dominant LFP rhythm and this phase preference can change as a function of burst spike count (Samengo and Montemurro, 2010; Constantinou et al, 2015). Using this idea, computational models have proposed bursting as a mechanism to encode instantaneous features of an oscillating current into a pattern of spikes that can be transmitted to distant areas (Kepecs and Lisman, 2003; Samengo et al, 2013).…”