Abstract

The hippocampal local field potential (LFP) exhibits a strong correlation with behavior. During rest, the theta rhythm is not prominent, but during active behavior, there are strong rhythms in the theta, theta harmonics, and gamma ranges. With increasing running velocity, theta, theta harmonics and gamma increase in power and in cross-frequency coupling, suggesting that neural entrainment is a direct consequence of the total excitatory input. While it is common to study the parametric range between the LFP and its complementing power spectra between deep rest and epochs of high running velocity, it is also possible to explore how the spectra degrades as the energy is completely quenched from the system. Specifically, it is unknown whether the 1/f slope is preserved as synaptic activity becomes diminished, as low frequencies are generated by large pools of neurons while higher frequencies comprise the activity of more local neuronal populations. To test this hypothesis, we examined rat LFPs recorded from the hippocampus and entorhinal cortex during barbiturate overdose euthanasia. Within the hippocampus, the initial stage entailed a quasi-stationary LFP state with a power-law feature in the power spectral density. In the second stage, there was a successive erosion of power from high- to low-frequencies in the second stage that continued until the only dominant remaining power was <20 Hz. This stage was followed by a rapid collapse of power spectrum toward the absolute electrothermal noise background. As the collapse of activity occurred later in hippocampus compared with medial entorhinal cortex, it suggests that the ability of a neural network to maintain the 1/f slope with decreasing energy is a function of general connectivity. Broadly, these data support the energy cascade theory where there is a cascade of energy from large cortical populations into smaller loops, such as those that supports the higher frequency gamma rhythm. As energy is pulled from the system, neural entrainment at gamma frequency (and higher) decline first. The larger loops, comprising a larger population, are fault-tolerant to a point capable of maintaining their activity before a final collapse.

Highlights

  • It has been evident that hippocampal localfield potential (LFP) activity is strongly correlated with behavior (Vanderwolf, 1969; Buzsaki, 2005)

  • As to rat 730 and rat 782, another probe was implanted in the medial entorhinal cortex (MEC)

  • A sample of hippocampal LFP from stage 1 (Figure 1B) reveals that theta can express significant deviations from a sinusoid (Buzsaki et al, 1983; Terrazas et al, 2005). This non-sinusoidal waveform is related to high order theta harmonics due to the non-linearity of hippocampal LFP (Scheffer-Teixeira and Tort, 2016; Sheremet et al, 2016; Zhou et al, 2019)

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Summary

Introduction

It has been evident that hippocampal localfield potential (LFP) activity is strongly correlated with behavior (Vanderwolf, 1969; Buzsaki, 2005). The increase in gamma power at faster running speeds is associated with enhanced theta-gamma coupling (Sheremet et al, 2018). The power spectra density takes the form of Amplitude = 1/frequency^α, where alpha falls is a value between zero and two (characteristic of a pink noise spectra; Buzsaki, 2006). While this decomposition treats different frequency bands as independent signals, the theta and gamma oscillations are not isolated rhythms. Similar to theta and gamma, the slope of the spectra that is attributed to the background has been found to change with increasing running speed (Sheremet et al, 2019b), suggesting that it is sensitive to increased synaptic currents and may be interrelated with the rhythms that are often ascribed as being independent from the background spectra

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