Abstract
Broadband spontaneous macroscopic neural oscillations are rhythmic cortical firing which were extensively examined during the last century, however, their possible origination is still controversial. In this work we show how macroscopic oscillations emerge in solely excitatory random networks and without topological constraints. We experimentally and theoretically show that these oscillations stem from the counterintuitive underlying mechanism—the intrinsic stochastic neuronal response failures (NRFs). These NRFs, which are characterized by short-term memory, lead to cooperation among neurons, resulting in sub- or several- Hertz macroscopic oscillations which coexist with high frequency gamma oscillations. A quantitative interplay between the statistical network properties and the emerging oscillations is supported by simulations of large networks based on single-neuron in-vitro experiments and a Langevin equation describing the network dynamics. Results call for the examination of these oscillations in the presence of inhibition and external drives.
Highlights
We examine a neuron with periodic stimulation trials of 10, 12, and 15 Hz, and neuronal response failures (NRFs) appear after a short transient where the neuron exhibits an increase of its neuronal response latency (NRL) (Figure 1, upper panel)
We have demonstrated that intrinsic NRFs drive a neural network activity toward oscillations, where high frequency oscillations, gamma, and low frequency oscillations, delta and theta, coexist
The high frequency oscillations correspond to the average delay between connected neurons in the network, while low frequency oscillations are governed by statistical properties of the network, e.g., the average number of connections per neuron and the average critical frequency of neurons
Summary
The most widespread cooperative activity of neurons within the cortex is spontaneous macroscopic oscillations (Silva et al, 1991; Gray, 1994; Contreras et al, 1997; Buzsáki and Draguhn, 2004; Chialvo, 2010), which range between sub- and hundred- Hertz (Basar et al, 2001; Brovelli et al, 2004; Buzsáki and Draguhn, 2004; Grillner et al, 2005; Giraud and Poeppel, 2012). It was found that the theta rhythms (Klimesch, 1999; Buzsáki and Draguhn, 2004), oscillations in the range of 4-10 Hz, play a key role in the formation and retrieval of episodic and spatial memory (Hasselmo, 2005). This theta rhythm is usually accompanied by high frequency oscillations in the range of 30-80 Hz, known as gamma oscillations (Colgin and Moser, 2010). Most of the proposed mechanisms are based on the existence of inhibitory synapses
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