Neuronal response impedance mechanism implementing cooperative networks with low firing rates and μs precision.

Roni Vardi,Haya Brama,Edward A. Stern,Hagar Marmari,Shira Sardi,Pinhas Sabo,Amir Goldental,Ido Kanter

doi:10.3389/fncir.2015.00029

Abstract

Realizations of low firing rates in neural networks usually require globally balanced distributions among excitatory and inhibitory links, while feasibility of temporal coding is limited by neuronal millisecond precision. We show that cooperation, governing global network features, emerges through nodal properties, as opposed to link distributions. Using in vitro and in vivo experiments we demonstrate microsecond precision of neuronal response timings under low stimulation frequencies, whereas moderate frequencies result in a chaotic neuronal phase characterized by degraded precision. Above a critical stimulation frequency, which varies among neurons, response failures were found to emerge stochastically such that the neuron functions as a low pass filter, saturating the average inter-spike-interval. This intrinsic neuronal response impedance mechanism leads to cooperation on a network level, such that firing rates are suppressed toward the lowest neuronal critical frequency simultaneously with neuronal microsecond precision. Our findings open up opportunities of controlling global features of network dynamics through few nodes with extreme properties.

Highlights

The attempt to understand high cognitive functionalities and cooperative activities of neurons within a network results in many open questions
Stabilization of the Neuronal Response Latency When a neuron is repeatedly stimulated its response latency, neuronal response latency (NRL), stretches gradually. This effect was demonstrated for a 30 Hz stimulation frequency (Figure 1A) using cultured cortical neurons functionally separated from their network by synaptic blockers and stimulated such that most stimulations resulted in an evoked spike (Materials and Methods)
The low firing rate for a given neural network topology was achieved in simulations using specific distributions of excitatory and inhibitory synapses, which balance spike birth and death trends

Summary

Introduction

The attempt to understand high cognitive functionalities and cooperative activities of neurons within a network results in many open questions. The second puzzle is the realization of precise neuronal response timings on a network level (Vanrullen et al, 2005; Butts et al, 2007; Panzeri et al, 2010), whereas their variations are typically in the order of several milliseconds (Lass and Abeles, 1975; Mainen and Sejnowski, 1995; Schoppa and Westbrook, 1999; Foust et al, 2010). This realization is a prerequisite for the feasibility of temporal codes, which might play a role in brain functionalities. In this work we demonstrate that network low firing rates and neuronal precise response timings both stem from a single neuronal property, the neuronal response impedance mechanism, which counter-intuitively leads to cooperation among individual neurons comprising a network.

Methods

Results

Conclusion