Abstract

Neuronal circuits in the rodent barrel cortex are characterized by stable low firing rates. However, recent experiments show that short spike trains elicited by electrical stimulation in single neurons can induce behavioral responses. Hence, the underlying neural networks provide stability against internal fluctuations in the firing rate, while simultaneously making the circuits sensitive to small external perturbations. Here we studied whether stability and sensitivity are affected by the connectivity structure in recurrently connected spiking networks. We found that anti-correlation between the number of afferent (in-degree) and efferent (out-degree) synaptic connections of neurons increases stability against pathological bursting, relative to networks where the degrees were either positively correlated or uncorrelated. In the stable network state, stimulation of a few cells could lead to a detectable change in the firing rate. To quantify the ability of networks to detect the stimulation, we used a receiver operating characteristic (ROC) analysis. For a given level of background noise, networks with anti-correlated degrees displayed the lowest false positive rates, and consequently had the highest stimulus detection performance. We propose that anti-correlation in the degree distribution may be a computational strategy employed by sensory cortices to increase the detectability of external stimuli. We show that networks with anti-correlated degrees can in principle be formed by applying learning rules comprised of a combination of spike-timing dependent plasticity, homeostatic plasticity and pruning to networks with uncorrelated degrees. To test our prediction we suggest a novel experimental method to estimate correlations in the degree distribution.

Highlights

  • The distribution for the sum of in- and out-degrees shows that ACOR networks have a tight distribution for the sum of pre- and postsynaptic connections per cell, whereas postively correlated (PCOR) networks show a wide range of values of the summed degrees, with some cells that make few pre- and postsynaptic contacts and others that have many synaptic contacts (Fig. 2C, in Section 4 we relate these differences to metabolic demands on the cell)

  • We studied the mean shortest path between the excitatory neurons, which is the shortest path between two nodes, averaged across all pairs and provides a measure of the effective connectivity in the network

  • We tested whether the mean shortest path length was affected by correlations in the degree distribution and found that for the typical networks used here (480 excitatory neurons and connection probability 0.05), ACOR networks had a significantly longer mean shortest path length, with an increase of 1-2 % compared to PCOR networks (p < 0.001, significance was tested using a two-sided t-test, Fig. 3C)

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Summary

Introduction

A fundamental goal of neuroscience is to elucidate how neural circuits respond to small external inputs, while simultaneously remaining stable against neuronal noise. This is especially a problem for cortical networks producing sparse activity, because weak external inputs involve a number of spikes that is comparable to the number of spikes produced by spontaneous activity. Neuronal noise can arise from intrinsic and extrinsic sources and influences every level of the nervous system (Jacobson et al 2005; Faisal et al 2008). Noise has in some cases been found to limit the information capacity of neurons (Schneidman et al 1998; London et al 2002), but could enhance the computational capability of neurons in other circumstances (Rudolph and Destexhe 2001; Stacey and Durand 2001)

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