Anti-correlations in the degree distribution increase stimulus detection performance in noisy spiking neural networks

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. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1007/s10827-016-0629-1) contains supplementary material, which is available to authorized users.