When Response Variability Increases Neural Network Robustness to Synaptic Noise

Cortical sensory neurons are known to be highly variable, in the sense that responses evoked by identical stimuli often change dramatically from trial to trial. The origin of this variability is uncertain, but it is usually interpreted as detrimental noise that reduces the computational accuracy of neural circuits. Here we investigate the possibility that such response variability might in fact be beneficial, because it may partially compensate for a decrease in accuracy due to stochastic changes in the synaptic strengths of a network. We study the interplay between two kinds of noise, response (or neuronal) noise and synaptic noise, by analyzing their joint influence on the accuracy of neural networks trained to perform various tasks. We find an interesting, generic interaction: when fluctuations in the synaptic connections are proportional to their strengths (multiplicative noise), a certain amount of response noise in the input neurons can significantly improve network performance, compared to the same network without response noise. Performance is enhanced because response noise and multiplicative synaptic noise are in some ways equivalent. So if the algorithm used to find the optimal synaptic weights can take into account the variability of the model neurons, it can also take into account the variability of the synapses. Thus, the connection patterns generated with response noise are typically more resistant to synaptic degradation than those obtained without response noise. As a consequence of this interplay, if multiplicative synaptic noise is present, it is better to have response noise in the network than not to have it. These results are demonstrated analytically for the most basic network consisting of two input neurons and one output neuron performing a simple classification task, but computer simulations show that the phenomenon persists in a wide range of architectures, including recurrent (attractor) networks and sensorimotor networks that perform coordinate transformations. The results suggest that response variability could play an important dynamic role in networks that continuously learn.