High-Fidelity Coding with Correlated Neurons

Positive correlations in the activity of neurons are widely observed in the brain. Previous studies have shown these correlations to be detrimental to the fidelity of population codes, or at best marginally favorable compared to independent codes. Here, we show that positive correlations can enhance coding performance by astronomical factors. Specifically, the probability of discrimination error can be suppressed by many orders of magnitude. Likewise, the number of stimuli encoded—the capacity—can be enhanced more than tenfold. These effects do not necessitate unrealistic correlation values, and can occur for populations with a few tens of neurons. We further show that both effects benefit from heterogeneity commonly seen in population activity. Error suppression and capacity enhancement rest upon a pattern of correlation. Tuning of one or several effective parameters can yield a limit of perfect coding: the corresponding pattern of positive correlation leads to a ‘lock-in’ of response probabilities that eliminates variability in the subspace relevant for stimulus discrimination. We discuss the nature of this pattern and we suggest experimental tests to identify it.Author Summary: Traditionally, sensory neuroscience has focused on correlating inputs from the physical world with the response of a single neuron. Two stimuli can be distinguished solely from the response of one neuron if one stimulus elicits a response and the other does not. But as soon as one departs from extremely simple stimuli, single-cell coding becomes less effective, because cells often respond weakly and unreliably. High fidelity coding then relies upon populations of cells, and correlation among those cells can greatly affect the neural code. While previous theoretical studies have demonstrated a potential coding advantage of correlation, they allowed only a marginal improvement in coding power. Here, we present a scenario in which a pattern of correlation among neurons in a population yields an improvement in coding performance by several orders of magnitude. By “improvement” we mean that a neural population is much better at both distinguishing stimuli and at encoding a large number of them. The scenario we propose does not invoke unrealistic values of correlation. What is more, it is even effective for small neural populations and in subtle cases in which single-cell coding fails utterly. These results demonstrate a previously unappreciated potential for correlated population coding.