Robust information propagation through noisy neural circuits

Sensory neurons give highly variable responses to stimulation, which can limit the amount of stimulus information available to downstream circuits. Much work has investigated the factors that affect the amount of information encoded in these population responses, leading to insights about the role of covariability among neurons, tuning curve shape, etc. However, the informativeness of neural responses is not the only relevant feature of population codes; of potentially equal importance is how robustly that information propagates to downstream structures. For instance, to quantify the retina’s performance, one must consider not only the informativeness of the optic nerve responses, but also the amount of information that survives the spike-generating nonlinearity and noise corruption in the next stage of processing, the lateral geniculate nucleus. Our study identifies the set of covariance structures for the upstream cells that optimize the ability of information to propagate through noisy, nonlinear circuits. Within this optimal family are covariances with “differential correlations”, which are known to reduce the information encoded in neural population activities. Thus, covariance structures that maximize information in neural population codes, and those that maximize the ability of this information to propagate, can be very different. Moreover, redundancy is neither necessary nor sufficient to make population codes robust against corruption by noise: redundant codes can be very fragile, and synergistic codes can—in some cases—optimize robustness against noise.Author summary: Information about the outside world, which originates in sensory neurons, propagates through multiple stages of processing before reaching the neural structures that control behavior. While much work in neuroscience has investigated the factors that affect the amount of information contained in peripheral sensory areas, very little work has asked how much of that information makes it through subsequent processing stages. That’s the focus of this paper, and it’s an important issue because information that fails to propagate cannot be used to affect decision-making. We find a tradeoff between information content and information transmission: neural codes which contain a large amount of information can transmit that information poorly to subsequent processing stages. Thus, the problem of robust information propagation—which has largely been overlooked in previous research—may be critical for determining how our sensory organs communicate with our brains. We identify the conditions under which information propagates well—or poorly—through multiple stages of neural processing.