How Do Efficient Coding Strategies Depend on Origins of Noise in Neural Circuits?

Neural circuits reliably encode and transmit signals despite the presence of noise at multiple stages of processing. The efficient coding hypothesis, a guiding principle in computational neuroscience, suggests that a neuron or population of neurons allocates its limited range of responses as efficiently as possible to best encode inputs while mitigating the effects of noise. Previous work on this question relies on specific assumptions about where noise enters a circuit, limiting the generality of the resulting conclusions. Here we systematically investigate how noise introduced at different stages of neural processing impacts optimal coding strategies. Using simulations and a flexible analytical approach, we show how these strategies depend on the strength of each noise source, revealing under what conditions the different noise sources have competing or complementary effects. We draw two primary conclusions: (1) differences in encoding strategies between sensory systems—or even adaptational changes in encoding properties within a given system—may be produced by changes in the structure or location of neural noise, and (2) characterization of both circuit nonlinearities as well as noise are necessary to evaluate whether a circuit is performing efficiently.Author Summary: For decades the efficient coding hypothesis has been a guiding principle in determining how neural systems can most efficiently represent their inputs. However, conclusions about whether neural circuits are performing optimally depend on assumptions about the noise sources encountered by neural signals as they are transmitted. Here, we provide a coherent picture of how optimal encoding strategies depend on noise strength, type, location, and correlations. Our results reveal that nonlinearities that are efficient if noise enters the circuit in one location may be inefficient if noise actually enters in a different location. This offers new explanations for why different sensory circuits, or even a given circuit under different environmental conditions, might have different encoding properties.