The Army of One (Sample): the Characteristics of Sampling-based Probabilistic Neural Representations

There is growing evidence that humans and animals represent the uncertainty associated with sensory stimuli and utilize this uncertainty during planning and decision making in a statistically optimal way. Recently, a nonparametric framework for representing probabilistic information has been proposed whereby neural activity encodes samples from the distribution over external variables. Although such sample-based probabilistic representations have strong empirical and theoretical support, two major issues need to be clarified before they can be considered as viable candidate theories of cortical computation. First, in a fluctuating natural environment, can neural dynamics provide sufficient samples to accurately estimate a stimulus? Second, can such a code support accurate learning over biologically plausible time-scales? Although it is well known that sampling is statistically optimal if the number of samples is unlimited, biological constraints mean that estimation and learning in the cortex must be supported by a relatively small number of possibly dependent samples. We explored these issues in a cue combination task by comparing a neural circuit that employed a sampling-based representation to an optimal estimator. For static stimuli, we found that a single sample is sufficient to obtain an estimator with less than twice the optimal variance, and that performance improves with the inverse square root of the number of samples. For dynamic stimuli, with linear-Gaussian evolution, we found that the efficiency of the estimation improves significantly as temporal information stabilizes the estimate, and because sampling does not require a burn-in phase. Finally, we found that using a single sample, the dynamic model can accurately learn the parameters of the input neural populations up to a general scaling factor, which disappears for modest sample size. These results suggest that sample-based representations can support estimation and learning using a relatively small number of samples and are therefore highly feasible alternatives for performing probabilistic cortical computations.
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