Flexible and accurate decoding of neural populations through stochastic comodulation

Sensory-guided behavior requires reliable encoding of information (from stimuli to neural responses) and flexible decoding (from neural responses to behavior). In typical decision tasks, a small subset of cells within a large population encode task-relevant stimulus information and need to be identified by later processing stages for relevant information to be transmitted. A statistically optimal decoder (e.g., maximum likelihood) can utilize task-relevant cells for any given task configuration, but relies on complete knowledge of the relationship between the task and the stimulus-response and noise properties of the encoding population. The brain could learn an optimal decoder for a task through supervised learning (i.e., regression), but this typically requires many training trials, and thus lacks the flexibility of humans or animals, that can rapidly adjust to changes in task parameters or structure. Here, we propose a novel decoding solution based on functionally targeted stochastic modulation. Population recordings during different discrimination tasks have revealed that a substantial portion of trial-to-trial variability in cell responses can be explained by stochastic modulatory signals that are shared, and that seem to preferentially target task-informative neurons (Rabinowitz et al., 2015). The variability introduced by these modulators corrupts the encoded stimulus signal, but we propose that it also serves as a label for the informative neurons, allowing decoder to solve the identification problem. We show in simulations of a modulated Poisson spiking model that a linear decoder with readout weights proportional to the estimated neuron-specific strength of modulation achieves performance close to an optimal decoder.