Distinct mechanisms for evidence accumulation and choice memory explain diverse neuronal dynamics

A computation that is thought to underlie many decisions is the gradual accumulation of noisy evidence over time until a bound is reached, which triggers the commitment to a choice. The integration-to-bound framework captures the behavior in many decisions, as well as the pooled responses across neurons in many brain regions, suggesting that choices are formed based on the accumulated evidence encoded in neuronal firing rates. However, the correspondence between accumulated evidence and neuronal dynamics is only on aggregate. The choice-related dynamics of individual neurons are heterogeneous and appear inconsistent with representing a single bounded integration process. It is unclear how the diversity of choice dynamics might be reconciled with an integration-to-bound framework. Here we show that heterogeneous choice dynamics can be explained by state-dependent representations of accumulated evidence, before and after the commitment to a choice–which is implied by distinct mechanisms for integrating evidence and for maintaining the memory of the choice. We recorded from hundreds of neurons simultaneously using Neuropixels probes from five frontal brain regions in rats performing a task that requires the gradual accumulation of auditory evidence. We developed a statistical approach that models spike trains with state-dependent Poisson generalized linear models whose encoding of accumulated evidence depends on whether a bound has been reached. State-dependent encoding of accumulated evidence well predicts the diverse choice dynamics of individual neurons, better than models with stationary encoding. Moreover, we found that rat frontal regions, in particular the medial prefrontal cortex, represent accumulated evidence more strongly before than after the commitment to a choice, indicating that frontal circuits are differentially engaged during evidence accumulation and during choice memory. These findings suggest that the diversity of choice dynamics results from a single multi-staged decision process.