The information bottleneck as a principle underlying multi-area cortical representations during decision-making

Abstract

Decision-making emerges from distributed computations across multiple brain areas, but it is unclear why the brain distributes the computation. In deep learning, artificial neural networks use multiple areas (or layers) and form optimal representations of task inputs. These optimal representations are sufficient to perform the task well, but minimal so they are invariant to other irrelevant variables. We recorded single neurons and multiunits in dorsolateral prefrontal cortex (DLPFC) and dorsal premotor cortex (PMd) in monkeys during a perceptual decision-making task. We found that while DLPFC represents task-related inputs required to compute the choice, the downstream PMd contains a minimal sufficient, or optimal, representation of the choice. To identify a mechanism for how cortex may form these optimal representations, we trained a multi-area recurrent neural network (RNN) to perform the task. Remarkably, DLPFC and PMd resembling representations emerged in the early and late areas of the multi-area RNN, respectively. The DLPFC-resembling area partially orthogonalized choice information and task inputs and this choice information was preferentially propagated to downstream areas through selective alignment with inter-area connections, while remaining task information was not. Our results suggest that cortex uses multi-area computation to form minimal sufficient representations by preferential propagation of relevant information between areas. SignificanceThe brain uses multiple areas for cognition, decision-making, and action, but it is unclear why cortical activity differs by brain area. Machine learning and information theory suggests that one benefit of multiple areas is that it provides an "information bottleneck" that compresses inputs into an optimal representation that is minimal and sufficient to solve the task. Combining experimental recordings from behaving animals and computational simulations, we show that later brain areas have a tendency to form such minimal sufficient representations of task inputs through preferential propagation of task-relevant information present in earlier areas. Our results thus provide insight into one possible reason why the brain uses multiple brain areas for supporting decision-making and action.