Abstract

We have the capacity to follow arbitrary stimulus-response rules, meaning simple policies that guide our behavior. Rule identity is broadly encoded across decision-making circuits, but there are less data on how rules shape the computations that lead to choices. One idea is that rules could simplify these computations. When we follow a rule, there is no need to encode or compute information that is irrelevant to the current rule, which could reduce the metabolic or energetic demands of decision-making. However, it is not clear if the brain can actually take advantage of this computational simplicity. To test this idea, we recorded from neurons in 3 regions linked to decision-making, the orbitofrontal cortex (OFC), ventral striatum (VS), and dorsal striatum (DS), while macaques performed a rule-based decision-making task. Rule-based decisions were identified via modeling rules as the latent causes of decisions. This left us with a set of physically identical choices that maximized reward and information, but could not be explained by simple stimulus-response rules. Contrasting rule-based choices with these residual choices revealed that following rules (1) decreased the energetic cost of decision-making; and (2) expanded rule-relevant coding dimensions and compressed rule-irrelevant ones. Together, these results suggest that we use rules, in part, because they reduce the costs of decision-making through a distributed representational warping in decision-making circuits.

Highlights

  • We have a tremendous capacity to change how we perceive and respond to the world as our environment and goals change

  • We focus on measuring population representations of choice features in 3 areas implicated in decision-making and reward processing: Area 13 of the orbitofrontal cortex (OFC), the nucleus accumbens core of the ventral striatum (VS), and both the caudate and putamen in the dorsal striatum (DS)

  • Two rhesus macaques performed a total of 128 sessions (73,627 trials) of the Cognitive SetShifting Task (CSST, Fig 1A, [7,40]), a macaque analog of the Wisconsin Card Sorting Task

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Summary

Introduction

We have a tremendous capacity to change how we perceive and respond to the world as our environment and goals change. We know from many studies that rule identity is encoded in firing rate changes of neurons in specific brain regions, classically in the dorsolateral prefrontal cortex (dlPFC; [1,2,3,4]), and in regions implicated in decision-making, like the orbitofrontal cortex (OFC) and striatum [5,6,7,8,9,10]. Implementing a rule requires more than encoding its identity in the right structures, and an important question remains unanswered: How do rules shape neural processing?. One possibility is that rules warp the way the world is represented in decision-making circuits. Many decisions require us to solve very high-dimensional problems, where the correct response is some complex function of our past choices, reward history, and the various

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