Knowing whether core reward regions carry information about the positions of relevant objects is crucial for adjudicating between choice models. One limitation of previous studies, including our own, is that spatial positions can be consistently differentially associated with rewards, and thus position can be confounded with attention, motor plans, or target identity. We circumvented these problems by using a task in which value—and thus choices—was determined solely by a frequently changing rule, which was randomized relative to spatial position on each trial. We presented offers asynchronously, which allowed us to control for reward expectation, spatial attention, and motor plans in our analyses. We find robust encoding of the spatial position of both offers and choices in two core reward regions, orbitofrontal Area 13 and ventral striatum, as well as in dorsal striatum of macaques. The trial-by-trial correlation in noise in encoding of position was associated with variation in choice, an effect known as choice probability correlation, suggesting that the spatial encoding is associated with choice and is not incidental to it. Spatial information and reward information are not carried by separate sets of neurons, although the two forms of information are temporally dissociable. These results highlight the ubiquity of multiplexed information in association cortex and argue against the idea that these ostensible reward regions serve as part of a pure value domain.

Flexible decision-making, a defining feature of human cognition, is typically thought of as a canonical pFC function. Recent work suggests that the striatum may participate as well; however, its role in this process is not well understood. We recorded activity of neurons in both the ventral (VS) and dorsal (DS) striatum while rhesus macaques performed a version of the Wisconsin Card Sorting Test, a classic test of flexibility. Our version of the task involved a trial-and-error phase before monkeys could identify the correct rule on each block. We observed changes in firing rate in both regions when monkeys switched rules. Specifically, VS neurons demonstrated switch-related activity early in the trial-and-error period when the rule needed to be updated, and a portion of these neurons signaled information about the switch context (i.e., whether the switch was intradimensional or extradimensional). Neurons in both VS and DS demonstrated switch-related activity at the end of the trial-and-error period, immediately before the rule was fully established and maintained, but these signals did not carry any information about switch context. We also observed associative learning signals (i.e., specific responses to options associated with rewards in the presentation period before choice) that followed the same pattern as switch signals (early in VS, later in DS). Taken together, these results endorse the idea that the striatum participates directly in cognitive set reconfiguration and suggest that single neurons in the striatum may contribute to a functional handoff from the VS to the DS during reconfiguration processes.