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A longstanding dichotomy in cognitive psychology and neuroscience pits controlled, top-down driven behavior against associative, bottom-up driven behavior, where cognitive control processes allow us to override well-learned stimulus-response (S-R) associations. By contrast, some previous studies have raised the intriguing possibility of an integration between associative and controlled processing in the form of stimulus-control state (S-C) associations, the learned linkage of specific stimuli to particular control states, such as high attentional selectivity. The neural machinery mediating S-C learning remains poorly understood, however. Here, we combined human functional magnetic resonance imaging (fMRI) with a previously developed Stroop protocol that allowed us to dissociate reductions in Stroop interference based on S-R learning from those based on S-C learning. We modeled subjects' acquisition of S-C and S-R associations using an associative learning model and then used trial-by-trial S-C and S-R prediction error (PE) estimates in model-based behavioral and fMRI analyses. We found that PE estimates derived from S-C and S-R associations accounted for the reductions in behavioral Stroop interference effects in the S-C and S-R learning conditions, respectively. Moreover, model-based fMRI analyses identified the caudate nucleus as the key structure involved in selectively updating stimulus-control state associations. Complementary analyses also revealed a greater reliance on parietal cortex when using the learned S-R versus S-C associations to minimize Stroop interference. These results support the emerging view that generalizable control states can become associated with specific bottom-up cues, and they place the caudate nucleus of the dorsal striatum at the center of the neural stimulus-control learning machinery.

The Caudate Nucleus Mediates Learning of Stimulus–Control State Associations