The caudate nucleus mediates learning of stimulus–control state associations

Abstract

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.