The caudate nucleus mediates learning of stimulus control state associations.
A longstanding dichotomy in cognitive psychology and neuroscience pits controlled, top down driven against associative, bottom up driven behavior, where cognitive control processes allow us to override well learned stimulus response (S R) associations. By contrast, some recent 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 functional neuroimaging (fMRI) with a recently developed Stroop protocol that allowed us to dissociate reductions in Stroop interference based on S R learning from those based on S C learning in humans. We modeled subjects' acquisition of S C and S R associations using an associative learning model and then employed 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 utilizing 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. SIGNIFICANCE STATEMENT Recent behavioral studies have demonstrated that control states, for instance, heightened attentional selectivity, can become directly associated with and subsequently retrieved by particular stimuli, thus breaking down the traditional dichotomy between top down and bottom up driven behavior. However, the neural mechanisms underlying this type of stimulus control learning remain poorly understood. We therefore combined non invasive human neuroimaging with a task that allowed us to dissociate the acquisition of stimulus control associations from that of stimulus response associations. The results revealed the caudate nucleus as the key brain structure involved in selectively driving stimulus control learning. These data represent the first identification of the neural mechanisms of stimulus specific control associations, and they significantly extend current conceptions of the type of learning processes mediated by the caudate.
The Journal of neuroscience the official journal of the Society for Neuroscience