The primate putamen processes cognitive flexibility alongside the caudate and ventral striatum with similar speeds of updating values

Abstract

The putamen is thought to generate habitual actions by processing value information relayed from the ventral striatum through the caudate nucleus. However, it is a question what value the putamen neurons process and whether the putamen receives serially processed value through the striatal structures. We found that neurons in the primate putamen, caudate, and ventral striatum selectively encoded flexibly updated values for adaptive behaviors with similar learning speeds, rather than stably sustained values for habit. In reversal value learning, rostral striatum neurons dynamically adjusted their responses to object values in alignment with changes in saccade reaction times following reversals. Notably, the value acquisition speeds within trials were similar, proposing a parallel value update in each striatal region. However, in stable value retrieval, most did not encode the values for habitual saccades. Our findings suggest that the rostral striatum including the putamen is selectively involved in the parallel processing of cognitive flexibility.