We tested the hypothesis that neuronal activity in the striatum is sensitive to changes in stimulus-reward association. A novel go/no-go reaction-time task was used that allowed us to change associations between stimuli and rewards within single experimental sessions. Changes in stimulus-reward association led to rapid modulations of spike activity throughout the medial striatum. Decoding analysis showed that more neurons in the dorsomedial striatum, compared to the ventromedial striatum, were sensitive to changes in stimulus-reward association. Some neurons only decoded changes in stimulus value. Other neurons decoded changes in the animals' reaction times, which were reduced to rewarded stimuli. Most, but not all, neurons that decoded changes in stimulus-reward association also decoded whether rats made go or no-go responses independent of stimulus value. Crucially, changes in these neural measures of stimulus-reward association preceded changes in behavioral performance by several trials. The firing patterns of neurons that decoded changes in stimulus-reward association were highly heterogeneous. There was also a considerable amount of trial-to-trial variability across groups of simultaneously recorded neurons. By contrast, we observed spatially consistent alterations in striatal local field potentials (LFPs) when stimulus-reward associations were changed. There was increased power in the theta range for LFP responses to newly rewarded stimuli and increased spike-field coherence in the theta range for neurons that decoded stimulus value, but not for neurons that were exclusively sensitive to reaction times. Together, our results suggest that changes in stimulus-reward association lead to an immediate modulation of the medial striatum. Through effects on downstream components of the basal ganglia, the medial striatum may enable rapid flexibility in action selection.
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