Abstract
The striatum integrates sensorimotor and motivational signals, likely playing a key role in reward-based learning of goal-directed behavior. However, cell type-specific mechanisms underlying reinforcement learning remain to be precisely determined. Here, we investigated changes in membrane potential dynamics of dorsolateral striatal neurons comparing naïve mice and expert mice trained to lick a reward spout in response to whisker deflection. We recorded from three distinct cell types: (i) direct pathway striatonigral neurons, which express type 1 dopamine receptors; (ii) indirect pathway striatopallidal neurons, which express type 2 dopamine receptors; and (iii) tonically active, putative cholinergic, striatal neurons. Task learning was accompanied by cell type-specific changes in the membrane potential dynamics evoked by the whisker deflection and licking in successfully-performed trials. Both striatonigral and striatopallidal types of striatal projection neurons showed enhanced task-related depolarization across learning. Striatonigral neurons showed a prominent increase in a short latency sensory-evoked depolarization in expert compared to naïve mice. In contrast, the putative cholinergic striatal neurons developed a hyperpolarizing response across learning, driving a pause in their firing. Our results reveal cell type-specific changes in striatal membrane potential dynamics across the learning of a simple goal-directed sensorimotor transformation, helpful for furthering the understanding of the various potential roles of different basal ganglia circuits.
Highlights
The changes in neural circuits underlying reward-based sensorimotor learning remain incompletely understood
We found that Vm dynamics of striatal projections neurons (SPNs) in whisker-related dorsolateral striatum (DLS) were strongly modulated during performance of a task in which mice were trained to lick a water-reward spout in response to a whisker deflection.[19]
Using the whole-cell recording technique, we examined Vm dynamics of 3 cell types in the striatum before and after learning a simple goal-directed sensorimotor transformation, finding 2 important changes: (i) SPNs in expert mice showed an enhanced depolarization compared to naıve mice; and (ii) TANs developed a hyperpolarizing response in expert mice
Summary
The changes in neural circuits underlying reward-based sensorimotor learning remain incompletely understood. We found that Vm dynamics of striatal projections neurons (SPNs) in whisker-related DLS were strongly modulated during performance of a task in which mice were trained to lick a water-reward spout in response to a whisker deflection.[19] Here, in a new set of recordings, we compare Vm responses from naıve and expert mice, before and after task learning. We recorded tonically active, putative cholinergic, interneurons (TANs), which form a small distinct population of cells with large somata in the striatal microcircuitry.[20,21,22,23] TANs developed a hyperpolarizing response and a pause in action potential firing with task learning, in agreement with previous studies.[24,25,26] Our data are consistent with the hypothesis that prominent cell-type-specific changes in striatal activity might accompany reward-based sensorimotor learning
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