Coding dynamics of the striatal networks during learning

Abstract

The rat dorsomedial (DMS) and dorsolateral striatum (DLS), equivalent to caudate nucleus and putamen in primates, are required for goal-directed and habit behaviour, respectively. However, it is still unclear whether and how this functional dichotomy emerges in the course of learning. In this study we investigated this issue by recording DMS and DLS single neuron activity in rats performing a continuous spatial alternation task, from the acquisition to optimized performance. We first applied a classical analytical approach to identify task-related activity based on the modifications of single neuron firing rate in relation to specific task events or maze trajectories. We then used an innovative approach based on Hawkes process to reconstruct a directed connectivity graph of simultaneously recorded neurons, that was used to decode animal behavior. This approach enabled us to better unravel the role of DMS and DLS neural networks across learning stages. We showed that DMS and DLS display different task-related activity throughout learning stages, and the proportion of coding neurons over time decreases in the DMS and increases in the DLS. Despite theses major differences, the decoding power of both networks increases during learning. These results suggest that DMS and DLS neural networks gradually reorganize in different ways in order to progressively increase their control over the behavioral performance.

Significance statement Our study helps understanding the role of the dorsomedial (DMS) and dorsolateral striatum (DLS) during the acquisition and optimization of a behavioral strategy. It is generally believed that the DMS mediates action-outcome associations, whereas the DLS supports habit behavior, but it is still unclear how these processes emerges during learning. To analyze the dynamic changes of DMS and DLS network activity across learning stages, we used a mathematical analysis combining single neuron firing rate and connectivity between neurons to decode rat behavior in a goal-directed spatial task. We demonstrated that both DMS and DLS activity supports behavioral performance throughout all learning stages, thus challenging the hypothesis of a gradual shift from DMS to DLS activity.