Medium spiny neurons activity reveals the discrete segregation of mouse dorsal striatum.

Javier Alegre-Cortés,Ramon Reig,Roberto Montanari,María Sáez

doi:10.7554/elife.60580

Abstract

Behavioral studies differentiate the rodent dorsal striatum (DS) into lateral and medial regions; however, anatomical evidence suggests that it is a unified structure. To understand striatal dynamics and basal ganglia functions, it is essential to clarify the circuitry that supports this behavioral-based segregation. Here, we show that the mouse DS is made of two non-overlapping functional circuits divided by a boundary. Combining in vivo optopatch-clamp and extracellular recordings of spontaneous and evoked sensory activity, we demonstrate different coupling of lateral and medial striatum to the cortex together with an independent integration of the spontaneous activity, due to particular corticostriatal connectivity and local attributes of each region. Additionally, we show differences in slow and fast oscillations and in the electrophysiological properties between striatonigral and striatopallidal neurons. In summary, these results demonstrate that the rodent DS is segregated in two neuronal circuits, in homology with the caudate and putamen nuclei of primates.

Highlights

The basal ganglia are a group of subcortical nuclei involved in a diversity of functions including motor control, learning, decision making, and reward (Packard and Knowlton, 2002; Schultz et al, 1997; Yin and Knowlton, 2006)
Once it had been shown that DLS and DMS circuits could be separated based on their slow wave oscillation (SWO), we studied the transition from one circuit to the other, exploring the properties of this brain state in dorsocentral striatum (DCS) (Figure 3A), a hypothetical third region between DLS and DMS
Human caudate and putamen have been compared to the rodent DLS and DMS, respectively (Balleine and O’Doherty, 2010), based in their corticostriatal connectivity and behavioral functions

Summary

Introduction

The basal ganglia are a group of subcortical nuclei involved in a diversity of functions including motor control, learning, decision making, and reward (Packard and Knowlton, 2002; Schultz et al, 1997; Yin and Knowlton, 2006). Some recent studies have divided the DS in two regions, dorsomedial (DMS) and dorsolateral (DLS) striatum, based on their behavioral roles (Graybiel, 2008; Hauber and Schmidt, 1994). While both regions participate in motor control, DLS is often related with habit, stimulus-response associations and navigation, whereas the DMS mediates action-outcome associations, goal-directed actions and flexible shifting between behavioral strategies, suggesting a role in higher cognitive functions (Faure et al, 2005; Hilario and Costa, 2008; Lerner et al, 2015; Thorn et al, 2010). In order to understand the basal ganglia circuits and their related behaviors, an essential question should be addressed: Is the functional segregation of the DS supported by two different circuits?

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