Bidirectional Control of Reversal in a Dual Action Task by Direct and Indirect Pathway Activation in the Dorsolateral Striatum in Mice

Abstract

The striatum is a key brain structure involved in the processing of cognitive flexibility, which results from the balance between the flexibility demanded for novel learning of motor actions and the inflexibility required to preserve previously learned actions. In particular, the dorsolateral portion of the striatum (DLS) is engaged in the learning of action sequence. This process is temporally driven by fine adjustments in the function of the two main neuronal populations of the striatum, known as the direct pathway medium spiny neurons (dMSNs) and indirect pathway medium spiny neurons (iMSNs). Here, using optogenetics, behavioral, and electrophysiological tools, we addressed the relative role of both neuronal populations in the acquisition of a reversal dual action sequence in the DLS. While the channelrhodopsin-induced activation of dMSNs and iMSNs of the DLS did not induce changes in the learning rate of the sequence, the specific activation of the dMSNs of the DLS facilitated the acquisition of a reversal dual action sequence; the activation of iMSNs induced a significant deficit in the acquisition of the same task. Taken together our results indicate an antagonistic relationship between dMSNs and iMSNs on the acquisition of a reversal dual action sequence.

GPRIN3 Controls Neuronal Excitability, Morphology, and Striatal-Dependent Behaviors in the Indirect Pathway of the Striatum

“…We have previously demonstrated the involvement of MSN populations in locomotor, exploratory, and operant behaviors (Durieux et al, 2009(Durieux et al, , 2012Laurent et al, 2017). Therefore, the impact of GPRIN3 KO was first evaluated on behaviors, such as locomotion (open field test), motor coordination and motor learning (accelerated rotarod), and also anxiety-like (elevated plus maze, light-dark box, and marble-burying tests) and depressive-like behaviors (tail suspension and sucrose preference), given that all these behaviors are related to the striatum.…”

“…The striatum is the primary input nucleus of the basal ganglia integrating sensorial, emotional, and higher cognitive responses (Hassoun et al, 2005;Wen et al, 2016;Laurent et al, 2017;Mal-tese et al, 2018). It receives dense dopaminergic innervations from the substantia nigra and from the ventral tegmental area (VTA) (Watabe-Uchida et al, 2012).…”

It takes two to tango: Dorsal direct and indirect pathways orchestration of motor learning and behavioral flexibility

“…Our lab recently investigated the respective roles of the d-and i-MSNs of the DLS in the acquisition of a new sequence learning in a reversal task using optogenetics in a chronic manner (Laurent et al, 2017). We generated a disbalance in BG activity by overactivating or boosting each pathway during the reversal process, and test the consequences of this perturbation on the animals' performance and ability to learn a new sequence.…”

Thalamic afferents to prefrontal cortices from ventral motor nuclei in decision‐making

“…The description of the innervation from the whole prefrontal cortex into segregated striatal areas, led to the exploration of basal ganglia functions associated with prefrontal cortical functions in monkeys (Graybiel, 1991;Romo et al, 1992;Joel & Weiner, 1994;Jaeger et al, 1995;Afifi, 2003). Some recently described striatal functions related to prefrontal cortical integration in rats that are of interest to this review, include motivational drive (Kreitzer & Berke, 2011), generation of self-paced movements (Klaus et al, 2017), and context-dependent facilitation of appropriate movements (Kreitzer & Berke, 2011), as well as learning involved in risk-based decisionmaking (Leblond et al, 2011), solution of cognitive conflicts between actions (Laurent et al, 2017), selection of action alternatives (Canales & Graybiel, 2000), decision-making particularly, in relation to the effort invested to obtain a reward (Carvalho Poyraz et al, 2016) and cost-benefit decision-making (Friedman et al, 2015).…”