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

Muriel Laurent,Danie Rial,Serge N Schiffmann,Jean-François De Backer,Alban De Kerchove D'Exaerde

doi:10.3389/fnbeh.2017.00256

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.

Highlights

The ability of the brain to organize memories and action sequences in single units of cognition is of great importance for the increase in performance upon learning observed in animals
We examined the effects of the selective optogenetic activation of indirect pathway medium spiny neurons (iMSNs) and direct pathway medium spiny neurons (dMSNs) of the dorsolateral portion of the striatum (DLS) on the acquisition of a simple sequence
It had been shown previously that excitotoxic lesions of all striatal neurons of the DLS disrupt the dual action order learning (Yin, 2010). Combining this information with the results here gathered, it is suggested that at least in physiological conditions, the role of dMSNs is hierarchically predominant over the iMSNs to initiate learning

Summary

Introduction

The ability of the brain to organize memories and action sequences in single units of cognition is of great importance for the increase in performance upon learning observed in animals. The sequence of learned actions allows the achievement of a higher efficient assessment of acquired information (Hilario et al, 2012). In order to achieve a higher efficient state the sequential organization of actions requires precise timing, proper initiation, and termination of the sequence (Graybiel, 1998; Yin et al, 2009; Jin and Costa, 2010). The dorsal striatum is well-positioned to control such actions since it had been shown to play critical roles in motor planning, in the action “chunking” and in procedural learning processes (Graybiel, 1998; Yin and Knowlton, 2006; Balleine et al, 2009). While the DLS majorly receives afferents from sensorimotor areas, the DMS receives inputs mainly from associative areas (Voorn et al, 2004; Yin, 2010). Functional data from Yin and collaborators indicate that the DMS

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