Inactivation of the lateral but not medial dorsal striatum eliminates the excitatory impact of Pavlovian stimuli on instrumental responding

Abstract

Conditioned stimuli are important guides for behavioral actions. This experiment determined the role of the dorsal striatum in conditioned-stimulus modulation of instrumental responding using the pavlovian-instrumental transfer (PIT) paradigm. Rats received pavlovian training wherein two different auditory stimuli predicted the delivery of two food rewards. Next, rats were trained to perform two instrumental actions earning the same two rewards. Finally, the impact of pavlovian stimuli on instrumental performance was assessed in extinction: the stimuli were periodically presented while rats were free to perform the lever-press response. Before testing, medial or lateral dorsal striatum was infused with saline or baclofen/muscimol, to temporarily inactivate the region. Under saline, outcome-selective PIT was observed: presentation of a stimulus paired with the same outcome as the instrumental action elevated responding, whereas presentation of a stimulus paired with a different outcome did not. Inactivation of the dorsolateral striatum dramatically reduced this effect. Inactivation of the dorsomedial striatum left intact the ability of reward-related stimuli to invigorate responding; however, the selectivity of the stimulus effect was lost (i.e., both stimuli excited responding). These results indicate that subregions of the dorsal striatum play distinct roles in stimulus modulation of instrumental performance with the lateral region being vital for reward-related stimuli to excite responding and the medial region being involved in the integration of stimulus-reward associations with specific response-outcome associations to produce selective responding. These findings identify new roles for the dorsal striatum in mediating the incentive effects of reward-predictive stimuli on behavioral actions made to obtain reward.

Figure 1.

Schematic representation of the injection cannulas placements in coronal sections (Paxinos and Watson, 1998). The location of the injector tips is represented by circles for the DLS group and by squares for the DMS group. Numbers indicate the distance anterior to bregma in millimeters.

Figure 2.

Effects of inactivation of the DLS and the DMS on lever-press responding during a pavlovian stimulus within the pavlovian-instrumental transfer procedure. For all figures, “pre” represents the baseline instrumental responding in the absence of any stimuli, “same” represents responding during presentation of the stimulus paired with the same outcome as the available lever, and “different” represents responding during the stimulus that was paired with the outcome earned by the alternate, currently unavailable lever. A, Mean (±SEM) lever press responding after inactivation of the DLS. After saline infusions, responding was elevated during the Same and Different stimuli relative to baseline and the impact of the same stimulus was greater than that of the Different stimulus. After BAC/MUS infusion, the enhancement of responding by presentation of the Same stimulus was greatly reduced. B, Mean (±SEM) lever press responding after inactivation of the DMS. After saline infusions, responding was elevated during the Same and Different stimuli relative to baseline and the impact of the Same stimulus was greater than that of the Different stimulus. After BAC/MUS infusion, responding was elevated during both the Same and Different stimuli compared with baseline and responding during these stimuli did not differ. n = 8 per group. Please refer to the text for complete statistical analyses. *Difference between a stimulus and baseline (p < 0.05); ^#difference between the Same and Different stimuli; ^☆difference between saline and inactivation conditions (p < 0.05).