Posterior dorsomedial striatum is critical for both selective instrumental and Pavlovian reward learning

Abstract

The dorsal striatum (DS) has been implicated in instrumental learning but its role in the acquisition of stimulus-driven behaviour is not clear. To explore the contribution of the DS to both response-outcome (R-O) and stimulus-outcome (S-O) associative learning, we pharmacologically inactivated subregions (dorsolateral, anterior dorsomedial and posterior dorsomedial) of the DS during acquisition sessions in which subjects acquired two unique, novel R-O pairs or two unique, novel S-O pairs. To test whether specific R-O or S-O associations were learned under inactivation, rats were tested following selective-satiety devaluation of one outcome under drug-free conditions. In the instrumental task, control rats and rats with dorsolateral striatum (DLS) inactivation during learning responded less on the lever that had earned the devalued outcome than on the alternative lever at test, indicating that the DLS is not critical for the formation of R-O associations. In contrast, rats with inactivation of the medial DS (DMS) (either anterior or posterior) during learning responded indiscriminately, suggesting failure to acquire the novel R-O associations. In the Pavlovian task, both controls and rats with anterior DMS inactivation during learning responded less in the presence of the stimulus predicting the devalued outcome, whereas rats with DLS or posterior DMS inactivation during learning responded equally to the stimuli, indicating that they had not acquired the novel S-O associations. These data confirm that the DLS and anterior region DMS mediate different aspects of reward-related learning, and suggest that the posterior DMS may mediate a function common to both forms of learning (R-O and S-O). Finally, we demonstrate that both S-O and R-O associations are required for selective Pavlovian-instrumental transfer.

Fig. 1

Reconstruction of microinfusion sites in the DS. The location of the cannula tips is represented by circles for the DLS group, squares for the aDMS group and triangles for the pDMS group. Numbers on the left indicate distance relative to bregma in mm. The microinfusion sites are superimposed on coronal sections (adapted from the rat brain atlas of Paxinos & Watson, 1998).

Fig. 2

Inactivation of the aDMS and pDMS impairs acquisition of novel R-O associations as revealed in a subsequent test of outcome devaluation. (A) Mean responding (+ SEM) on both levers combined during pre-training with the same outcome (polycose) earned by both levers. There were no differences among groups. (B) Mean responding per session (+ SEM) on both levers combined during specific R-O training during which rats were exposed to two unique R-O pairs following a pre-session microinfusion of saline (control) or baclofen/muscimol (aDMS, pDMS, and DLS groups). Data are averaged across three consecutive training/inactivation sessions. The aDMS group responded more than the pDMS group but neither group was significantly different from saline controls. (C) Mean responding (+ SEM) on each of two levers during the 15-min devaluation test. Subjects were pre-fed with one of the two outcomes and the lever that previously delivered that outcome was termed ‘devalued’ and the lever that previously delivered the outcome that was not pre-fed was termed ‘non-devalued’. Saline control rats and rats with prior inactivation of the DLS during specific R-O training show a significant decrease in responding on the devalued lever relative to the non-devalued lever. Rats with prior inactivation of the aDMS and pDMS during specific R-O training show no significant differences in responding on the two levers. Control, N = 17; aDMS, N = 10; pDMS, N = 9; DLS, N = 9. *P < 0.05, **P < 0.01.

Fig. 3

Inactivation of the DLS and pDMS impairs acquisition of novel S-O associations as revealed in a subsequent test of outcome devaluation. (A) Mean magazine (reward port) responding (+ SEM) during pre-training with the same outcome available at each magazine. ‘Rewarded’ refers to the magazine that delivered the reward during the current stimulus, whereas ‘alternate’ refers to the magazine that was rewarded during the other (currently not present) stimulus; ‘pre’ refers to the period prior to stimulus presentation; ‘stimulus’ refers to the period during the stimulus. There were no differences among groups. (B) Mean magazine responding per session (+ SEM) during specific SO training (average of three training days) during which rats were exposed to two unique S-O pairs following a pre-session microinfusion of saline (control) or baclofen/muscimol (aDMS, pDMS and DLS). The aDMS group responded more than the pDMS group during stimulus presentation but neither group was significantly different from saline controls. The aDMS group made more entries to the alternate magazine than all other groups. (C) Mean magazine responding (+ SEM) during the stimuli or equivalent pre-stimulus periods in the devaluation test. Subjects were pre-fed with one of the two outcomes and the stimulus previously associated with that outcome was termed ‘devalued’ and the stimulus previously associated with the outcome that was not pre-fed was termed ‘non-devalued’. Saline control rats and rats with prior inactivation of the aDMS during specific S-O training show a significant decrease in responding during the devalued stimulus relative to the non-devalued stimulus. Rats with prior inactivation of the DLS and pDMS during specific S-O training show no significant differences in responding during the two stimuli. Group N-values as in Fig. 1. *P < 0.05; **P < 0.01.

Fig. 4

Expression of PIT is impaired if subjects have failed to acquire either the selective R-O or selective S-O associations that underlie performance in this task. Mean lever-press responding (+ SEM) during test sessions during periods with no stimuli (baseline) and during presentation of the two stimuli used during the specific S-O training (no rewards were delivered). ‘Same’ refers to the stimulus paired with the same outcome as was previously earned by pressing the available lever; ‘different’ refers to the stimulus paired with the other outcome. All groups elevated responding from baseline during presentations of either stimulus. Only the control group showed a significantly greater enhancement of responding during presentation of the same vs. different stimulus. **P < 0.01.