The role of the nucleus accumbens in instrumental conditioning: Evidence of a functional dissociation between accumbens core and shell

Abstract

In three experiments we examined the effect of bilateral excitotoxic lesions of the nucleus accumbens core or shell subregions on instrumental performance, outcome devaluation, degradation of the instrumental contingency, Pavlovian conditioning, and Pavlovian-instrumental transfer. Rats were food deprived and trained to press two levers, one delivering food pellets and the other a sucrose solution. All animals acquired the lever-press response although the rate of acquisition and overall response rates in core-lesioned animals were depressed relative to that in the shell- or sham-lesioned animals. Furthermore, in shell- and sham-lesioned rats, post-training devaluation of one of the two outcomes using a specific satiety procedure produced a selective reduction in performance on the lever that, in training, delivered the prefed outcome. In contrast, the core-lesioned rats failed to show a selective devaluation effect and reduced responding on both levers. Subsequent tests revealed that these effects of core lesions were not caused by an impairment in their ability to recall the devalued outcome, to discriminate the two outcomes, or to encode the instrumental action-outcome contingencies to which they were exposed. Additionally, the core lesions did not have any marked effect on Pavlovian conditioning or on Pavlovian-instrumental transfer. Importantly, although shell-lesioned rats showed no deficit in any test of instrumental conditioning or in Pavlovian conditioning, they failed to show any positive transfer in the Pavlovian-instrumental transfer test. This double dissociation suggests that nucleus accumbens core and shell differentially mediate the impact of instrumental and Pavlovian incentive processes, respectively, on instrumental performance.

Fig. 1.

Schematic representation of excitotoxic lesions of the NAC core (A) and shell (B). Shaded areas represent the maximum (black) and minimum (gray) extent of the lesions for the animals included in the behavioral analyses. Coronal sections are taken from the following points in the anteroposterior plane beginning at top left: +2.2, +1.7, +1.6, +1.2, +1.0, and +0.7 mm anterior to bregma (Paxinos and Watson, 1998).

Fig. 2.

Photomicrographs showing thionin-stained coronal sections through the nucleus accumbens. Top, Representative core lesions. Bottom, Representative shell lesions. Left, Images of the general region of the NAC (40× magnification) of core-lesioned (top) and shell-lesioned (bottom) animals. Middle, Greater magnification of the region indicated by the outlined boxes in the left images; arrowheads indicate lesion boundaries.Right, High-magnification photographs of the region of the lesions shown in the middle images (in lesioned animals) but in sham-lesioned animals. Allimages are from slices taken at ∼2.6 mm anterior to bregma. ac, Anterior commissure; Co, NAC core; LV, lateral ventricle; Sh, NAC shell.

Fig. 3.

Mean lever-press responses per minute for the three groups across days of training. Responding was reinforced on days 1–3 on an RR-5 schedule of reinforcement, on days 4–6 on an RR-10 schedule of reinforcement, and on days 7–9 on an RR-20 schedule of reinforcement.

Fig. 4.

Mean lever-press responses for the devaluation tests conducted in experiment 1 for each of the lesioned groups.A, Sham. B, Shell. C, Core. For A–C, the left panel displays the mean response rate per minute at the end of training. Thesecond panel from the left displays responses per minute for the devalued and nondevalued outcomes in a two-lever, choice extinction test. The third panel from the left illustrates the mean performance during the retraining sessions, and the right panel displays the mean lever-press responses per minute in a rewarded, two-lever test after devaluation of one of the instrumental outcomes.SED represents the SE of the difference in responding for the within-subjects variable. DEV, Devalued; NON, nondevalued.

Fig. 5.

Mean lever-press responses during tests of the sensitivity of the animals to the selective degradation of one instrumental action–outcome contingency in each of the lesioned groups. A, Sham. B, Shell.C, Core. For A–C, the left panel displays mean lever presses per minute across days of contingency degradation training, and the right paneldisplays the mean responses per minute on the two levers in an extinction test.

Fig. 6.

Mean magazine entries per minute during CS presentations and in the pre-CS interval across days of Pavlovian training.

Fig. 7.

Mean lever presses per minute during the presentation of each of the stimuli minus the mean lever presses per minute during the no-stimulus (Ø) baseline period for each of the three lesion groups. The term same refers to responding during the stimulus that was paired with the same outcome as that earned in training on that lever, whereas the termdifferent refers to responding during the stimulus that was paired with a different outcome than that earned in training on that lever.