The effect of lesions of the basolateral amygdala on instrumental conditioning

Abstract

In three experiments, we assessed the effect of lesions of the amygdala basolateral complex (BLA) on instrumental conditioning in rats. In experiment 1, the lesion had no effect on the acquisition of either lever pressing or chain pulling in food-deprived rats whether these actions earned food pellets or a maltodextrin solution. The lesion did attenuate, however, the impact of outcome devaluation, induced by sensory-specific satiety, on instrumental performance both when assessed in extinction and when reward was delivered contingent on instrumental performance. In experiment 2, evidence was found to suggest that the lesioned rats differed from shams in their ability to encode the specific action-outcome contingencies to which they were exposed during training: lesioned rats failed to adjust their performance appropriately when the action-outcome contingency was degraded. These effects were not caused by an inability of BLA lesioned rats to discriminate the two instrumental actions; these rats were similar to shams in their acquisition of a heterogeneous instrumental chain involving lever pressing and chain pulling (experiment 3). In experiment 4, however, lesions of the BLA were found to produce a deficit in the ability of rats to use the specific properties of the instrumental outcomes used in the previous experiments to discriminate rewarded from unrewarded actions in a free operant discrimination situation. Together these results suggest that in instrumental conditioning, the BLA mediates outcome encoding, specifically relating the sensory features of nutritive commodities to the emotional consequences induced by their consumption.

Fig. 1.

Diagrams of coronal sections (−1.88, −2.3, −2.8, −3.3, −3.8 mm posterior to bregma, from top tobottom) on which the extent of cell loss observed after bilateral infusions of quinolynic acid aimed at the BLA has been reconstructed from histology to reveal the largest (darker) and smallest (lighter) regions of damage induced in BLA lesioned animals used in this series of experiments.

Fig. 2.

Experiment 1: the mean number of lever presses (left panel) and chain pulls (right panel) performed per outcome during instrumental acquisition on the FI 20 reinforcement schedule used in experiment 1. Data are averaged across blocks of five outcomes and presented separately for group BLA (●) and group Sham (■).

Fig. 3.

Experiment 1: the number of lever presses and chain pulls (i.e., actions) per minute during instrumental training (left panel) and during the choice extinction test conducted after one of the training outcomes was devalued by a specific satiety treatment. Data from the extinction test are presented for group Sham (center panel) and group BLA (right panel) averaged across 2 min periods with performance of the action that previously delivered the prefed, i.e.,Devalued, outcome (●) presented separately from performance of the action that had delivered the non-prefed, i.e.,Valued, outcome (○) for each group.

Fig. 4.

Experiment 1: the number of lever presses and chain pulls (i.e., actions) per minute during the choice reward test conducted after one of the training outcomes was devalued by a specific satiety treatment. In contrast to the extinction test, performance of lever press and chain pull actions delivered the training outcomes on independent random ratio schedules. Data from the reward test are presented for group Sham (left panel) and group BLA (right panel) averaged across 2 min periods with performance of the action that previously delivered the prefed, i.e., Devalued, outcome (●) presented separately from performance of the action that had delivered the non-prefed, i.e.,Valued, outcome (○) for each group.

Fig. 5.

Experiment 2: mean performance of lever press and chain pull actions per minute, averaged over 3 min bins, during each of the 4 d of contingency assessment (left four panels) and during the extinction test (right panel). Test performance is divided into two panels: thetop panels show the data from group Sham and thebottom panels show the data from group BLA. In this figure, performance of each action is presented separately in each panel according to whether the action-outcome contingency has been degraded, i.e., the outcome delivered by performing the action is the same as the one now delivered without performing the action (same, ●), or has not been degraded, i.e., the outcome delivered by performing the action differs from that delivered without performing the action (diff, ○). In the panel illustrating the extinction test (extn), the previously degraded action-outcome contingency remains designated assame and the nondegraded as diff, although no outcomes were presented in this test.

Fig. 6.

Experiment 3: performance on the heterogeneous chain of instrumental actions presented as actions per opportunity in each second after performance of either the lever press or chain pull actions presented separately for each of the possible orders of these responses and for animals in group Sham (left panel) and group BLA (right panel). For half of the rats in each group, A1 was lever pressing and A2 was chain pulling, whereas for the remaining rats these assignments were reversed.

Fig. 7.

Experiment 4: mean performance of the rewarded (A+) and unrewarded (A−) actions in the outcome discrimination training sessions presented separately for the minimum A+ (left panel) and maximum A+ (right panel) sessions and for groups Sham and group BLA.