The effect of lesions of the insular cortex on instrumental conditioning: evidence for a role in incentive memory

Abstract

In three experiments, we assessed the effect of lesions aimed at the gustatory region of the insular cortex 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, however, attenuate the impact of outcome devaluation, induced by sensory-specific satiety, on instrumental performance but only when assessed in an extinction test. This effect was not secondary to an impairment in instrumental learning; in experiment 2, no 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. In experiment 3, however, lesioned rats were found to be insensitive to the impact of an incentive learning treatment conducted when they were undeprived; although, again, this deficit was confined to a test conducted in extinction. These results are consistent with the view that, in instrumental conditioning, the gustatory region of the insular cortex is involved in encoding the taste of food outcomes in memory and, hence, in encoding the incentive value assigned to these outcomes on the basis of prevailing motivational conditions.

Fig. 1.

Experiment 1. Diagrams of coronal sections (0.48–1.7 mm anterior to bregma) on which the extent of cell loss observed after bilateral infusions of quinolinic acid aimed at the gustatory region of the insular cortex has been reconstructed from histology to reveal the largest (darker) and smallest (lighter) regions of damage induced in group GC. Thelines drawn on the right-hand hemisphere extending laterally from the corpus callosum (cc) and the claustrum (CL) reflect divisions between (from thetop) primary somatosensory (S), granular (GI), dorsal agranular (dAI), and ventral agranular (vAI) regions of insular cortex, respectively, as labeled on the lowermost section. rf, Rhinal fissure.

Fig. 2.

Experiment 1. Photomicrograph showing a Nissl-stained coronal section through the insular cortex (∼1.0 mm anterior bregma). A shows this section in low magnification, whereas in B, the area enclosed by thedashed rectangle in A has been enlarged to give a clearer indication of the lesion boundaries (arrows). cc, Corpus callosum;rf, rhinal fissure.

Fig. 3.

Experiment 1. The mean number of lever presses (left) and chain pulls (right) 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 are presented separately for group GC (filled circles) and group sham (open circles).

Fig. 4.

Experiment 1. The number of lever presses and chain pulls (i.e., actions) per minute during instrumental training (left) 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 (middle) and group GC (right) averaged across 2 min periods with performance of the action that previously delivered the pre-fed, i.e., devalued (Deval), outcome (filled circles) presented separately from performance of the action that had delivered the non-pre-fed, i.e., valued (Val), outcome (open circles) for each group.

Fig. 5.

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) and group GC (right) averaged across 2 min periods with performance of the action that previously delivered the pre-fed, i.e., devalued (Deval), outcome (filled circles) presented separately from performance of the action that had delivered the non-pre-fed, i.e., valued (Val), outcome (open circles) for each group.

Fig. 6.

Experiment 2. Mean performance of lever-press and chain-pull actions per minute, averaged over 3 min periods, 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: A, showing the data from group sham; andB, showing the data from group GC. In this figure, performance of each action is presented separately in eachpanel 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, filled circles) or has not been degraded, i.e., the outcome delivered by performing the action differs from that delivered without performing the action (Diff, open circles). In thepanel illustrating the extinction test, the previously degraded action-outcome contingency remains designated asSame and the nondegraded as Diff, although no outcomes of any kind were presented in this test.

Fig. 7.

Experiment 3. Diagrams of coronal sections (0.48–1.7 mm anterior to bregma) on which the extent of cell loss observed after bilateral infusions of quinolinic acid aimed at the gustatory region of the insular cortex has been reconstructed from histology to reveal the largest (darker) and smallest (lighter) regions of damage induced in group GC. Abbreviations are as for Figure 1.

Fig. 8.

Experiment 3. Performance of lever-press and chain-pull actions averaged across 4 min periods in the choice extinction test conducted after a post-training reduction in food deprivation. Before this test, all of the rats were allowed to learn about the effect of the shift in food deprivation on the incentive value of one of the two food outcomes used in training by giving them brief consummatory contact with that outcome in the new, i.e., low deprivation, state. The effect of this treatment on choice performance in extinction is presented for group sham (left) and group GC (right) with the performance of the action that, in training, delivered the outcome re-exposed in the low deprivation state (i.e., Deval, filled circles) plotted separately from performance of the other action (i.e., Val, open circles) in each group.

Fig. 9.

Experiment 3. Rate of performance of the lever-press and chain-pull actions in the reacquisition tests conducted after the extinction test. Rats were shifted between high and low levels of deprivation with the effect of these shifts assessed on the relative performance of the devalued (Dev) and valued (Val) actions, as designated in the extinction test. The average rate of performance of each action was averaged across the two sessions conducted in each deprivation state and plotted separately for group sham (left) and group GC (right).