Double dissociation of basolateral and central amygdala lesions on the general and outcome-specific forms of pavlovian-instrumental transfer

Abstract

This series of experiments compared the effects of lesions of the basolateral complex (BLA) and the central nucleus (CN) of the amygdala on a number of tests of instrumental learning and performance and particularly on the contribution of these structures to the specific and general forms of pavlovian-instrumental transfer (PIT). In experiment 1, groups of BLA-, CN-, and sham-lesioned rats were first trained to press two levers, each earning a unique food outcome (pellets or sucrose), after which they were given training in which two auditory stimuli (tone and white noise) were paired with these same outcomes. Tests of specific satiety induced outcome devaluation, and tests of PIT revealed that, although the rats in all of the groups performed similarly during both the instrumental and pavlovian acquisition phases, BLA, but not CN, lesions abolished selective sensitivity to a change in the reward value of the instrumental outcome as well as to the selective excitatory effects of reward-related cues in PIT. In experiment 2, we developed a procedure in which both the general motivational and the specific excitatory effects of pavlovian cues could be assessed in the same animal and found that BLA lesions abolished the outcome-specific but spared the general motivational effects of pavlovian cues. In contrast, lesions of CN abolished the general motivational but spared the specific effects of these cues. Together, these results suggest that the BLA mediates outcome-specific incentive processes, whereas CN is involved in controlling the general motivational influence of reward-related events.

Figure 1.

Schematic representation of excitotoxic lesions of the amygdala, with largest area of damage in light gray and smallest area of damage in dark gray. Lesions of the CN are displayed in the left column, and lesions of the BLA are displayed in the right column. Sections are from -1.88, -2.30, -2.80, and -3.30 mm relative to bregma, from top to bottom, respectively, in the anteroposterior plane (adapted from Paxinos and Watson, 1998).

Figure 2.

Low-power photomicrograph showing, in a, a sham brain on which the major boundaries of the basolateral complex [comprising the basolateral and lateral amygdala (LA)] and of the CN have been marked along with the optic tract (opt) and external capsule (ec) as general landmarks, in b, a representative cell-body lesion of the basolateral complex, and in c, a representative cell-body lesion of the central nucleus. These coronal sections are all approximately -2.8 mm posterior to bregma.

Figure 3.

Experiment 1. A, Mean lever presses per minute (±1 SEM) across sessions of instrumental training averaged across the two instrumental actions for each of the lesion groups. B, Mean lever presses per minute in the 10 min extinction test (±1 SE of the difference of the means) conducted after selective devaluation of one of the instrumental outcomes. Devaluation was achieved using a specific-satiety procedure. Data are presented separately for the action that, in training, had delivered the now devalued outcome (Dev) and for the other action (Non) and for each of the lesioned groups.

Figure 4.

Experiment 1. Mean lever presses per minute in the 10 min rewarded devaluation test for each of the lesion groups (±1 SE of the difference of the means). Devaluation was achieved using a specific-satiety procedure as in the extinction test; however, performance of the two responses was rewarded with the outcomes that those responses had earned in training. Dev, Devalued; Non, nondevalued.

Figure 5.

Experiment 1. Consumption test of specific-satiety induced devaluation (±1SEof the difference of the means). Results are presented separately for consumption of the outcome that was the same as [devalued (Dev)] and different from [nondevalued (Non)] that outcome consumed immediately before the test phase and for each of the lesion groups.

Figure 6.

Experiment 1. Pavlovian conditioning and outcome-specific transfer. The left panel displays the mean number of magazine entries during the CS presentations and during the pre-CS intervals across days of pavlovian training for the three lesioned groups. The right panels display the mean number of lever presses per minute during the pavlovian-instrumental transfer test (±1 SE of the difference of the means). The number of responses during the baseline period was subtracted from the number of responses during the stimulus presentations to reveal the net excitatory effect of the stimuli. Same refers to the stimulus that predicts the same outcome as that delivered by the lever, whereas Different refers to the stimulus paired with the other outcome.

Figure 7.

Experiment 2. General versus outcome-specific transfer. The design of experiment 2 is presented at the top: S1, S2, S3 refer to the clicker, tone, and white noise stimuli; R1 and R2 refer to the left and right lever press actions; and O1, O2, and O3 refer to the pellet, 20% sucrose, and 20% polycose outcomes. The identity of the stimuli, actions, and outcomes was counterbalanced across subjects in each group. The bottom left panel displays the mean number of magazine entries during the CS presentations and during the pre-CS intervals across days of pavlovian training for the three lesioned groups. The right panels display the mean number of lever presses per minute during the pavlovian-instrumental transfer test separately for the outcome-specific CSs (i.e., S1 and S2 ± 1 SE of the difference of the means) and for the general excitatory stimulus (S3 ± 1 SEM). The number of responses during the baseline period was subtracted from the number of responses during the stimulus presentations to reveal transfer (i.e., the net excitatory effect of the stimuli over baseline). Same refers to the stimulus that predicts the same outcome as that delivered by the lever, Different refers to the stimulus paired with the other outcome, and General refers to the stimulus paired with the outcome that was not earned during instrumental training.