The amygdala is not necessary for unconditioned stimulus inflation after Pavlovian fear conditioning in rats

Abstract

The basolateral complex (BLA) and central nucleus (CEA) of the amygdala play critical roles in associative learning, including Pavlovian conditioning. However, the precise role for these structures in Pavlovian conditioning is not clear. Recent work in appetitive conditioning paradigms suggests that the amygdala, particularly the BLA, has an important role in representing the value of the unconditioned stimulus (US). It is not known whether the amygdala performs such a function in aversive paradigms, such as Pavlovian fear conditioning in rats. To address this issue, Experiments 1 and 2 used temporary pharmacological inactivation of the amygdala prior to a US inflation procedure to assess its role in revaluing shock USs after either overtraining (Experiment 1) or limited training (Experiment 2), respectively. Inactivation of the BLA or CEA during the inflation session did not affect subsequent increases in conditioned freezing observed to either the tone conditioned stimulus (CS) or the conditioning context in either experiment. In Experiment 3, NBQX infusions into the BLA impaired the acquisition of auditory fear conditioning with an inflation-magnitude US, indicating that the amygdala is required for associative learning with intense USs. Together, these results suggest that the amygdala is not required for revaluing an aversive US despite being required for the acquisition of fear to that US.

Figure 1.

Schematic representation of the locations of included cannula placements for the infusion of NBQX (●) or VEH (○) in the BLA for Experiment 1. (Coronal brain images adapted from Swanson [2004] and reprinted with permission from Academic Press ©2004.)

Figure 2.

Conditioned freezing during the overtraining session, inflation session, context, and tone tests (left to right, respectively) (Experiment 1). (A) Mean percentage of freezing (± SEM) during the 75-min overtraining session (15-trial blocks). (B) Mean percentage of freezing (± SEM) during the five-trial inflation session. For both line graphs, groups are denoted as follows: NBQX-INF group (○), VEH-INF group (□), NBQX-NoINF group (●), VEH-NoINF group (■). (C) Mean percentage of freezing (± SEM) across the 10-min context test. (D) Mean percentage of freezing (± SEM) during the two-trial tone test. Data are an average of freezing during the ITI periods. In both bar graphs, data are shown for INF groups (white bar) and the NoINF groups (black bar) within each drug type.

Figure 3.

Schematic representation of the locations of included cannula placements for the infusion of NBQX (closed) or VEH (open) in the BLA (circles) or CEA (squares) for Experiment 2. (Coronal brain images adapted from Swanson [2004] and reprinted with permission from Academic Press ©2004.)

Figure 4.

Conditioned freezing during the training session, inflation session, and tone test (left to right, respectively) (Experiment 2). (A) Mean percentage of freezing (± SEM) during the 10-trial (two-trial blocks) training session is shown for BLA-INF (○), CEA-INF (□), VEH-INF (△), BLA-NoINF (●), CEA-NoINF (■), and VEH-NoINF (▲). Conditioned freezing during the inflation session (Experiment 2). (B) Mean percentage of freezing (± SEM) during the five-trial inflation session for INF (○) and NoINF (●) for rats that received vehicle infusions (far left graph; collapsed across brain areas), NBQX infused into the BLA (middle graph), or NBQX infused into the CEA (right graph). Data are an average of freezing during the ITI periods. (C) Mean percentage of freezing (± SEM) during the two-trial tone test for the INF groups (white bars) and for the NoINF groups (black bar) within each drug group.

Figure 5.

Schematic representation of the locations of included cannula placements for the infusion of NBQX (●) or VEH (○) in the BLA for Experiment 3. (Coronal brain images adapted from Swanson [2004] and reprinted with permission from Academic Press ©2004.)

Figure 6.

Conditioned freezing during the training session, tone, and context tests (left to right, respectively) (Experiment 3). (A) Mean percentage of freezing (± SEM) during the 5-min training session. Groups are denoted as follows: NBQX (○),VEH (●). (B) Mean percentage of freezing (± SEM) during the 10-trial tone test. (C) Mean percentage of freezing (± SEM) across the 10-min context test. Data are an average of freezing during the ITI periods. In both bar graphs, data are shown for NBQX (white bar) and the VEH group (black bar).