Inactivation of the central but not the basolateral nucleus of the amygdala disrupts learning in response to overexpectation of reward

Abstract

The amygdala is critical for associating predictive cues with primary rewarding and aversive outcomes. This is particularly evident in tasks in which information about expected outcomes is required for normal responding. Here we used a pavlovian overexpectation task to test whether outcome signaling by amygdala might also be necessary for changing those representations in the face of unexpected outcomes. Rats were trained to associate several different cues with a food reward. After learning, two of the cues were presented together, in compound, followed by the same reward. Before each compound training session, rats received infusions of 2,3-dioxo-6-nitro-1,2,3,4-tetrahydrobenzo[f]quinoxaline-7-sulfonamide or saline into either the basolateral (ABL) or central nucleus (CeN) of amygdala. We found that infusions into CeN abolished the normal decline in responding to the compounded cue in a later probe test, whereas infusions into ABL had no effect. These results are inconsistent with the proposal that signaling of information about expected outcomes by ABL contributes to learning, at least in this setting, and instead implicate the CeN in this process, perhaps attributable to the hypothesized involvement of this area in attention and variations in stimulus processing.

Figure 1.

Effect of inactivation of ABL or CeN on changes in behavior after overexpectation. Shown is the experimental timeline linking conditioning, compound conditioning, and probe phases to data from each phase. Top, middle, and bottom rows indicate results from control, ABLi, and CeNi groups, respectively. In timeline and figures, V1 is a visual cue (a cue light), A1, A2, and A3 are auditory cues (tone, white noise, and clicker, counterbalanced), and O1 and O2 are different flavored sucrose pellets (banana and grape, counterbalanced). Positions of cannulae within ABL or CeN are shown beneath the timeline for the rats that received PBS (gray dot) or NBQX (black dot) before each compound conditioning session. A, Percentage of responding to food cup during cue presentation across 10 d of conditioning. Gray, black, and white squares indicate A1, A2, and A3 cues, respectively. B, Percentage of responding to food cup during cue presentation across 4 d of compound training. Gray, black, and white squares indicate A1/V1, A2, and A3 cues, respectively. C, Percentage of responding to food cup during cue presentation in the probe test. Line graph shows responding across the eight trials, and the bar graph shows average responding in these eight trials. Gray, black, and white colors indicate A1, A2, and A3 cues, respectively (*p < 0.05 or better).