Neural correlates in basolateral and central amygdala during reward seeking in the face of punishment

The inability to suppress actions despite adverse consequences is a hallmark of compulsive behaviors and is amygdala dependent. To study the amygdala’s role in responding despite adverse consequences, we compared single-unit activity in the basolateral (BLA) or central (CeA) amygdala before and after reward-seeking under punishment threat.

Rats started each trial by pressing an initial lever, which triggered an outcome-specific 5-s auditory cue (white noise, pure tone, or clicker), signaling one of three reinforcement conditions: 100% sucrose reward, 20% reward/80% omission, or 80% reward/20% footshock punishment. Next, the active and inactive levers were extended, and pressing on the active lever terminated the auditory cue and triggered an outcome-specific 1-s visual cue predicting either reward, reward omission, or shock. After training, we implanted eight tetrodes in the BLA (n=7) or CeA (n=5) and recorded single-unit activity of ∼100 neurons per region during task performance.

CeA neurons, and to a lesser extent BLA neurons, responded differently to the distinct auditory cues and outcomes. The discrimination between conditions partially explained the capacity of neuronal activity to predict the latency to lever press to complete the trial. The failure to suppress reward-seeking behavior in the face of punishment coincided with the reactivation of reward-seeking-sensitive and the loss of inhibition of punishment-sensitive neuronal populations.

In conclusion, we found that after extended training, opposing populations of activated and inhibited neurons in CeA, and to a lesser extent in BLA, control completion of reward-seeking despite punishment.