The Central Nucleus of the Amygdala Encodes the Motivation to Pursue Ethanol

Abstract

Prior studies implicate the central nucleus of the amygdala (CeA) in reward motivation, yet how this region encodes motivation for ethanol (EtOH) seeking and consumption-and how this compares to encoding of natural rewards--remains poorly understood. We recorded single-unit neural activity from rats during a cued instrumental task in which lever insertion on each trial indicates the opportunity to lever press for ethanol and post-press lever retraction signals ethanol delivery. We found neurons responsive to multiple trial events (lever insertion and retraction cues, lever press, port entry, and reward licks), including neurons with rhythmic activity entrained to licking during EtOH consumption. Notably, CeA neural responses to the lever insertion cue at trial start encoded both the likelihood and speed of engagement during reward seeking. Using a supervised classifier, we found that trial engagement and motivation level could be decoded from pre-trial and lever insertion response periods. Finally, we assessed whether these effects generalized to natural reward seeking. Sucrose-rewarded rats (both ethanol-exposed and ethanol-naive) showed higher motivation (more rewards earned and shorter first-press latencies) and stronger CeA recruitment and responses at lever insertion than ethanol-rewarded rats, in agreement with the notion that CeA circuits amplify reward-predictive cue signals to facilitate rapid action initiation under high motivational states. Together, these findings indicate that CeA neurons dynamically encode motivational states, with tonic activity and reward-predictive cue responses predicting both engagement in reward seeking and the vigor of action initiation. We suggest these patterns of neural activity drive ethanol and sucrose pursuit. Significance StatementHow motivational states drive reward-seeking is a central question in systems neuroscience, yet the mechanisms linking neural signals to action initiation remain poorly understood. Recording single-unit activity in the amygdala central nucleus (CeA) during cued ethanol self-administration revealed that neural responses to reward-predictive cues encoded both the decision to engage in reward seeking and the vigor of action initiation, and motivational state was decoded from cue-evoked signals and tonic activity even before cue presentation. Consistent with greater motivation for the more palatable sucrose reward, CeA neurons showed stronger cue responses and greater anticipatory firing preceding tongue contact with reward, compared with ethanol-rewarded rats. These findings identify CeA activity patterns that link motivational state to the rapid initiation of goal-directed action.