Rapid value learning reveals generalized and context-dependent codes in frontal cortex

Abstract

Studying how the brain represents value spans distinct methods and training histories, from neuroimaging in task-naive humans to single-neuron recordings in extensively trained non-human primates. Similar findings across fields have encouraged the untested assumption that rapidly emerging and overtrained value representations are equivalent. Here we recorded single-neuron activity in anterior cingulate cortex (ACC) and orbitofrontal cortex (OFC) as macaques learned novel cue values and chose between novel and overtrained cues. Value responses emerged within 4-7 cue presentations, matching behavioural adaptation. Yet ACC and OFC used distinct codes. ACC encoded value in a common format that generalised across training history. OFC coding was more context-dependent, with distinct subpopulations recruited by choice experience. Choice novelty was also encoded independently of value before chosen value signals emerged. During learning, ACC responses shifted from overtrained secondary reinforcers to newly predictive cues. These findings establish the necessary (rapid acquisition) and sufficient (generalised format) conditions for comparing value representations across methods, species, and training histories.