Rapid emergence of latent knowledge in the sensory cortex drives learning.

Rapid learning confers significant advantages on animals in ecological environments. Despite the need for speed, animals appear to only slowly learn to associate rewarded actions with predictive cues. This slow learning is thought to be supported by gradual changes to cue representation in the sensory cortex. However, evidence is growing that animals learn more rapidly than classical performance measures suggest, challenging the prevailing model of sensory cortical plasticity. Here we investigated the relationship between learning and sensory cortical representations. We trained mice on an auditory go/no-go task that dissociated the rapid acquisition of task contingencies (learning) from its slower expression (performance). Optogenetic silencing demonstrated that the auditory cortex drives both rapid learning and slower performance gains but becomes dispensable once mice achieve 'expert' performance. Instead of enhanced cue representations, two-photon calcium imaging of auditory cortical neurons throughout learning revealed two higher-order signals that were causal to learning and performance. A reward-prediction signal emerged rapidly within tens of trials, was present after action-related errors early in training, and faded in expert mice. Silencing at the time of this signal impaired rapid learning, suggesting that it serves an associative role. A distinct cell ensemble encoded and controlled licking suppression that drove slower performance improvements. These ensembles were spatially clustered but uncoupled from sensory representations, indicating higher-order functional segregation within auditory cortex. Our results reveal that the sensory cortex manifests higher-order computations that separably drive rapid learning and slower performance improvements, reshaping our understanding of the fundamental role of the sensory cortex.