Rapid emergence of latent knowledge in the sensory cortex drives learning

Abstract

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 cues1–4. This slow learning is thought to be supported by gradual changes to cue representation in the sensory cortex2,5. However, evidence is growing that animals learn more rapidly than classical performance measures suggest6,7, 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)7. 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 representations8, 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. In mice, learning and performance on an auditory task is driven by higher-order signals in the auditory cortex that are no longer required when the mouse has achieved expert-level performance.