Rapid emergence of latent knowledge in the sensory cortex drives learning

Abstract

Rapid learning confers significant advantages to 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 a gradual expansion of predictive 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 (AC) drives both rapid learning and slower performance gains but becomes dispensable at expert. Rather than enhancement or expansion of cue representations, two-photon calcium imaging of AC excitatory neurons throughout learning revealed two higher-order signals that were causal to learning and performance. First, a reward prediction (RP) signal emerged rapidly within tens of trials, was present after action-related errors only early in training, and faded at expert levels. Strikingly, silencing at the time of the RP signal impaired rapid learning, suggesting it serves an associative and teaching role. Second, a distinct cell ensemble encoded and controlled licking suppression that drove the slower performance improvements. These two ensembles were spatially clustered but uncoupled from underlying sensory representations, indicating a higher-order functional segregation within AC. 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.