Dissociating task acquisition from expression during learning reveals latent knowledge

SUMMARY Performance on cognitive tasks during learning is used to measure intelligence, yet it remains controversial since such testing is susceptible to contextual factors. To what extent does performance during learning depend on the testing context, rather than underlying knowledge? We trained mice, rats and ferrets on a range of tasks to examine how testing context impacts the acquisition of knowledge versus its expression. We interleaved reinforced trials with “probe” trials in which we omitted reinforcement. Across tasks, each animal species performed remarkably better in probe trials during learning and inter-animal variability was strikingly reduced. Reinforcement feedback is thus critical for learning-related plasticity but, paradoxically, masks the expression of underlying knowledge. We capture these results with a network model in which learning occurs during reinforced trials while context modulates only the read-out parameters. Probing learning by omitting reinforcement thus uncovers latent knowledge and identifies context—not “smartness”—as the major source of individual variability. HIGHLIGHTS Knowledge acquisition and expression can be segregated by the introduction of non-reinforced probe trials across a variety of animal species and behavioral tasks. Animals learn much faster and in a more stereotyped way in non-reinforced probe trials than their performance in the presence of reinforcement suggests. Underperformance and variability in performance arise from sensitivity to the behavioral testing context, not acquisition of sensorimotor associations. A circuit model accounts for context-dependent performance by modulating the integration of sensorimotor associations. eTOC Kuchibhotla et al. show the acquisition and expression of knowledge can be behaviorally dissociated in mice, rats, and ferrets across a variety of sensorimotor tasks. Across animals, variability in performance arises from the testing context, not underlying aptitude.