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Rapid cortical reorganization tracks goal-directed sensorimotor learning in real time

Anthony RenardiD, Georgios FoustoukosiD, Maya Iuga, Pol BechiD, Axel BisiiD, Robin F. DardiD, Sylvain CrochetiD, Carl C.H. PeterseniD

Abstract

Sensorimotor associations are typically thought to require days of training to consolidate in sensory cortex, yet adaptive behavior can emerge within minutes. Here, we developed a barrel cortex-dependent whisker-based detection task in which mice learned to associate a novel tactile whisker stimulus with reward within a single behavioral session. Longitudinal two-photon calcium imaging of layer 2/3 barrel cortex neurons revealed that reward-driven learning rapidly reorganized the neuronal representation of the whisker deflection within a single session. Population decoding tracked this transition trial-by-trial during learning with neuronal trajectories mirroring behavior. Critically, neurons that gained stimulus responsiveness across training preferentially took part in spontaneous reactivation events during learning, suggesting that online reactivations could act as a potential upstream selection mechanism. Our results suggest that reward-based learning evokes rapid sensory cortical reorganization on the timescale of minutes, which could be mediated by a concurrent reactivation-based mechanism driving plasticity.

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