Rapid prey capture learning drives a slow resetting of network activity in rodent binocular visual cortex

Neocortical neurons possess stable firing rate set points to which they faithfully return when perturbed. These set points are established early and are stable through adulthood, suggesting they are immutable. Here we challenge this idea using an ethological vision-dependent prey capture learning paradigm in juvenile rats. This learning required visual cortex (V1), and enhanced tuning of V1 neurons to specific behavioral epochs. Chronic recordings revealed a slow, state-dependent increase in V1 firing that began after learning was complete and persisted for days. This upward firing rate plasticity was gradual, gated by wake states, and in L2/3 was driven by a TNFα-dependent increase in excitatory synapses onto pyramidal neurons – all features of homeostatic plasticity within V1. Finally, TNFα inhibition after learning reduced retention of hunting skills. Thus, naturalistic learning in juvenile animals co-opts homeostatic forms of plasticity to reset firing rate setpoints within V1, in a process that facilitates skill consolidation.