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

Neurons within primary visual cortex (V1) possess stable firing rate set points to which they faithfully return when perturbed by passive sensory manipulations. Chronic recordings in vivo suggest that these set points are present early in postnatal development and are stable through adulthood, raising the possibility that once they are established, they are largely immutable. Here we challenge this idea, using an ethological, vision-dependent prey capture learning paradigm in juvenile (critical period) rats. Juvenile rats rapidly (in one day) became proficient at catching crickets. This learning was impaired when V1 was inactivated, and was accompanied by an increase in the number of binocular V1 (V1b) neurons with firing reliably tied to specific behavioral epochs during hunts, indicating that hunting drives rapid functional plasticity within V1b. Remarkably, this rapid learning set in motion a slow, state-dependent increase in V1b firing, that began after learning was complete and persisted for days. This upward firing rate plasticity was gradual, occurred selectively during wake states, and in L2/3 was driven by a TNF-dependent increase in excitatory synapses and excitatory synaptic charge onto pyramidal neurons - all features of homeostatic forms of plasticity within V1. Finally, TNF inhibition administered after learning was complete diminished this increase in excitability and impaired the retention of hunting skills. Taken together, these data suggest that naturalistic learning in juvenile animals co-opts homeostatic forms of plasticity to reset firing rate setpoints within V1b, in a process that facilitates skill consolidation.