Abstract
During developmental critical periods (CPs), the brain undergoes high levels of experience-dependent plasticity due to enhanced sensitivity to external stimuli. While classic sensory deprivation or alteration paradigms have been tremendously useful in characterizing visual CP plasticity mechanisms in visual cortex, how active learning remodels visual system circuitry during the visual CP to support behavioral function is still unknown. To address this, I used a naturalistic and ethological prey capture learning paradigm to assess how vision-dependent learning during the CP affects binocular visual cortex (V1b) and the superficial superior colliculus (sSC). I found that prey capture learning requires V1 and selectively remodels V1b excitatory circuitry, as perisomatic and dendritic inhibitory contacts remain unchanged after hunting. Furthermore, this rewiring is specific for feedback and recurrent connections supporting V1 computations, as spine density is unchanged in oblique dendrites of hunting mice, which receive predominantly feedforward visual input. Moreover, prey capture learning also increases excitatory input onto widefield (WF) cells in the sSC, a process stabilized by TNF⍺-dependent signaling and independent from V1, suggesting cooperative functions of cortical and subcortical pathways of visual processing. Thus, CP learning induces persistent excitatory structural plasticity in cortical and subcortical regions in the visual system to support adaptive, ethological behavior.