Visual experience exerts an instructive role on cortical feedback inputs to the primary visual cortex

Contextual modulations in the primary visual cortex (V1) critically depend on feedback (FB) connections linking high-order cortical areas with lower-order ones and reflect natural image statistics. FB projections may encode learned statistical regularities of the environment through their connectivity and tuning, enabling context-dependent modulation of cortical activity. However, it remains unknown if the properties of FB connections reflect experienced visual statistics. Here, we used dual-color two-photon imaging to measure the tuning properties and retinotopic organization of inputs from the lateromedial (LM) visual area in layer 1 of V1 in mice reared wearing goggles that limit their visual experience to a narrow range of orientations. We found that the manipulation biased the orientation tuning and the major axis of the receptive fields of LM inputs toward the experienced orientations. The tuning-dependent retinotopic specificity of FB inputs was different in mice exposed to distinct orientations. We could recapitulate the effects of goggle rearing in a model in which Hebbian plasticity modifies the synaptic weights of V1 inputs in LM, while those of FB inputs are shaped by anti-Hebbian plasticity. Our results support an instructive role for visual experience in shaping both the functional properties and the organization of FB inputs and are consistent with the possibility that ascending and descending cortical pathways follow distinct plasticity rules. They also suggest the circuit mechanisms through which cortical circuits might learn and encode statistical regularities of the environment.