Learning enhances the relative impact of top-down processing in the visual cortex

Theories have proposed that in sensory cortices learning can enhance top-down modulation by higher brain areas while reducing bottom-up sensory inputs. To address circuit mechanisms underlying this process, we examined the activity of layer 2/3 (L2/3) excitatory neurons in the mouse primary visual cortex (V1) as well as L4 neurons, the main bottom-up source, and long-range top-down projections from the retrosplenial cortex (RSC) during associative learning over days using chronic two-photon calcium imaging. During learning, L4 responses gradually weakened, while RSC inputs became stronger. Furthermore, L2/3 acquired a ramp-up response temporal profile with learning, coinciding with a similar change in RSC inputs. Learning also reduced the activity of somatostatin-expressing inhibitory neurons (SOM-INs) in V1 that could potentially gate top-down inputs. Finally, RSC inactivation or SOM-IN activation was sufficient to partially reverse the learning-induced changes in L2/3. Together, these results reveal a learning-dependent dynamic shift in the balance between bottom-up and top-down information streams and uncover a role of SOM-INs in controlling this process.