Development of coherent cortical responses reflects increased discriminability of feedforward inputs and their alignment with recurrent circuits

Sensory cortical areas guide behavior by transforming stimulus-driven inputs into reliable activity patterns. In the visual cortex, layer 4 (L4) neurons activated by the same edge orientation provide feedforward input to layers 2/3 (L2/3) modules sharing strong recurrent connections. This alignment facilitates selective amplification, driving a reliable, modular representation of orientation, but how it develops remains unclear. Using electrophysiology and calcium imaging, we find that in visually naive animals, L4-L2/3 coactivity lacks orientation specificity. One contributing factor is low orientation discriminability in L4, which improves with experience. However, computational modeling indicates that misaligned feedforward-recurrent interactions also play a critical role and predict developmental changes in tuning dynamics of sustained L2/3 responses, which we confirm with whole-cell recordings. Altogether, our study provides evidence that enhanced discriminability of L4 feedforward inputs and their alignment with recurrent L2/3 interactions following experience contribute to the development of reliable sensory representations with laminar-temporal coherence.