Coherent cortical representations develop after experience via feedforward-recurrent circuit alignment

Abstract

Selective and reliable cortical sensory representations depend on synaptic interactions between feedforward inputs, conveying information from lower levels of the sensory pathway, and recurrent networks that reciprocally connect neurons functioning at the same hierarchical level. Here we explore the development of feedforward/recurrent interactions in primary visual cortex of the ferret that is responsible for the representation of orientation, focusing on the feedforward inputs from cortical layer 4 and its relation to the modular recurrent network in layer 2/3 before and after the onset of visual experience. Using simultaneous laminar electrophysiology and calcium imaging we found that in experienced animals, individual layer 4 and layer 2/3 neurons exhibit strongly correlated responses with the modular recurrent network structure in layer 2/3. Prior to experience, layer 2/3 neurons exhibit comparable modular correlation structure, but this correlation structure is missing for individual layer 4 neurons. Further analysis of the receptive field properties of layer 4 neurons in naive animals revealed that they exhibit very poor orientation tuning compared to layer 2/3 neurons at this age, and this is accompanied by the lack of spatial segregation of ON and OFF subfields, the definitive property of layer 4 simple cells in experienced animals. Analysis of the response dynamics of layer 2/3 neurons with whole-cell patch recordings confirms that individual layer 2/3 neurons in naive animals receive poorly-selective feedforward input that does not align with the orientation preference of the layer 2/3 responses. Further analysis reveals that the misaligned feedforward input is the underlying cause of reduced selectivity and increased response variability that is evident in the layer 2/3 responses of naive animals. Altogether, our experiments indicate that the onset of visual experience is accompanied by a critical refinement in the responses of layer 4 neurons and the alignment of feedforward and recurrent networks that increases the selectivity and reliability of the representation of orientation in V1.