The developmental emergence of reliable cortical representations

Abstract

The fundamental structure of cortical networks arises early in development before the onset of sensory experience. However, how endogenously generated networks respond to the onset of sensory experience and how they form mature sensory representations with experience remain unclear. In this study, we examined this ‘nature–nurture transform’ at the single-trial level using chronic in vivo calcium imaging in ferret visual cortex. At eye opening, visual stimulation evokes robust patterns of modular cortical network activity that are highly variable within and across trials, severely limiting stimulus discriminability. These initial stimulus-evoked modular patterns are distinct from spontaneous network activity patterns present before and at the time of eye opening. Within a week of normal visual experience, cortical networks develop low-dimensional, highly reliable stimulus representations that correspond with reorganized patterns of spontaneous activity. Using a computational model, we propose that reliable visual representations derive from the alignment of feedforward and recurrent cortical networks shaped by novel patterns of visually driven activity. Sensory experience transforms endogenously structured cortical networks with diverse and unreliable visual responses into reliable representations. This process is proposed to involve the alignment of feedforward and recurrent networks.