The Emergence of Cortical Representations

The internal and external world is thought to be represented by distributed patterns of cortical activity. The emergence of these cortical representations over the course of development remains an unresolved question. In this talk, I share results from a series of recent studies combining theory and experiments in the cortex of the ferret, a species with a well-defined columnar organization and modular network of orientation-selective responses in visual cortex. I show that prior to the onset of structured sensory experience, endogenous mechanisms set up a highly organized cortical network structure that is evident in modular patterns of spontaneous activity characterized by strong, clustered local and long-range correlations. This correlation structure is remarkably consistent across both sensory and association areas in the early neocortex, suggesting that diverse cortical representations initially develop according to similar principles. Next, I explore a classical candidate mechanism for producing modular activity – local excitation and lateral inhibition. I present the first empirical test of this mechanism through direct optogenetic cortical activation and discuss a plausible circuit implementation. Then, focusing on the visual cortex, I demonstrate that these endogenously structured networks enable orientation-selective responses immediately after eye opening. However, these initial responses are highly variable, lacking the reliability and low-dimensional structure observed in the mature cortex. Reliable responses are achieved after an experience-dependent co-reorganization of stimulus- evoked and spontaneous activity following eye opening. Based on these observations, I propose the hypothesis that the alignment between feedforward inputs and the recurrent network plays a crucial role in transforming the initially variable responses into mature and reliable representations.