Interpretation of correlated neural variability from models of feed-forward and recurrent circuits

Neural populations respond to the repeated presentations of a sensory stimulus with correlated variability. These correlations have been studied in detail, with respect to their mechanistic origin, as well as their influence on stimulus discrimination and on the performance of population codes. A number of theoretical studies have endeavored to link network architecture to the nature of the correlations in neural activity. Here, we contribute to this effort: in models of circuits of stochastic neurons, we elucidate the implications of various network architectures—recurrent connections, shared feed-forward projections, and shared gain fluctuations—on the stimulus dependence in correlations. Specifically, we derive mathematical relations that specify the dependence of population-averaged covariances on firing rates, for different network architectures. In turn, these relations can be used to analyze data on population activity. We examine recordings from neural populations in mouse auditory cortex. We find that a recurrent network model with random effective connections captures the observed statistics. Furthermore, using our circuit model, we investigate the relation between network parameters, correlations, and how well different stimuli can be discriminated from one another based on the population activity. As such, our approach allows us to relate properties of the neural circuit to information processing.Author summary: The response of neurons to a stimulus is variable across trials. A natural solution for reliable coding in the face of noise is the averaging across a neural population. The nature of this averaging depends on the structure of noise correlations in the neural population. In turn, the correlation structure depends on the way noise and correlations are generated in neural circuits. It is in general difficult to identify the origin of correlations from the observed population activity alone. In this article, we explore different theoretical scenarios of the way in which correlations can be generated, and we relate these to the architecture of feed-forward and recurrent neural circuits. Analyzing population recordings of the activity in mouse auditory cortex in response to sound stimuli, we find that population statistics are consistent with those generated in a recurrent network model. Using this model, we can then quantify the effects of network properties on average population responses, noise correlations, and the representation of sensory information.