Separating intrinsic interactions from extrinsic correlations in a network of sensory neurons

Correlations in sensory neural networks have both extrinsic and intrinsic origins. Extrinsic or stimulus correlations arise from shared inputs to the network and, thus, depend strongly on the stimulus ensemble. Intrinsic or noise correlations reflect biophysical mechanisms of interactions between neurons, which are expected to be robust to changes in the stimulus ensemble. Despite the importance of this distinction for understanding how sensory networks encode information collectively, no method exists to reliably separate intrinsic interactions from extrinsic correlations in neural activity data, limiting our ability to build predictive models of the network response. In this paper we introduce a general strategy to infer population models of interacting neurons that collectively encode stimulus information. The key to disentangling intrinsic from extrinsic correlations is to infer the couplings between neurons separately from the encoding model and to combine the two using corrections calculated in a mean-field approximation. We demonstrate the effectiveness of this approach in retinal recordings. The same coupling network is inferred from responses to radically different stimulus ensembles, showing that these couplings indeed reflect stimulus-independent interactions between neurons. The inferred model predicts accurately the collective response of retinal ganglion cell populations as a function of the stimulus.