Time-dependent maximum entropy model for populations of retinal ganglion cells

Abstract

The inverse Ising model is used in computational neuroscience to infer probability distributions of the synchronous activity of large neuronal populations. This method allows for finding the Boltzmann distribution with single neuron biases and pairwise interactions that maximizes the entropy and reproduces the empirical statistics of the recorded neuronal activity. Here we apply this strategy to large populations of retinal output neurons (ganglion cells) of different types, stimulated by multiple visual stimuli with their own statistics. The activity of retinal output neurons is driven by both the inputs from upstream neurons, which encode the visual information and reflect stimulus statistics, and the recurrent connections, which induce network effects. We first apply the standard inverse Ising model approach, and show that it accounts well for the systems collective behavior when the input visual stimulus has short-ranged spatial correlations, but fails for long-ranged ones. This happens because stimuli with long-ranged spatial correlations synchronize the activity of neurons over long distances. This effect cannot be accounted for by pairwise interactions, and so by the pairwise Ising model. To solve this issue, we apply a previously proposed framework that includes a temporal dependence in the single neurons biases to model how neurons are driven in time by the stimulus. Thanks to this addition, the stimulus effects are taken into account by the biases, and the pairwise interactions allow for characterizing the network effect in the population activity and for reproducing the structure of the recurrent functional connections in the retinal architecture. In particular, the inferred interactions are strong and positive only for nearby neurons of the same type. Inter-type connections are instead small and slightly negative. Therefore, the retinal architecture splits into weakly interacting subpopulations composed of strongly interacting neurons. Overall, this temporal framework fixes the problems of the standard, static, inverse Ising model and accounts for the systems collective behavior, for stimuli with either short or long-range correlations.