Searching for Collective Behavior in a Large Network of Sensory Neurons

Maximum entropy models are the least structured probability distributions that exactly reproduce a chosen set of statistics measured in an interacting network. Here we use this principle to construct probabilistic models which describe the correlated spiking activity of populations of up to 120 neurons in the salamander retina as it responds to natural movies. Already in groups as small as 10 neurons, interactions between spikes can no longer be regarded as small perturbations in an otherwise independent system; for 40 or more neurons pairwise interactions need to be supplemented by a global interaction that controls the distribution of synchrony in the population. Here we show that such “K-pairwise” models—being systematic extensions of the previously used pairwise Ising models—provide an excellent account of the data. We explore the properties of the neural vocabulary by: 1) estimating its entropy, which constrains the population's capacity to represent visual information; 2) classifying activity patterns into a small set of metastable collective modes; 3) showing that the neural codeword ensembles are extremely inhomogenous; 4) demonstrating that the state of individual neurons is highly predictable from the rest of the population, allowing the capacity for error correction.Author Summary: Sensory neurons encode information about the world into sequences of spiking and silence. Multi-electrode array recordings have enabled us to move from single units to measuring the responses of many neurons simultaneously, and thus to ask questions about how populations of neurons as a whole represent their input signals. Here we build on previous work that has shown that in the salamander retina, pairs of retinal ganglion cells are only weakly correlated, yet the population spiking activity exhibits large departures from a model where the neurons would be independent. We analyze data from more than a hundred salamander retinal ganglion cells and characterize their collective response using maximum entropy models of statistical physics. With these models in hand, we can put bounds on the amount of information encoded by the neural population, constructively demonstrate that the code has error correcting redundancy, and advance two hypotheses about the neural code: that collective states of the network could carry stimulus information, and that the distribution of neural activity patterns has very nontrivial statistical properties, possibly related to critical systems in statistical physics.