Approximate Inference for Time-Varying Interactions and Macroscopic Dynamics of Neural Populations

The models in statistical physics such as an Ising model offer a convenient way to characterize stationary activity of neural populations. Such stationary activity of neurons may be expected for recordings from in vitro slices or anesthetized animals. However, modeling activity of cortical circuitries of awake animals has been more challenging because both spike-rates and interactions can change according to sensory stimulation, behavior, or an internal state of the brain. Previous approaches modeling the dynamics of neural interactions suffer from computational cost; therefore, its application was limited to only a dozen neurons. Here by introducing multiple analytic approximation methods to a state-space model of neural population activity, we make it possible to estimate dynamic pairwise interactions of up to 60 neurons. More specifically, we applied the pseudolikelihood approximation to the state-space model, and combined it with the Bethe or TAP mean-field approximation to make the sequential Bayesian estimation of the model parameters possible. The large-scale analysis allows us to investigate dynamics of macroscopic properties of neural circuitries underlying stimulus processing and behavior. We show that the model accurately estimates dynamics of network properties such as sparseness, entropy, and heat capacity by simulated data, and demonstrate utilities of these measures by analyzing activity of monkey V4 neurons as well as a simulated balanced network of spiking neurons.Author Summary: Simultaneous analysis of large-scale neural populations is necessary to understand coding principles of neurons because they concertedly process information. Methods of thermodynamics and statistical mechanics are useful to understand collective phenomena of the interacting elements, and they have been successfully used to understand diverse activity of neurons. However, most analysis methods assume stationary data, in which activity rates of neurons and their correlations are constant over time. This assumption is easily violated in the data recorded from awake animals. Neural correlations likely organize dynamically during behavior and cognition, and this may be independent from the modulated activity rates of individual neurons. Recently several methods were proposed to simultaneously estimate dynamics of neural interactions. However, these methods are applicable to up to about 10 neurons. Here by combining multiple analytic approximation methods, we made it possible to estimate time-varying interactions of much larger neural populations. The method allows us to trace dynamic macroscopic properties of neural circuitries such as sparseness, entropy, and sensitivity. Using these statistics, researchers can now quantify to what extent neurons are correlated or de-correlated, and test if neural systems are susceptible within a specific behavioral period.