Searching for collective behavior in a network of real 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.Comment: 24 pages, 19 figure

Stimulus-dependent maximum entropy models of neural population codes

Neural populations encode information about their stimulus in a collective fashion, by joint activity patterns of spiking and silence. A full account of this mapping from stimulus to neural activity is given by the conditional probability distribution over neural codewords given the sensory input. To be able to infer a model for this distribution from large-scale neural recordings, we introduce a stimulus-dependent maximum entropy (SDME) model---a minimal extension of the canonical linear-nonlinear model of a single neuron, to a pairwise-coupled neural population. The model is able to capture the single-cell response properties as well as the correlations in neural spiking due to shared stimulus and due to effective neuron-to-neuron connections. Here we show that in a population of 100 retinal ganglion cells in the salamander retina responding to temporal white-noise stimuli, dependencies between cells play an important encoding role. As a result, the SDME model gives a more accurate account of single cell responses and in particular outperforms uncoupled models in reproducing the distributions of codewords emitted in response to a stimulus. We show how the SDME model, in conjunction with static maximum entropy models of population vocabulary, can be used to estimate information-theoretic quantities like surprise and information transmission in a neural population.Comment: 11 pages, 7 figure

The Computational Structure of Spike Trains

Neurons perform computations, and convey the results of those computations through the statistical structure of their output spike trains. Here we present a practical method, grounded in the information-theoretic analysis of prediction, for inferring a minimal representation of that structure and for characterizing its complexity. Starting from spike trains, our approach finds their causal state models (CSMs), the minimal hidden Markov models or stochastic automata capable of generating statistically identical time series. We then use these CSMs to objectively quantify both the generalizable structure and the idiosyncratic randomness of the spike train. Specifically, we show that the expected algorithmic information content (the information needed to describe the spike train exactly) can be split into three parts describing (1) the time-invariant structure (complexity) of the minimal spike-generating process, which describes the spike train statistically; (2) the randomness (internal entropy rate) of the minimal spike-generating process; and (3) a residual pure noise term not described by the minimal spike-generating process. We use CSMs to approximate each of these quantities. The CSMs are inferred nonparametrically from the data, making only mild regularity assumptions, via the causal state splitting reconstruction algorithm. The methods presented here complement more traditional spike train analyses by describing not only spiking probability and spike train entropy, but also the complexity of a spike train's structure. We demonstrate our approach using both simulated spike trains and experimental data recorded in rat barrel cortex during vibrissa stimulation.Comment: Somewhat different format from journal version but same conten

Supervised Parameter Estimation of Neuron Populations from Multiple Firing Events

The firing dynamics of biological neurons in mathematical models is often determined by the model's parameters, representing the neurons' underlying properties. The parameter estimation problem seeks to recover those parameters of a single neuron or a neuron population from their responses to external stimuli and interactions between themselves. Most common methods for tackling this problem in the literature use some mechanistic models in conjunction with either a simulation-based or solution-based optimization scheme. In this paper, we study an automatic approach of learning the parameters of neuron populations from a training set consisting of pairs of spiking series and parameter labels via supervised learning. Unlike previous work, this automatic learning does not require additional simulations at inference time nor expert knowledge in deriving an analytical solution or in constructing some approximate models. We simulate many neuronal populations with different parameter settings using a stochastic neuron model. Using that data, we train a variety of supervised machine learning models, including convolutional and deep neural networks, random forest, and support vector regression. We then compare their performance against classical approaches including a genetic search, Bayesian sequential estimation, and a random walk approximate model. The supervised models almost always outperform the classical methods in parameter estimation and spike reconstruction errors, and computation expense. Convolutional neural network, in particular, is the best among all models across all metrics. The supervised models can also generalize to out-of-distribution data to a certain extent.Comment: 31 page

Advancing models of the visual system using biologically plausible unsupervised spiking neural networks

Spikes are thought to provide a fundamental unit of computation in the nervous system. The retina is known to use the relative timing of spikes to encode visual input, whereas primary visual cortex (V1) exhibits sparse and irregular spiking activity – but what do these different spiking patterns represent about sensory stimuli? To address this question, I set out to model the retina and V1 using a biologically-realistic spiking neural network (SNN), exploring the idea that temporal prediction underlies the sensory transformation of natural inputs. Firstly, I trained a recurrently-connected SNN of excitatory and inhibitory units to predict the sensory future in natural movies under metabolic-like constraints. This network exhibited V1-like spike statistics, simple and complex cell-like tuning, and - advancing prior studies - key physiological and tuning differences between excitatory and inhibitory neurons. Secondly, I modified this spiking network to model the retina to explore its role in visual processing. I found the model optimized for efficient prediction to capture retina-like receptive fields and - in contrast to previous studies - various retinal phenomena, such as latency coding, response omissions, and motion-tuning properties. Notably, the temporal prediction model also more accurately predicts retinal ganglion cell responses to natural images and movies across various animal species. Lastly, I developed a new method to accelerate the simulation and training of SNNs, obtaining a 10-50 times speedup, with performance on a par with the standard training approach on supervised classification benchmarks and for fitting electrophysiological recordings of cortical neurons. The retina and V1 models lay the foundation for developing normative models of increasing biological realism and link sensory processing to spiking activity, suggesting that temporal prediction is an underlying function of visual processing. This is complemented by a new approach to drastically accelerate computational research using SNNs