Fast sampling-based inference in balanced neuronal networks

Multiple lines of evidence support the notion that the brain performs probabilistic inference in multiple cognitive domains, including perception and decision making. There is also evidence that probabilistic inference may be implemented in the brain through the (quasi-)stochastic activity of neural circuits, producing samples from the appropriate posterior distributions, effectively implementing a Markov chain Monte Carlo algorithm. However, time becomes a fundamental bottleneck in such sampling-based probabilistic representations: the quality of inferences depends on how fast the neural circuit generates new, uncorrelated samples from its stationary distribution (the posterior). We explore this bottleneck in a simple, linear-Gaussian latent variable model, in which posterior sampling can be achieved by stochastic neural networks with linear dynamics. The well-known Langevin sampling (LS) recipe, so far the only sampling algorithm for continuous variables of which a neural implementation has been suggested, naturally fits into this dynamical framework. However, we first show analytically and through simulations that the symmetry of the synaptic weight matrix implied by LS yields critically slow mixing when the posterior is high-dimensional. Next, using methods from control theory, we construct and inspect networks that are optimally fast, and hence orders of magnitude faster than LS, while being far more biologically plausible. In these networks, strong - but transient - selective amplification of external noise generates the spatially correlated activity fluctuations prescribed by the posterior. Intriguingly, although a detailed balance of excitation and inhibition is dynamically maintained, detailed balance of Markov chain steps in the resulting sampler is violated, consistent with recent findings on how statistical irreversibility can overcome the speed limitation of random walks in other domains.