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Modern neural interfaces allow access to the activity of up to a million neurons within brain circuits. However, bandwidth limits often create a trade-off between greater spatial sampling (more channels or pixels) and the temporal frequency of sampling. Here we demonstrate that it is possible to obtain spatio-temporal super-resolution in neuronal time series by exploiting relationships among neurons, embedded in latent low-dimensional population dynamics. Our novel neural network training strategy, selective backpropagation through time (SBTT), enables learning of deep generative models of latent dynamics from data in which the set of observed variables changes at each time step. The resulting models are able to infer activity for missing samples by combining observations with learned latent dynamics. We test SBTT applied to sequential autoencoders and demonstrate more efficient and higher-fidelity characterization of neural population dynamics in electrophysiological and calcium imaging data. In electrophysiology, SBTT enables accurate inference of neuronal population dynamics with lower interface bandwidths, providing an avenue to significant power savings for implanted neuroelectronic interfaces. In applications to two-photon calcium imaging, SBTT accurately uncovers high-frequency temporal structure underlying neural population activity, substantially outperforming the current state-of-the-art. Finally, we demonstrate that performance could be further improved by using limited, high-bandwidth sampling to pretrain dynamics models, and then using SBTT to adapt these models for sparsely-sampled data. 

Continuing advances in neural interfaces have enabled simultaneous monitoring of spiking activity from hundreds to thousands of neurons. To interpret these large-scale data, several methods have been proposed to infer latent dynamic structure from high-dimensional datasets. One recent line of work uses recurrent neural networks in a sequential autoencoder (SAE) framework to uncover dynamics. SAEs are an appealing option for modeling nonlinear dynamical systems, and enable a precise link between neural activity and behavior on a single-trial basis. However, the very large parameter count and complexity of SAEs relative to other models has caused concern that SAEs may only perform well on very large training sets. We hypothesized that with a method to systematically optimize hyperparameters (HPs), SAEs might perform well even in cases of limited training data. Such a breakthrough would greatly extend their applicability. However, we find that SAEs applied to spiking neural data are prone to a particular form of overfitting that cannot be detected using standard validation metrics, which prevents standard HP searches. We develop and test two potential solutions: an alternate validation method (“sample validation”) and a novel regularization method (“coordinated dropout”). These innovations prevent overfitting quite effectively, and allow us to test whether SAEs can achieve good performance on limited data through large-scale HP optimization. When applied to data from motor cortex recorded while monkeys made reaches in various directions, large-scale HP optimization allowed SAEs to better maintain performance for small dataset sizes. Our results should greatly extend the applicability of SAEs in extracting latent dynamics from sparse, multidimensional data, such as neural population spiking activity. 

Advances in neural recording present increasing opportunities to study neural activity in unprecedented detail. Latent variable models (LVMs) are promising tools for analyzing this rich activity across diverse neural systems and behaviors, as LVMs do not depend on known relationships between the activity and external experimental variables. However, progress with LVMs for neuronal population activity is currently impeded by a lack of standardization, resulting in methods being developed and compared in an ad hoc manner. To coordinate these modeling efforts, we introduce a benchmark suite for latent variable modeling of neural population activity. We curate four datasets of neural spiking activity from cognitive, sensory, and motor areas to promote models that apply to the wide variety of activity seen across these areas. We identify unsupervised evaluation as a common framework for evaluating models across datasets, and apply several baselines that demonstrate benchmark diversity. We release this benchmark through EvalAI. http://neurallatents.github.io/