The dynamics and geometry of choice in premotor cortex.

The brain represents sensory variables in the coordinated activity of neural populations, in which tuning curves of single neurons define the geometry of the population code. Whether the same coding principle holds for dynamic cognitive variables remains unknown because internal cognitive processes unfold with a unique time course on single trials observed only in the irregular spiking of heterogeneous neural populations. Here we show the existence of such a population code for the dynamics of choice formation in the primate premotor cortex. We developed an approach to simultaneously infer population dynamics and tuning functions of single neurons to the population state. Applied to spike data recorded during decision-making, our model revealed that populations of neurons encoded the same dynamic variable predicting choices, and heterogeneous firing rates resulted from the diverse tuning of single neurons to this decision variable. The inferred dynamics indicated an attractor mechanism for decision computation. Our results reveal a common geometric principle for neural encoding of sensory and dynamic cognitive variables.

A unifying perspective on neural manifolds and circuits for cognition.

Two different perspectives have informed efforts to explain the link between the brain and behaviour. One approach seeks to identify neural circuit elements that carry out specific functions, emphasizing connectivity between neurons as a substrate for neural computations. Another approach centres on neural manifolds - low-dimensional representations of behavioural signals in neural population activity - and suggests that neural computations are realized by emergent dynamics. Although manifolds reveal an interpretable structure in heterogeneous neuronal activity, finding the corresponding structure in connectivity remains a challenge. We highlight examples in which establishing the correspondence between low-dimensional activity and connectivity has been possible, unifying the neural manifold and circuit perspectives. This relationship is conspicuous in systems in which the geometry of neural responses mirrors their spatial layout in the brain, such as the fly navigational system. Furthermore, we describe evidence that, in systems in which neural responses are heterogeneous, the circuit comprises interactions between activity patterns on the manifold via low-rank connectivity. We suggest that unifying the manifold and circuit approaches is important if we are to be able to causally test theories about the neural computations that underlie behaviour.

Learning non-stationary Langevin dynamics from stochastic observations of latent trajectories.

Many complex systems operating far from the equilibrium exhibit stochastic dynamics that can be described by a Langevin equation. Inferring Langevin equations from data can reveal how transient dynamics of such systems give rise to their function. However, dynamics are often inaccessible directly and can be only gleaned through a stochastic observation process, which makes the inference challenging. Here we present a non-parametric framework for inferring the Langevin equation, which explicitly models the stochastic observation process and non-stationary latent dynamics. The framework accounts for the non-equilibrium initial and final states of the observed system and for the possibility that the system's dynamics define the duration of observations. Omitting any of these non-stationary components results in incorrect inference, in which erroneous features arise in the dynamics due to non-stationary data distribution. We illustrate the framework using models of neural dynamics underlying decision making in the brain.

Moving beyond generalization to accurate interpretation of flexible models.

Machine learning optimizes flexible models to predict data. In scientific applications, there is a rising interest in interpreting these flexible models to derive hypotheses from data. However, it is unknown whether good data prediction guarantees accurate interpretation of flexible models. Here we test this connection using a flexible, yet intrinsically interpretable framework for modelling neural dynamics. We find that many models discovered during optimization predict data equally well, yet they fail to match the correct hypothesis. We develop an alternative approach that identifies models with correct interpretation by comparing model features across data samples to separate true features from noise. We illustrate our findings using recordings of spiking activity from the visual cortex of behaving monkeys. Our results reveal that good predictions cannot substitute for accurate interpretation of flexible models and offer a principled approach to identify models with correct interpretation.