Neural activity exhibits dynamics that in addition to a behavior of interest also relate to other brain functions or internal states. Understanding how neural dynamics explain behavior requires dissociating behaviorally relevant and irrelevant dynamics, which is not achieved with current neural dynamic models as they are learned without considering behavior. We develop a novel preferential subspace identification (PSID) algorithm that models neural activity while dissociating and prioritizing its behaviorally relevant dynamics. Applying PSID to large-scale neural activity in two monkeys performing naturalistic 3D reach-and-grasps uncovered new features for neural dynamics. First, PSID revealed the behaviorally relevant dynamics to be markedly lower-dimensional than otherwise implied. Second, PSID discovered distinct rotational dynamics that were more predictive of behavior.Finally, PSID more accurately learned the behaviorally relevant dynamics for each joint and recording channel.PSID provides a general new tool to reveal behaviorally relevant neural dynamics that can otherwise go unnoticed.

Motor function depends on neural dynamics spanning multiple spatiotemporal scales of population activity, from spiking of neurons to larger-scale local field potentials (LFP). How multiple scales of low-dimensional population dynamics are related in control of movements remains unknown. Multiscale neural dynamics are especially important to study in naturalistic reach-and-grasp movements, which are relatively under-explored. We learn novel multiscale dynamical models for spike-LFP network activity in monkeys performing naturalistic reach-and-grasps. We show low-dimensional dynamics of spiking and LFP activity exhibited several principal modes, each with a unique decay-frequency characteristic. One principal mode dominantly predicted movements. Despite distinct principal modes existing at the two scales, this predictive mode was multiscale and shared between scales, and was shared across sessions and monkeys, yet did not simply replicate behavioral modes. Further, this multiscale mode’s decay-frequency explained behavior. We propose that multiscale, low-dimensional motor cortical state dynamics reflect the neural control of naturalistic reach-and-grasp behaviors.

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Inferring complex spatiotemporal dynamics in neural population activity is critical for investigating neural mechanisms and developing neurotechnology. These activity patterns are noisy observations of lower-dimensional latent factors and their nonlinear dynamical structure. A major unaddressed challenge is to model this nonlinear structure, but in a manner that allows for flexible inference, whether causally, non-causally, or in the presence of missing neural observations. We address this challenge by developing DFINE, a new neural network that separates the model into dynamic and manifold latent factors, such that the dynamics can be modeled in tractable form. We show that DFINE achieves flexible nonlinear inference across diverse behaviors and brain regions. Further, despite enabling flexible inference unlike prior neural network models of population activity, DFINE also better predicts the behavior and neural activity, and better captures the latent neural manifold structure. DFINE can both enhance future neurotechnology and facilitate investigations across diverse domains of neuroscience.

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