Modeling and inference methods for switching regime-dependent dynamical systems with multiscale neural observations

Abstract

Objective. Realizing neurotechnologies that enable long-term neural recordings across multiple spatial-temporal scales during naturalistic behaviors requires new modeling and inference methods that can simultaneously address two challenges. First, the methods should aggregate information across all activity scales from multiple recording sources such as spiking and field potentials. Second, the methods should detect changes in the regimes of behavior and/or neural dynamics during naturalistic scenarios and long-term recordings. Prior regime detection methods are developed for a single scale of activity rather than multiscale activity, and prior multiscale methods have not considered regime switching and are for stationary cases. Approach. Here, we address both challenges by developing a switching multiscale dynamical system model and the associated filtering and smoothing methods. This model describes the encoding of an unobserved brain state in multiscale spike-field activity. It also allows for regime-switching dynamics using an unobserved regime state that dictates the dynamical and encoding parameters at every time-step. We also design the associated switching multiscale inference methods that estimate both the unobserved regime and brain states from simultaneous spike-field activity. Main results. We validate the methods in both extensive numerical simulations and prefrontal spike-field data recorded in a monkey performing saccades for fluid rewards. We show that these methods can successfully combine the spiking and field potential observations to simultaneously track the regime and brain states accurately. Doing so, these methods lead to better state estimation compared with single-scale switching methods or stationary multiscale methods. Also, for single-scale linear Gaussian observations, the new switching smoother can better generalize to diverse system settings compared to prior switching smoothers. Significance. These modeling and inference methods effectively incorporate both regime-detection and multiscale observations. As such, they could facilitate investigation of latent switching neural population dynamics and improve future brain-machine interfaces by enabling inference in naturalistic scenarios where regime-dependent multiscale activity and behavior arise.