Anticipatory organization of neural population dynamics speeds behavioral decisions

Abstract

Expectations guide behavior and shape sensory responses in single neurons, but their influence on population-level neural dynamics is unknown. Here, we employ a dynamical systems framework to examine the collective spiking activity of neuronal populations in the auditory forebrain of European starlings, a species of songbird, as they categorize natural song syllables while sensory expectations are manipulated. We show first that sensory-driven neural population spiking activity traces smooth, low-dimensional latent trajectories that closely reflect the identity of sensory signals. Like the stimulus-driven responses of single neurons, the geometry of the population trajectories is also modulated by expectation. In single neurons, expectation sharpens differences between responses to signals in the same category, but at the population-level the effect is opposite: expectation increases the similarity between responses to signals in the same category. To understand how population-level response dynamics can differ from those in single neurons, we develop (and test empirically) a dynamical model that relates spiking activity at these two biological scales. The model leverages response redundancy between neurons, a capacity we term degeneracy-enabled remapping, and enables the observed simultaneous expectation-dependent increases in the separability of single-neuron responses and decreases in the separability of population trajectories in the task-potent subspace, i.e., the population activity dimensions tied to behavioral categorization. Examining the relationship between expectation-modulated population trajectories and behavior in detail, we find that single-trial categorization errors are tied to drift in the trajectory toward the opposing task-potent manifold. This suggests that expectations help establish structured, hypothesis-dependent initial conditions that precede the target-driven population response. In support of this, both behavioral accuracy and behavioral reaction time are predicted by the direction of early population motion within the task-potent subspace. We conclude that expectation drives anticipatory organization of population response variability into a structured, behaviorally relevant geometry that pre-positions subsequent population activity on task-potent manifolds to support rapid, accurate, behavioral outcomes.