Anticipatory organization of neural population dynamics speeds behavioral decisions.

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