Cerebellar neural populations orchestrate dopamine reward signaling with single-trial precision.

Abstract

Reward-based learning requires neural circuits to rapidly register outcomes and adapt behavior, yet how subcortical circuits contribute to temporally precise reward signaling remains elusive. Here, we identify a cerebellar mechanism encoding rewards with single-trial precision. Utilizing cleared-tissue tractography, electrophysiology, and two-photon imaging in a mouse foraging task, we describe a brief population silencing in the deep cerebellar nucleus (DCN), termed instantaneous population silencing (IPS), triggered by synchronized activity of Purkinje cells (PCs). This transient silencing emerges 100 ms after reward, scales with reward prediction errors, and induces rebound phasic firing of ventral tegmental area (VTA) dopamine neurons. Such single-trial temporal accuracy enabled precise reward control via PC-to-DCN or DCN-to-VTA projections. A single 5-ms optogenetic pulse suffices to elicit one IPS and corresponding phasic VTA response, shifting behavior with single-trial precision. Our findings underscore the cerebellum's role in real-time reward coding, illustrating how population dynamics achieve temporal and single-event precision.