Predictive and instructive cerebellar encoding of dopamine reward drives motivated behavior

To learn motivated behaviors, animals must both anticipate rewards and reinforce actions that yield them. Although cerebellar activity encodes natural rewards such as water and food, it also coordinates physical movements such as eating and drinking. To disentangle reward from consummatory movements, we trained mice to push for delayed dopamine (DA) rewards delivered directly into the brain.

Here we show that cerebellar input streams use both predictive and instructive codes for DA reward. Two-photon imaging revealed that many cerebellar granule cells (GrCs) predictively encoded DA rewards with sustained activity that ‘stretched’ to match 1-second or 2-second delay intervals before terminating upon reward receipt. By contrast, most cerebellar climbing fibers (CFs) spiked just after DA delivery.

In mice also trained with water rewards, encoding strength for DA matched or exceeded that for water. Both cell types contributed causally: chronic GrC inhibition disrupted self-stimulation learning, and CF self-stimulation ‘rewards’ drove moderate operant learning in naive animals. Thus, cerebellar encoding of DA reward helps drive motivated behavior, suggesting deeper cerebellar integration in brain reward prediction networks.

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