Dataset for: A silent eligibility trace enables dopamine dependent synaptic plasticity for reinforcement learning in the mouse striatum

Learning from positive reinforcement is essential for adaptive behavior. Dopamine dependent synaptic plasticity is a candidate mechanism. Computational models of reinforcement learning assume a silent eligibility trace, initiated by synaptic activity, and transformed into plastic changes by later action of dopamine. To investigate test this hypothesis experimentally, we measured time-dependent modulation of synaptic plasticity by dopamine in adult mouse striatum using whole-cell recording. Experiments focused on synapses of dopamine D1 receptor expressing spiny projection neurons. Presynaptic activity followed by postsynaptic action potentials (pre-post) caused spike-time dependent long-term depression in D1-expressing neurons. Applying a dopamine D1 receptor agonist during induction of spike-time dependentpre-post plasticity caused long-term potentiation. This long-term potentiation was masked by long-term depression occurring concurrently, and was unmasked when long-term depression was blocked by calcium channel antagonists. LLong-term potentiation was blocked by a Ca2+-permeable AMPA receptor antagonist but not by an NMDA antagonist. Spike-time dependent plasticity-inducingPre-post stimulation caused transient elevation of rectification – a marker for expression of Ca2+-permeable AMPA receptors – for two to four seconds after stimulation. Importantly, as a direct test of the eligibility trace hypothesis, dopamine was uncaged at specific time-points before and after pre- and post-synaptic conjunction of activity. Dopamine caused potentiation selectively at synapses that were active two seconds before dopamine release, but not at earlier or later times. Our results provide direct evidence for a synaptic eligibility trace in the synapses of striatal neurons, based on a novel dopamine timing dependent plasticity mechanism.