Neuron
Volume 91, Issue 3, 3 August 2016, Pages 574-586
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Article
Spontaneous Synaptic Activation of Muscarinic Receptors by Striatal Cholinergic Neuron Firing

https://doi.org/10.1016/j.neuron.2016.06.021Get rights and content
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Highlights

  • Striatal cholinergic firing drives spontaneous muscarinic activation in MSNs

  • Paired recordings reveal unitary muscarinic events that occur without failure

  • Muscarinic receptors reliably encode physiological patterns of cholinergic firing

  • Cholinergic inputs onto MSNs are independent and exhibit high release probability

Summary

Cholinergic interneurons (CHIs) play a major role in motor and learning functions of the striatum. As acetylcholine does not directly evoke postsynaptic events at most striatal synapses, it remains unclear how postsynaptic cholinergic receptors encode the firing patterns of CHIs in the striatum. To examine the dynamics of acetylcholine release, we used optogenetics and paired recordings from CHIs and medium spiny neurons (MSNs) virally overexpressing G-protein-activated inwardly rectifying potassium (GIRK) channels. Due to the efficient coupling between endogenous muscarinic receptors and GIRK channels, we found that firing of individual CHIs resulted in monosynaptic spontaneous inhibitory post-synaptic currents (IPSCs) in MSNs. Paired CHI-MSN recordings revealed that the high probability of acetylcholine release at these synapses allowed muscarinic receptors to faithfully encode physiological activity patterns from individual CHIs without failure. These results indicate that muscarinic receptors in striatal output neurons reliably decode CHI firing.

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