Coincidence of cholinergic pauses, dopaminergic activation and depolarisation of spiny projection neurons drives synaptic plasticity in the striatum

John N. J. Reynolds (), Riccardo Avvisati, Paul D. Dodson, Simon D. Fisher, Manfred J. Oswald, Jeffery R. Wickens and Yan-Feng Zhang ()
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John N. J. Reynolds: University of Otago, School of Biomedical Sciences, Brain Health Research Centre
Riccardo Avvisati: University of Bristol
Paul D. Dodson: University of Bristol
Simon D. Fisher: University of Otago, School of Biomedical Sciences, Brain Health Research Centre
Manfred J. Oswald: University of Otago, School of Biomedical Sciences, Brain Health Research Centre
Jeffery R. Wickens: University of Otago, School of Biomedical Sciences, Brain Health Research Centre
Yan-Feng Zhang: University of Otago, School of Biomedical Sciences, Brain Health Research Centre

Nature Communications, 2022, vol. 13, issue 1, 1-9

Abstract: Abstract Dopamine-dependent long-term plasticity is believed to be a cellular mechanism underlying reinforcement learning. In response to reward and reward-predicting cues, phasic dopamine activity potentiates the efficacy of corticostriatal synapses on spiny projection neurons (SPNs). Since phasic dopamine activity also encodes other behavioural variables, it is unclear how postsynaptic neurons identify which dopamine event is to induce long-term plasticity. Additionally, it is unknown how phasic dopamine released from arborised axons can potentiate targeted striatal synapses through volume transmission. To examine these questions we manipulated striatal cholinergic interneurons (ChIs) and dopamine neurons independently in two distinct in vivo paradigms. We report that long-term potentiation (LTP) at corticostriatal synapses with SPNs is dependent on the coincidence of pauses in ChIs and phasic dopamine activation, critically accompanied by SPN depolarisation. Thus, the ChI pause defines the time window for phasic dopamine to induce plasticity, while depolarisation of SPNs constrains the synapses eligible for plasticity.

Date: 2022
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DOI: 10.1038/s41467-022-28950-0

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