Ca2+-dependent phosphodiesterase 1 regulates the plasticity of striatal spiny projection neuron glutamatergic synapses

Cell Rep. 2024 Aug 27;43(8):114540. doi: 10.1016/j.celrep.2024.114540. Epub 2024 Jul 25.

Abstract

Long-term synaptic plasticity at glutamatergic synapses on striatal spiny projection neurons (SPNs) is central to learning goal-directed behaviors and habits. Our studies reveal that SPNs manifest a heterosynaptic, nitric oxide (NO)-dependent form of long-term postsynaptic depression of glutamatergic SPN synapses (NO-LTD) that is preferentially engaged at quiescent synapses. Plasticity is gated by Ca2+ entry through CaV1.3 Ca2+ channels and phosphodiesterase 1 (PDE1) activation, which blunts intracellular cyclic guanosine monophosphate (cGMP) and NO signaling. Both experimental and simulation studies suggest that this Ca2+-dependent regulation of PDE1 activity allows for local regulation of dendritic cGMP signaling. In a mouse model of Parkinson disease (PD), NO-LTD is absent because of impaired interneuronal NO release; re-balancing intrastriatal neuromodulatory signaling restores NO release and NO-LTD. Taken together, these studies provide important insights into the mechanisms governing NO-LTD in SPNs and its role in psychomotor disorders such as PD.

Keywords: CP: Neuroscience; L-type Ca(2+) channel; Parkinson's disease; autism; cGMP; low-threshold spiking interneuron; nitric oxide; phosphodiesterase; spiny projection neuron; striatum; synaptic plasticity.

MeSH terms

  • Animals
  • Calcium / metabolism
  • Corpus Striatum / metabolism
  • Cyclic GMP / metabolism
  • Cyclic Nucleotide Phosphodiesterases, Type 1* / metabolism
  • Glutamic Acid / metabolism
  • Long-Term Synaptic Depression / physiology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Neuronal Plasticity* / physiology
  • Neurons* / metabolism
  • Nitric Oxide / metabolism
  • Synapses* / metabolism

Substances

  • Cyclic Nucleotide Phosphodiesterases, Type 1
  • Nitric Oxide
  • Cyclic GMP
  • Glutamic Acid
  • Calcium