Fast synaptic transmission between striatal spiny projection neurons

Striatal inhibition plays an important role in models of cortex-basal ganglia function and is altered in many basal ganglia diseases. The gamma-aminobutyric acid ergic spiny projection neuron comprises >95% of striatal neurons, but despite strong anatomical evidence, the electrophysiological properties and functions of their local axon collaterals are unknown. We simultaneously recorded from adjacent spiny projection neurons (<5-10 microm) in whole-cell patch mode and demonstrated a fast synaptic connection between 2669 pairs in cortex-striatum-substantia nigra organotypic cultures and 538 pairs in acute striatal slices. The synapse, which was blocked by gamma-aminobutyric acid type A antagonists, displayed a wide range of failure rates, was depolarizing at rest, and reversed above -60 mV. Presynaptic bursts of action potentials were highly correlated with total postsynaptic depolarization at rest. Synaptic transmission was optimized for burst discharge >14 Hz and showed considerable short-term plasticity, including paired-pulse depression at intervals <25 ms, intraburst facilitation, and interburst augmentation. This activity-dependent collateral interaction provides the basis for a new class of basal ganglia models in which striatal neurons cooperate as well as compete during processing of cortical inputs.